American Journal of Botany 101(11): 1821–1835, 2014.

AJB CENTENNIAL REVIEW

THE PLASTOCHRON INDEX: STILL USEFUL AFTER NEARLY SIX DECADES1

ROGER D. MEICENHEIMER2 Department of Biology, Miami University, Oxford, Ohio 45056 USA The plastochron index (PI) introduced by Erickson and Michelini in 1957 provides a solution to a long-standing problem, of how to measure time in growing plant populations, such that the occurrence of critical developmental events can be more readily detected, compared, and analyzed, than if chronologic time is used. The PI reduces the rather large variation associated with chronologic time in measuring such events by taking advantage of the growth characteristics of stem organs that repeat at regular intervals (the plastochron) and has found widespread application in botanical research. The original formulation and derivation of the PI and associated leaf plastochron index (LPI) is reviewed. Additional formulations that have been developed to overcome some of the limitations of the original PI formulation are examined. Major advancements that have been achieved in understanding the physiology, growth, and development of agriculturally important and current model plant species are reviewed to illustrate how various researchers have used the PI in such studies. Potential uses to which the PI and LPI might be applied in emerging frontiers of plant science are suggested. A searchable bibliography of most all the primary research studies that cite the original PI article is provided. Key words: Arabidopsis; Glycine; Linum; Lycoperiscon; Nicotiana; Pisum; plant growth and development; plastochron index; Populus; Xanthium.

Given the nature of scientific inquiry, there are relatively few concepts that long withstand the onslaught of relentless technological developments over extended periods of time. The plastochron index (PI) introduced by Erickson and Michelini in 1957 is one such concept, which provided a solution to a longstanding problem, of how to measure time in growing plant populations, such that the occurrence of critical developmental events could more readily be detected, compared, and analyzed. That this ground-breaking concept was originally published in the American Journal of Botany, now in its centenary year of publication, is significant since that venue, undoubtedly, was instrumental in its widespread dissemination and adoption by plant scientists throughout the world. To assess the depth of this impact, I analyzed Web of Science (WOS) resources that revealed the original Erickson and Michelini (1957) article has been directly cited in over 400 research papers published by authors from 29 nations, working in 20 different WOS research areas, at an average frequency of ca. 10 citations/year from 1965–2013. While these direct citations were most prevalent in plant science (66%), agriculture (17%), and environmental science/ecology (14%), they also included such diverse research areas as oceanography and marine/freshwater biology, food science, biotechnology, molecular, cellular, developmental, and evolutionary biology. 1 Manuscript received 2 September 2014; revision accepted 22 September 2014. The author thanks the Editor-in-Chief of the American Journal of Botany, Dr. Judy Jernstedt, for inviting this contribution. Insightful and helpful comments by anonymous reviewers are gratefully acknowledged. This paper is dedicated to the memory of Professor Ralph O. Erickson (1914–2006). 2 E-mail: [email protected]

doi:10.3732/ajb.1400305

In addition, the original article has been cited in 15 WOS review articles (Erickson, 1976; Jennings, 1976; Cordero and Gunckel, 1982; Dale, 1988; Sinha et al., 1993; Barlow, 1994; Ballach, 1997; Duarte et al., 1994; Lord et al., 1994; McMaster, 1997; Prusinkiewicz, 1998; McMaster, 2005; Venema et al., 2005; Gould et al., 2007; Rowan and Bendich, 2009) to which we can add an additional, perhaps most highly pertinent review relative to this account, that by Lamoreaux et al. (1978). Because that review was also published in the American Journal of Botany, I have primarily confined my discussion to the utilization, improvements, and advancements that have been made to the PI from 1976 onward. For those readers, who might wish to delve into the species and research areas not covered in this review, Appendix S1 (see Supplemental Data with the online version of this article) contains a searchable, complete bibliography of the 433 papers that cite the original article. The organization of this review of the PI, after 58 yr of use, is first to recapitulate the essential criteria for derivation and formulation of a plastochron index. Solutions to several of the initial limitations of the original PI formulation are then identified. Major advancements that have been achieved in understanding the physiology, growth, and development of agriculturally important and current model plant species are reviewed to illustrate how various researchers have used the PI in such studies. The value of the PI to developmental studies on current model plant taxa is assessed and a projection of how the PI might be used in future refinement of such studies suggested. DEFINITION OF A PLASTOCHRON History— Given that studies of biological development involve consideration of how organic form and content of organisms change over time, it is essential to have a reliable clock

American Journal of Botany 101(11): 1821–1835, 2014; http://www.amjbot.org/ © 2014 Botanical Society of America

1821

1822

AMERICAN JOURNAL OF BOTANY

with which to measure such change. The units of such a clock should be consistently applicable among organisms within a population and should yield the same measure of time among such organisms. Utilization of a clock that measures time in familiar chronologic units is problematic when studying plant growth and development since in a given population one observes, even under the most uniform environmental conditions possible, stochastic variation with regard to the onset of seed germination and that variance continues as growth of the individual plant bodies within the population progresses. Because of this initial variation, measures of developmental events within a population of plants will be associated with extremely wide variances if chronologic time is used to track these events. Fifty-eight years ago, Ralph Erickson and Francis Michelini (1957) proposed an alternative clock that has found wide use in studies on plant stem development. The unit of the Erickson and Michelini clock is the plastochron, a concept that was initially proposed by Askenasy (1880) during his studies on filamentous Charaphylaceae growth. Askenasy coined the term plastochron to refer to the time that elapsed between initiation of two successive internode cells of Nitella. Esau (1953) attributed Schmidt (1924) as the first author to use plastochron in reference to the initiation of two successive leaf primordia, or pairs of primordia in plants with decussate, or opposite phyllotaxis, at the level of the shoot apical meristem (SAM). Esau later (1965, pp. 105–106) attributed Schmidt (1924) as designating the plastochron as the period of time between the initiation of two successive individual, pairs, or whorls of leaf primordia by shoot apices, exhibiting spiral, opposite, or whorled arrangement. She noted that the term plastochron, as originally defined by Askenasy (1880) referred to “a time interval between two successive similar events occurring in a series of similar periodically repeated events.” She further noted, that under this general definition, plastochron could be applied to the time interval between (1) initial periclinal divisions within the inner most tunica layer of the SAM, associated with leaf primordia initiation, (2) morphological manifestation of apical growth, or lamina of primordia, (3) development of internodes, axillary buds, or floral organs, and (4) similar stages of vascularization of the shoot. Esau (1965) observed that plastochron could be used to indicate the developmental age of the plant as a whole, as well, and the plastochron index provided a refinement of this age that proved more useful in characterizing leaf development, than chronologic age, in that tight developmental trends emerged among many morphological and physiological parameters when it was used (Michelini, 1958). According to McMaster (2005), current general usage typically employs plastochron for the rate of primordia initiation on the shoot apex, and phyllochron for the rate of leaf emergence from the shoot bud. It should be noted that plastochron (English spelling, plastochrone) refers to an interval of time and that the terms “plastochron interval” or “plastochron duration” that are employed by several researchers using the PI are redundant. We humans love our abbreviations, which when it comes to “PI”, appears overly used! It should be noted that PI has also been used for the plastochron interval, a related but different concept that is employed by marine ecologists, reviewed by Duarte et al. (1994). It should also be noted that Richards (1951) introduced the phyllotaxis index, which is also abbreviated PI in the literature, but usually there is little opportunity for confusion among these two concepts, associated with the same abbreviation.

[Vol. 101

Since the introduction of the plastochron index and the present, two significant “revolutions” have occurred. The first was the “digital revolution”, which brought the computing power of calculating machines into everyday life, in terms of first rather mundane aspects of efficient algorithms of initial interest to only a small sector of society to the present situation where those algorithms are used (mostly unknowingly) by everyone who uses a “smart” cell phone. The second was the molecular genetics revolution, which, building upon the digital revolution, permitted us to not only unravel the intricacies of the genetic code of select “model” organisms, but progress beyond those model organisms to begin to ask comparative questions that are inherent in our quest toward understanding the evolution of development of all organisms. Throughout this time period and these two rather significant paradigm revolutions, the concept of the plastochron index has maintained predominance. I think that the reason for the PI’s longevity resides in its widespread utility in facilitating our understanding of plant growth and designing experiments with high temporal resolution. DERIVATION AND FORMULATION OF A PLASTOCHRON INDEX An Ah ha! moment— Erickson (1991) recounts how his initial measurements on Clematis species under the tutelage of Edgar Anderson revealed the repetitive nature of events occurring in association with successive nodes, but that “nothing else striking appeared”. Subsequently, his studies on microsporocyte and pollen development in Lilium longiflorum revealed that since the floral bud grew exponentially, the logarithm of the bud length was a good developmental index for cytological events occurring within the developing flower. While discussing potential studies that could be conducted on Xanthium plants grown under glasshouse conditions with Francis Michelini, Erickson revealed “I wrote the formula for the plastochron index at the blackboard, as if I had known it all the time.” Thus, the initial formulation of the plastochron index would appear to be one of those rare intuitive moments that are known to crop up as a result of protracted study of related aspects of life’s mysteries. Erickson (1976) provides additional details concerning his insight into floral developmental indices, as well as the PI in his excellent review on modeling plant growth. The plastochron index— The PI is typically calculated by: PI  n ln Ln  ln R ln Ln  ln Ln 1 ,

(1)

where n is the sequential index number of the organ for which the PI is being calculated, with n increasing in an acropetal direction, R is the reference length of the organ, Ln is the length of an organ that is equal to, or just slightly longer than R, and Ln+1 is the length of an organ that is just slightly shorter than R. If leaves on seedlings are being studied, typically n = 0, for the cotyledons. Three underlying assumptions— Working from the initial intuitive formula for the PI, three fundamental requirements for its calculation were derived (Erickson and Michelini, 1957): (1) Organ growth must be exponential. (2) Successive organs must be growing at the same relative rates. (3) Successive plastochrons must be equal, where here, plastochrons are defined as

November 2014]

MEICENHEIMER–PLASTOCHRON INDEX REVIEW

1823

the time intervals between the attainment of length R by successive organs. Preliminary to the establishment of a PI for any plant species, it is necessary to collect some longitudinal data on the growth of the plant organ that will ultimately be used to formulate the index. These data allow the three basic assumptions underlying the original PI formulation to be verified. Three derivations— In their introductory article, Erickson and Michelini (1957) provided three separate ways in which the PI formula could be derived. Two of these derivations were based on geometry and the third on an exponential leaf growth model. Lamoreaux et al. (1978) dismissed the third derivation for the PI that Erickson and Michelini (1957) provided because it contained errors that made it difficult to follow. Erickson (1976) provided a more succinct derivation of the PI based on the exponential growth model. While most users of the PI seem more inclined to follow one of the two geometric derivations, if they concern themselves with that aspect, at all, Vallejos et al. (1983) corrected the original typographical errors and expressed appreciation for the exponential growth model derivation, since it was the foundation for the development of their linear model of the plastochron, which was proposed as a useful tool for comparative studies of environmental growth responses of different genotypes. Because the exponential growth model derivation best introduces the three underlying assumptions of the PI, it will be introduced first, followed by the two geometric derivations. Reiteration of these derivations will set the stage for discussion of alternative ways that have been developed for the calculation of the PI, in cases where one or more of these assumptions is discovered not to hold for a particular species, or circumstance. If the three underlying assumptions hold, the early growth of a suite of organs, numbered in ascending sequential acropetal order, is represented by a family of exponential equations (Fig. 1). The length of organ n is expressed as Ln = L0n + ekt and the length of organ n + 1 as Ln+1 = L0n+1 + ekt, where t = chronologic time, L is length of organs, n and n+1 at time t; L0 is the length of organs, n and n + 1 at t = 0, and k = relative chronologic rate of elongation of organ (1/L dL/dt). If ekt is eliminated between these two equations, then we have Ln/Ln+1 = L0n/L0n+1. This ratio was termed the plastochron ratio, a, by Richards (1951) and represents the ratio by which two successive organs differ. Alternatively it represents the ratio by which a single organ increases during a plastochron. The constant initial terms of the two exponential equations describing organ length are related by L0n = a·L0n+1 and using this, a single equation can be written for any organ in terms of its serial number n, and time, Ln = L0n + ert+(ln an) or via log transformation, as depicted in Fig. 2, ln Ln = ln L0n + rt + ln an, which upon rearrangement yields, rt  n ln Ln – ln L 0 n ln a,

(2)

We now set L0 = R = arbitrary organ reference length, that can be easily nondestructively measured. Noting that the continuous scale of plastochrons is represented by rt and is referred to as the plastochron index = PI; and since Ln / Ln+1 = a, so that ln a can be replaced by ln Ln – ln Ln+1, then we see that Eq. 2 is equivalent to Eq. 1, the familiar formula for the PI. If we isolate a section of the data of Fig. 2, as is done in Fig. 3, then we can recreate the first geometric derivation of the PI that was presented by Erickson and Michelini (1957). Figure 3 illustrates that if the plastochron is defined as the time elapsed between

Fig. 1. Linear plot of theoretical successive organ lengths, labeled acropetally, in order of appearance, n − 4 through n + 4, and growing exponentially, as a function of time. Successive organs along the stem are identified relative to organ n, which is just slightly larger than the reference length R to be used in calculating the PI at time x in Fig 3. Organs “n −” were initiated before “n”, and organs “n +” were initiated after n at the level of the shoot apical meristem.

the attainment of length R by successive organs, then the plant will be n plastochrons old when organ n is R long, and n + 1 plastochrons old when organ n + 1 attains length R. The challenge, to which the PI provides solution, is what is the age of the plant when neither n nor n + 1 organs are equal to R? That is, some fraction of the plastochron between n and n + 1? Representing this time as Tx in Fig. 3, we can see that the fractional plastochron is represented by AB/AC, but note that these units are not measurable at a single instant in time Tx. We can take advantage of the fact that if the three assumptions underlying the PI hold, then triangles ABD and CBE are similar, which implies that AB/AC = DB/DE, and furthermore, lengths DB and DE can be measured at the single point in time Tx. Alternatively, as pointed out by Erickson and Michelini (1957) in their second geometric derivation of the PI, if the three underlying assumptions hold, a semilog plot of organ length vs. organ number n should yield a straight line at any instant in time (Fig. 4). It can be noted that the slope of this line is the relative plastochron rate of organ elongation, 1/L dL/dpl. Again, by virtue of similar triangles ABD and CBE, the fractional plastochron between n and n + 1 plastochrons can be calculated by DB/DE, measured at time, Tx. Both these geometric derivations, yield the initial equivalent formulae: PI  n AB AC  n DB DE ,

(3)

where AB/AC cannot be calculated at time Tx, but, DB/DE = (ln Ln– ln R) / (ln Ln – ln Ln+1) can and is of course equivalent to Eq. 1. It is of historical interest, that in 1957, log transformation and even accumulation of sums of squares for statistical analysis were time consuming and tedious efforts. Erickson (1960) published a nomogram that was designed to facilitate assessment of the PI in the absence of the convenience of contemporary scientific calculators and statistical software. While early application of the PI relied on graphical “by the eye” assessment of the growth characteristics of the target organ, as computing power and software evolved the underlying assumptions were subject to more precise statistical evaluation, as illustrated by studies on Ranunculus (Meicenheimer, 1979), Epilobium (Meicenheimer,

1824

[Vol. 101

AMERICAN JOURNAL OF BOTANY

Fig. 2. Log transformation of theoretical longitudinal data of Fig. 1 illustrates that the three essential criteria for PI development are fulfilled. Straight lines resulting from log transformation indicate the organs are growing exponentially. Parallel lines of successive organs indicate that they are all growing at equal relative rates. Equal spacing of lines indicate that the plastochrons are equal between the initiation of successive organs.

1981), Dianthus chinensis (McCauley and Croxdale, 1984), Fraxinus (Merrill, 1986), Arabidopsis (Groot and Meicenheimer, 2000), and others. Leaf plastochron index— Another index, closely related to the PI, which allows age determinations for organs that are inaccessible without dissection and for organs that are no longer growing exponentially, or, at all, is the leaf plastochron index (LPI) defined as: LPI  PI – n ,

(4)

where ñ is the index number of an organ, using the same acropetal numbering scheme as applied to n and PI is the plastochron index. There appears to be some confusion among some researchers with regard to the PI and LPI concepts. To clarify, the PI allows the morphological age of a plant to be expressed in terms of the total plastochrons that have passed the reference length R. The LPI allows the morphological age of any organ of interest to be expressed relative to the reference length. So for any given PI, the LPI of an organ is 0 when ñ = R; negative when ñ < R; and positive when ñ > R. The PI expresses the age of the plant or shoot, whereas the LPI expresses the age of individual organs comprising the shoot system. An example of how the LPI can be used to quantify the growth characteristics of the radial and vertical dimensions of the stem, as well as leaves within the shoot bud can be found in Meicenheimer (1981). LIMITATIONS AND ADDITIONAL FORMULATIONS There are certain situations and/or plant species for which one or more of the three criteria for the original PI formulation do not hold. These include development of lateral organs along heteroblastic shoots, such as those taxa cited in Hill and Lord (1990), as well as plants for which the plastochron is so long that the older leaf exits exponential growth before the next younger leaf becomes measurable (Meicenheimer, 1979; Merrill, 1986).

Fig. 3. Detailed isolation of n − 1, n, and n + 1 theoretical longitudinal log-transformed data of Fig. 2, illustrating the widely used geometric derivation of the PI for calculating the PI at time Tx, using organ reference length R. It is easy to see that at point A, the PI would equal n and that at point C, the PI would equal n + 1. The PI at point B would be equal to n + AB/AC, but this cannot be determined at time Tx! However, DB/DE = AB/ AC, since triangles ABD and CBE are similar, and DB/DE can be calculated at time Tx! By substitution, the PI can therefore be calculated as n + DB/DE, as given in Eq. 1 in the text, at time Tx.

Hill and Lord (1990) proposed a reformulation of the PI to enable its calculation in these cases, using repeated measurements of the same organ, as it grows through the reference length R (Fig. 5). That is, let the function depicted in Fig. 5 represent the exponential growth of organ n through time. As before, what is desired is the fractional value of the plastochron, AB/AC, which is equivalent to CE/CD given that triangles ACD and BCE are similar. However, CE/CD cannot be obtained as in the original case, because either the plastochron is too long, the relative plastochron rate of elongation too rapid, or a combination of these circumstances. CE/CD is equivalent to



PI  i ln L ni,t 2 – ln R

ln L

ni,t 2



 ln L ni,t1 ,

(5)

where i is the node number, numbering acropetally, R is the organ reference length, L(ni,t1) is the length of the oldest organ, with L ≤ R, at node i at time = 1, and L(ni,t2) is the length of the same organ, with L ≥ R, at node i at time = 2. Using this formulation of the PI allows the fractional component of the index to be calculated using measurements on the same organ that bracket the reference length at least two times. It should be noted that Eq. 5 formulation of the PI is similar to the leaf measuring-interval index proposed by Chen et al. (2009) who appeared to be unaware of the Hill and Lord (1990) formulation. Among the most environmentally sensitive growth processes are initiation and expansion of leaves (Vendeland et al., 1982). Low temperatures and drought stress lengthen the plastochron. In addition, water stress has significant influence on leaf expansion. In the original Erickson and Michelini (1957) article, reference was made to Askenasy’s (1880) calculated values of “Wachstrumgeschwindigkeit” = ln (In/In+1) = a = natural logarithm of two successive internode lengths. Erickson and Michelini pointed out that Askenasy’s a is equivalent to their p, or the leaf relative plastochron rate of elongation, and that their variable r is the relative chronological rate of leaf elongation.

November 2014]

MEICENHEIMER–PLASTOCHRON INDEX REVIEW

Fig. 4. Detailed isolation of n − 1, n, and n + 1 theoretical longitudinal log-transformed data of Fig. 2, illustrating an alternative geometric derivation of the PI, at time Tx, using organ reference length R. Here, the logtransformed lengths of successive organs are plotted as a function of sequence number n at time Tx. It is easy to see that at point A, the PI would equal n and that at point C, the PI would equal n + 1, but none of the organs are at point A or C at time Tx. The PI at point B would be equal to n + AB/ AC, but this cannot be determined at time Tx! However, DB/DE = AB/AC, since triangles ABD and CBE are similar, and DB/DE can be calculated at time Tx! By substitution, the PI can therefore be calculated as n + DB/DE, as given in Eq. 1 in the text, at time Tx.

1825

Fig. 5. Detailed isolation of n − 1, n, and n + 1 theoretical longitudinal log-transformed data similar to that of Fig. 2, but here the relative rate of organ growth is high enough and the plastochron long enough that only leaf n brackets the reference length R during times that the organ can be conveniently measured. PI cannot be calculated using Eq. 1 in this case. An alternative method of PI calculation was developed for such cases by Hill and Lord (1990). The PI at point B would be equal to n + AB/AC, but this cannot be determined at time Tx. However, CE/CD = AB/AC, since triangles ACD and BCE are similar, and CE/CD can be calculated by using measurements of organ n at time T1 (A) and at time T2 (C), when organ n is less than the reference length R at T1 and greater than R at T2. By substitution, the PI can therefore be calculated as n + CE/CD, as given in Eq. 5 in the text, at time Tx.

relative plastochron rates. These workers proposed an alternative PI formula using the length of a single leaf: Erickson (1976) further pointed out that the ratio Ln/Ln+1 was introduced as the variable a, termed plastochron ratio by Richards (1951), and reiterated that in their original article the natural log of a, symbolized by p, represents the relative plastochron rate of leaf elongation. Silk (1984) summarizes various strain rates (relative elemental growth rates) of organs from the literature. Silk (1980) referred to log Ln+1/Ln as the plastochron ratio and observed that quantitatively, it is invariant with temperature in cantaloupe. It would appear that rather than plastochron ratio, the term relative plastochron rate of elongation should have been applied to the log of the ratio of two successive leaves (Erickson and Michelini’s original p variable) and plastochron ratio used in reference to just the ratio (represented by variable a of Richards (1951) and Erickson (1976). Typically, the plastochron ratio is formulated such that the ratio is greater than 1. This confusion in terminology was carried over into the study on environmental effects on the PI of Glycine max by Vendeland et al. (1982), who also discussed the nomenclatural variations that exist in the literature. Vendeland et al. (1982) conducted studies on field-grown soybean to assess the validity of the initial three assumptions underlying PI formulation. These workers observed that under drought stress that two of the three assumptions failed: temporal functions of ln L were not parallel, and temporal functions of successive leaves were not equally spaced. The relative plastochron rate of leaf elongation was increased upon imposition of drought stress. Upon further analysis, the growth of smaller, younger leaves was observed to be retarded much more than older leaves when drought stress was imposed. Vendeland et al. (1982) concluded that the original PI formula assumptions were not supported, and if used in such studies, the PI would tend to mask the stress response because its calculation would involve an interpolation between leaves that are growing at different

PI  n ln Ln 1  ln R a ln Lnt 2  ln Lnt1 ,

(6)

where n is the sequential index number of the organ for which the PI is being calculated, with n increasing in an acropetal direction. If leaves on seedlings are being studied, typically n = 0, for the cotyledons. R′ is the reference length of organ associated with stressed conditions such that ln Lnt 2 – ln Lnt1  ln R – ln R a, where R is the reference length of organ associated with unstressed conditions and ln R′ = ln R − ln Lnt2 − ln Lnt1, where Lnt1 and Lnt2 is the length of the unstressed leaf at time 1 and 2, respectively. Here, ln Lnt2 – ln Lnt1 is the relative plastochron rate of the unstressed leaf, and Ln+1 is the length of the stressed organ. Comparisons of PI calculated by Eqs. 1 and 6 revealed that although both methods revealed dramatic changes in the PI time course in response to drought, Eq. 6 was much more responsive to both initiation and recovery to water stress. This responsiveness reflects the use of small, young leaves, which are more sensitive to drought stress in Eq. 6, and the lack of interpolation between these leaves and older less sensitive leaves used in Eq. 1. DEVELOPMENT OF RELATED INDICES Monocots—In their initial publication, Erickson and Michelini (1957) identified several known difficulties inherent to the formulation of the PI for species such as grasses, where young leaves and internodes are encased in sheaths, thereby preventing measurement of leaf lengths exhibiting exponential growth. Their suggestion that such difficulty could be circumvented by

1826

AMERICAN JOURNAL OF BOTANY

careful dissection of such plants has been formally verified by Dekankova and Jesko (1987) for Zea mays, but of course, this approach is destructive. Haun (1973) developed an observational developmental index for Triticum aestivum in which relative proportions of leaf lamina compared with an average maximum length were used instead of length measurements. A related index that many workers employ in their studies on members of the Poaceae is the Haun index: HI  n – 1 Ln Ln –1  0 b Ln Ln –1 b 1¯ , ¢ ±

(7)

where n is the number of leaves that have appeared on the shoot, Ln−1 is the blade length of the penultimate leaf, and Ln = blade length of the youngest expanding leaf that is emerging from the sheath of the penultimate leaf. The time function of the Haun index can be used to assess the phyllochron. McMaster (2005) thoroughly discusses the methods of study of the growth and development of temperate cereal crops in his Journal of Agricultural Science Centenary Review. Among researchers on Oryza sativa (rice), the term phyllochron is often used in reference to the time interval that elapses between appearances of successive leaves from the enclosing leaf sheaths associated with the main shoot apex. In rice the developmental processes of sequential axillary buds and leaves appear highly synchronized with the phyllochron of the main stem, making this a useful biological time unit with which to study the development of the entire shoot system (Miyamoto et al., 2004). In my experience, this proposed relationship is worthy of additional investigation (R. D. Meicenheimer, unpublished data). Beemster and Masle (1996) used both the Haun index and the plastochron index in their study on seedlings of Triticum aestivum subjected to root stress induced by high resistance to penetration through the soil. This stress slows leaf growth and reduces leaf size. It was determined that high resistance soil reduced rates of the shoot apex and leaf development but did not appear to have immediate effects on the pattern of development of newly initiated phytomers. The rate of leaf primordium development and associated node were related to plastochronic age. Effects on developmental patterns were first detected during the second plastochron of development. The ontogenetic pattern of leaf elongation was affected during the next few plastochrons preceding leaf emergence. Jain (1970) and Swan et al. (1981) used the corn leaf number index (CLNI) in their studies on Zea mays: CLNI = n + (zn + 1)/ (Zn + 1), where zn + 1 is the measured length of the emerging (n + 1)th leaf, Zn + 1 is the standard length Zn + 1 for leaf n +1, which is the average length of a large number of (n + 1)th leaves, just before emergence on the n + 2 leaf. Depending on the value of n, the n + 1 leaf is either at the intersection of the folds of leaf n, or at the intersection of the nth and (n − 1)th leaves. The CLNI was observed to be a continuous function of the length of the emerging leaf and provides a growth scale equal to 0.0 when the seedling emerged from the soil to n.0 when the tassel was fully emerged. The CLNI data from growth chamber and field studies indicated that corn growth was an approximate linear function of time. Growth rates were related to mean

[Vol. 101

temperature, diurnal temperature range, and photoperiod. Mean temperature and diurnal temperature range were by far the most important factors influencing growth rates. Sea grass— A commonly used technique that is often employed by ecologists studying population dynamics of various species of sea grass is the plastochron interval, also abbreviated PI (Duarte et al., 1994, which includes a list of sea grass species). The plastochron interval is premised on the observation that every sea grass leaf production is associated with a rhizome node. Patriquin (1973) proposed that sea grass root and rhizome production can be estimated by determining the time interval for the formation of new leaves and by counting associated leaf scars. The age of a shoot is measured as the total number of leaves produced during its life (number of leaf scars + number of standing leaves). The resulting time units correspond to the average time interval between initiation of two successive leaves on a shoot, referred to as the plastochron interval. Plastochron intervals represent indirect estimates of time, which although subject to seasonal variability, provide accurate estimates of time at interannual time scales (Brouns, 1985). The working formulation for the plastochron interval according to Jacobs (1979) is: Plastochron interval = (No. of shoots counted × Interval in days) / No. of new leaves. Duarte et al. (1994) reviews this and other techniques that are useful in reconstructing sea grass dynamics. Echavarria-Heras et al. (2013), however, recently challenged the prevalent idea that the plastochron interval is the best technique for determining sea grass productivity. Trees— Another group of plants Erickson and Michelini (1957) identified as potentially problematic were species exhibiting marked seasonal growth, such as trees. Although, Niklas (1991) used the LPI to study the biophysics of “young” and “old” petioles of field-grown twigs of Populus tremuloides, he noted that the LPI was an extremely crude measure of relative ages of leaves sampled in May and August, since young leaves were growing exponentially in May, old leaves, either were not growing or were growing slower in August. He considered the relationships among the petiole morphological features based on LPI to be equivocal. For oak seedlings, the Quercus morphological index was formulated to characterize the repeated flushes of shoot growth (Hanson et al., 1986). Various workers have successfully employed the PI and LPI in studies on tree seedlings exhibiting indeterminate growth under controlled environmental conditions. These include Populus (Larson and Isebrands, 1971), Fraxinus (Merrill, 1986), and Prunus (Horsley and Gottschalk, 1989). Pinus— Because there are numerous nodes with very short internodes even in young plants, only a few workers have destructively counted the number of nodes produced at a given stage in conifer seedlings (Lascoux et al., 1993). When the conifer species under study exhibit distinct heteroblastic changes, quantitative evaluation of this change or the size of the plants at the time of the change provided reasonable criteria for comparing genotypes. The total number of nodes in the main shoot was found to be closely linked to the increase in total plant size, but inversely related to the proportion of secondary needles, which indicated the amount of heteroblastic change. Climent et al. (2013) developed an ontogenetic index (OS): OS  N ds N t 1 2 , where Nt = total number of basal nodes observed, Nds is the

November 2014]

MEICENHEIMER–PLASTOCHRON INDEX REVIEW

number of nodes with axillary dwarf shoots present at any developmental stage. The square root exponent was chosen to normalize the distribution. The OS reflected the formation of secondary needles on the shoot, which is one of the important changes in Pinus (pine) seedling ontogeny. Secondary needles have been reported to be less sensitive to water loss compared with juvenile leaves (Pardos et al., 2009). The OS was found to only be partially correlated between pine species (Climent et al., 2013). APPLICATION OF THE PLASTOCHRON INDEX The usefulness of the PI continues to be evident by its use in research studies on various economically important and model plant species during the last 40 yr. This section continues coverage of select taxa initially reviewed by Lamoreaux et al. (1978) and discusses advancements up to the present. Grouping is by genera, more or less reflecting the historical order in which the PI was developed within these taxa, to reinforce the perception that development of a PI for any given taxon is likely to enhance the resolution of knowledge for that taxon. Xanthium— The species for which the PI was initially developed was Xanthium strumarium L., although X. italicum Moretti and X. penslyvanicum Wallr. were used by various researchers for this species in the past (http://www.tropicos.org/). Both Michelini and Maksysmowych, students in Erickson’s laboratory, used the concept to great advantage. Although Michelini subsequently entered the administrative side of academia, Maksymowych established a laboratory at Villanova, and focused on using the PI and LPI to develop what is one of the most detailed temporal and structural investigations into leaf development in existence. Most of that research has been synthesized in Analysis of Growth and Development of Xanthium (Maksymowych et al., 1990). Corresponding to the date of the review by Lamoreaux et al. (1978) and beyond, Maksymowych’s laboratory began concentrating on developmental aspects of the Xanthium stem. The effects of gibberellic acid on stem growth (Maksymowych et al., 1976; Maksymowych and Erickson, 1977) were found to result in a decrease in the plastochron coupled with changes in phyllotaxis that appeared stable. Similar but transient phyllotactic changes were found to occur within the terminal shoot that produced staminate inflorescences upon short day photoperiod induction of flowering (Erickson and Meicenheimer, 1977). Common to both these phyllotactic transformations were parallel decreases in the plastochron and the relative plastochron rate of stem expansion that resulted in a continuous transition of phyllotactic pattern from (2,3) to (3,5) contact parastichy pattern, but there was no significant change in the chronologic rate of stem expansion. The change in phyllotaxis thus occurred as a change in the relative distribution of growth on the shoot apex, not from a change in the chronologic rates of expansion of the SAM. It is of interest that in footnote 4 of the Erickson and Michelini (1957) article, they noted that p (ln a, in the present paper) may have some relation to the phyllotactic divergence of leaves and that the value of ln a varies widely among dicotyledonous species. They further noted that, they felt that ln a, the relative plastochron rate of growth, may be of great morphological interest. Detailed studies on the relative elemental rate of node and internode elongation revealed that the initially constant rate of

1827

elongation exhibited an acropetal pattern of elongation that diminished over time. Detailed studies on internodes positioned 4 mm and farther from the tip of the stem initially exhibited constant relative elemental rates of elongation. At about 2 cm removed from the tip, the relative elemental rates of internode elongation began to exhibit an acropetal pattern that diminished with LPI and distance from the node. Internode elongation stopped at 8 cm from the shoot tip (Maksymowych et al., 1985) Further studies revealed that in PI 14 stems the region of cell division extended 20 cm basipetally below the SAM. Mature cortical cell length was observed 55 mm below the stem apex, indicating that shoot growth occurred through cell expansion 20–55 mm below the apex (Maksymowych et al., 1989). Studies on the relative elemental rate of elongation of nodal regions of Xanthium stems indicated that these expanded at slower rates (0.05 d−1) compared with internodes (0.2 d−1) and that these rates decreased with age, stopping shortly after LPI 0 (Maksymowych and Orkwiszewski (1993). One potential use of the PI and LPI concepts that appears to have received little attention to date is the isoenzyme study by Chen and Towill (1970) on X. pennsylvanicum leaf development. This research revealed that during leaf development the nature of changes that occurred differed from enzyme to enzyme and from isoenzyme to isoenzyme. Some isoenzymes were characteristic to very young leaves, others to rapidly expanding leaves, and still others to older leaves. Many of the changes in isoenzyme patterns coincided with the cessation of cell division in the leaf or with termination of leaf expansion. A significant conclusion was that particular isoenzyme patterns depended on both leaf (LPI) and plant (PI) age. These early studies preceded current methods used to study the metabolome and transcriptome. One would hope that eventually the high chronologic resolution available with the PI and LPI concepts will be used in such studies in the future. Linum— Meicenheimer (1992) pointed out that the concepts of node and internode do not lend themselves to analyses of growth and differentiation processes of the shoot apex and intermediate region between the SAM and mature stem. While there are obvious regions of stem tissue between areas of leaf insertion on the stem, the term internode cannot be applied since there is vertical overlap of nodes in these areas of the stem. To circumvent this dilemma, the three-dimensional stem unit was proposed (Meicenheimer, 1992), and a plastochron index based on stem unit reference length R of 5 mm was developed. A stem unit plastochron index (SUPI) directly analogous to the leaf plastochron index (LPI) was developed for analysis of the growth characteristics of nodes and stem units. Linum ussitatisimum L. grown under constant environmental conditions exhibited constant phyllotaxis and plastochron for nodes 35–80, during which the stem unit was defined by the boundaries of four successive leaf primordia along the 3-, 5-, and 8-parastichies and radially by these boundaries extended to the centroid of the stem. Growth characteristics of Linum stem units −32 to 0 SUPI were analyzed. Vertical growth velocity was uniform within stem units, increasing with SUPI. Vertical strain rates of nodes were nonlinear and consistently lower than the linear vertical strain rates of subjacent stem units. Radial and tangential stem unit velocity fields were uniform and steady up to −25 SUPI, thereafter these fields were characterized by uniform spatial and temporal patterns. As a result of this analysis, it was concluded that the stem is a steady-state growth structure, rather like an elongating root, up to −25 SUPI, but

1828

AMERICAN JOURNAL OF BOTANY

thereafter becomes a repetitive growth structure, rather like a leaf (Meicenheimer, 2006). Populus— Larson and coworkers at the North Central Forest Experiment Station in Rhinelander, WI were quite successful in applying the PI to seedlings of Populus deltoides W. Bartram ex Marshall grown under uniform environmental conditions for which plants of PI 24 and older exhibit many features of steady state growth. That is, the plastochron had stabilized at ca. 1.1 d and the relative rates of leaf and internode elongation were constant for a given LPI (Larson, 1980a). A reference length R of 20 mm was selected as most convenient for PI calculation. The predictions of Larson and Isebrands (1971) that growth correlations between LPI and vessel metrics and the timing of transitions from primary and secondary vessel formation in Populus stems could be understood by employing the PI in developmental studies have now largely been validated. Autoradiography of arrays of leaves from plants in which C14 labeling of select LPI leaf lamina allowed Larson (1977) to detect a functional change in the vascular phyllotaxis of interconnected leaf traces through PI 16. This functional change in leaf trace interconnections occurred without a change in the contact parastichy pattern of leaf arrangement at the level of the SAM (R. D. Meicenheimer and P. R. Larson, unpublished data). Previous work on the structure and organization of the primary vascular system of P. deltoides (Larson, 1975, 1976, 1977, 1980a, b) was extended to include the development of empirical quantitative models describing the temporal and spatial changes in vessel characteristics of metaxylem within individual central leaf traces, as well as within all central leaf traces considered as a morphological unit (the central trace sympodia) at a given transverse level in the stem. Similar models were constructed for secondary vessel characteristics (Meicenheimer and Larson, 1983). These analyses revealed a functional developmental continuum between the central trace sympodia metaxylem and secondary vessels of the stem. It was discovered that the transition between the central trace sympodia metaxylem and secondary xylem production corresponded with the cessation of leaf and internode elongation. Blocking indole-3-acetic acid transport at −1 to 0 LPI, with N-1-naphthylphthalamic acid, and harvesting 6 plastochrons later, revealed that basipetal auxin transport mainly influenced the diameter of metaxylem vessels, as opposed to the number of vessels per central trace (Meicenheimer and Larson, 1985). The use of the PI has been extended to other species of Populus and hybrid genotypes. The PI and LPI concept allowed researchers to set up experiments to evaluate leaf gas exchange processes in Populus clones (Ceulemans and Impens, 1979, 1980; Ceulemans et al., 1980). It was discovered that clones with high leaf production rate exhibited low leaf growth rates and higher LPIs at maturity. Clones that yielded higher biomass and fast growth exhibited similar leaf production rates but with higher leaf growth rates. Although there were considerable differences in the plastochron, the LPI at maturity, and absolute leaf growth rates among clones, there were only small differences in the relative leaf growth rate among clones (Ceulemans et al., 1988). Analysis of feeding preference and phloem sap exudates collected from leaves of P. deltoides at different LPIs suggested that physiological and phytochemical differences as a function of LPI might contribute to the selection patterns for leaf stages by the aphid Chsilophorous populicola. Rapidly expanding leaves had significantly less lignification and new leaves had

[Vol. 101

shorter distances to the vascular bundles than senescent leaves (Gaudillere and Mousseau, 1989). Frost et al. (2012) measured plant height and diameters of internodes at LPI 5 and 20, as well as 3 cm from the ground to determine growth rates in transgenic RNAi lines of Populus termula × P. alba clones. Wilting of LPI 3 to 6 leaves was used as an indicator of incipient wilt to provide a benchmark to monitor the progress of experimental treatments and to anticipate the onset of wilt in soil moisture availability experiments. These workers hypothesized that the tonoplast sucrose fluxes mediated by the tonoplast-localized sucrose transporter (PtaSUT4) contribute to the regulation of osmotic gradients between cellular compartments, with potential to mediate sink provisioning and drought tolerance in Populus. Nicotiana— D’Agostino et al. (1982) used the PI and LPI to study the cytological events associated with natural senescence of leaves. Data were normalized relative to LPI 3 leaves for 14 PI old plants grown under normal greenhouse conditions. LPI 3, young adult leaves with tissues with organelle-rich, functioning cytoplasm were compared with LPI 8, presenescent leaves, and LPI 10, senescent leaves with severe cell disorganization. Cytological patterns observed in association with Nicotiana tabacum L. leaf aging and senescence were found to be similar to those observed in Gomphrena globosa L. (D’Agostino et al., 1982) in spite of the very different times required to reach the final stages of leaf senescence. Turgeon (1984) modified the LPI to permit comparison of green, light green and albino leaves of tobacco to compensate for leaves from these three groups being of different size throughout development. The end of exponential growth was identified as a useful reference point. Using reference leaf length R = 20 mm, ln(leaf area) for each plant type was plotted as a function of LPI. The LPI value at the point where these growth curves deviated from linearity (end of exponential growth) was then subtracted from the original LPI to obtain the modified LPI used in comparisons between types. The original and modified LPIs had scales of the same unit length, but differed in that the zero value is related to the 20 mm reference leaf length in the former and by the end of the exponential growth period in the latter. It was observed that 14C sucrose import progressively ceased in developing green leaves even when photosynthesis was prevented by darkening the leaves. It was concluded that cessation of sucrose import is not a direct result of export initiation nor does it require achievement of a positive carbon balance (Turgeon, 1984). Leaves between 3.3 and 3.5 LPI were used in autoradiograph studies to study source sink transitions in tobacco leaves. At this age in development, sink leaves are undergoing the sink–source transition. They are 12–13 cm long, and the import termination boundary is located 4–6 cm from the tip of the leaf (Turgeon, 1987). Import by the sink leaf was completely inhibited by exposing the sink leaf to anaerobic conditions, steamgirdling the sink-leaf petiole, or placing the entire plant in the cold. Phloem unloading was completely inhibited by cold, but continued when the sink leaf petiole was steam girdled and when the sink leaf was exposed to anaerobic environment. Only a small percentage of labeled nutrients was present in free space after unloading from sink-leaf veins under anaerobic environment (Turgeon, 1987). These results were interpreted as consistent with passive symplastic transfer of photoassimlates from phloem to surrounding cells in sink veins.

November 2014]

MEICENHEIMER–PLASTOCHRON INDEX REVIEW

Hill and Malmberg (1991) used the modified calculating formula summarized in Eq. 5 in studies on the growth of vegetative and reproductive shoots of N. tobacum to determine the relationship between corolla growth and time. There was a steady decline in the plastochron of leaves 9–20. The flower plastochron steadily increased during the growth of an individual cyme with the longest plastochron associated with the most distal flower. Variation in the flower plastochron was determined to reflect variation in rate of flower initiation, not the growth rate of individual flowers. The pattern of corolla expansion was observed to differ from that observed in tobacco leaves, in that the initial high but rapidly declining rate was not detected in the corolla. The duration of constant exponential growth was twice as long in the corolla compared with leaves (14 vs. 7 d). In addition, the corollas exhibited low-amplitude oscillations in relative growth rates, which were detectable because the growth of several cymes were plotted on a common time scale using the PI. There was a rapid rise in relative growth rate of the corolla as contrasted with a gradual decline in leaf relative growth rate as the organs approached their maximum final size. The leaf and corolla of tobacco appear to differ in the timing of similar developmental events and the timing of final organ expansion (Hill and Malmberg, 1991). Trull and Malmberg (1994) used the PI in studies on the Nicotiana mutant, Puzzle box, in which the inflorescence and floral programs are expressed together. The mean plastochron was calculated for six plants using the Hill and Malmberg (1991) technique (Eq. 5) and reference length R = 80 mm. Since the plant material studied were cultured explants instead of seed, the plastochron was calculated for 11 nodes counting the node just before flowering as node −1. Puzzle box plants exhibited an irregular plastochron. There was no consistent pattern between plants or as a function of LPI, nor was there a decrease in the plastochron before flowering as observed in wild-type tobacco (Trull and Malmberg, 1994). Zhuravlev et al. (1983) standardized tobacco protoplast sources in studies on tobacco mosaic virus to LPI 1–3 leaves from PI 16–18 plants. The PI and LPI has been used to standardize experimental and control plants inoculated with tobacco mosaic virus (Burundukova et al., 2009) as well as follow the progression of viral diseases in intact (Derrick et al., 1997) and grafted (Malinovskii et al., 1994) plants, and tissue and cell cultures obtained from inoculated plants (Malinovskii et al., 1993). Tsai et al. (1997) used the time course of the PI to compare wild type and rbcS antisense mutants of tobacco to establish that the early phase of shoot morphogenesis was prolonged in antisense plants with an increase number of leaves being produced during this phase of development. These workers suggested that the early phase change from early to late stages occurred when a threshold carbohydrate source strength is attained, which was delayed in the antisense plants that had reduced levels of ribulose 1,5-biphosphate carboxylase (Rubisco). Lycopersicon— Coleman and Greyson (1976) established a PI for vegetative Lycopersicon esculentum Mill. (tomato) based on R = 30 mm compound leaf length, with the objective of encouraging more precise age determination of the plant than had previously been used by tomato researchers. That objective appears to have borne fruit! Hicklenton and Jolliffe (1978, 1980) employed the PI to assess effects of CO2-enrichment on tomato physiology and yield.

1829

Subsequently, the PI (R = 20 mm leaf length) has been used to more precisely group plants for experimental and control groups and the LPI used to more precisely separate leaf samples on the basis of similar age in studies on ozone and light stress (McCool et al., 1982; McCool and Menge, 1983). The PI and leaf area and plant height were used as nondestructive covariant measurements to reduce plant to plant variation within treatments in statistical analyses of concurrent and sequential NO2 and O3 exposures (Goodyear and Ormrod, 1988) and within photoperiod differences in O3 sensitivity of both tomato and soybean (Goodyear and Ormrod, 1991). The PI was used similarly by Hale et al. (1985) in studies on effects of heavy metal mixtures of the nickel and copper. The LPI has provided means of assessing the rate of leaf development in studies on the role ethylene plays in chilling tolerance in tomato. Chill hardening was observed to increase ethylene synthesis in WT and ethylene insensitive mutant, but only increased the rate of leaf development, as measured using the PI and dry mass accumulation during the recovery period in WT plants only, indicating that a response to ethylene is involved in chilling tolerance development (Ciardi et al., 1997). Similarly, Brüggemann et al. (1992) used the PI to determine the effects of unfavorable combinations of low temperature and low light on tomato growth, development, and photosynthesis. As long as a critical 8°C threshold was not exceeded, there was no loss in developmental capacity of the plants. The negative effects of the 8°C threshold was related to irreversible damage to apical meristem tissue, which could be circumvented by drought-hardening prior to chilling. PI as a function of time was used as a nondestructive indicator to examine the effect of temperature on the developmental rate of the shoot between the second and twelfth leaf stage of tomato. A lack of significant difference between the plastochrons of treatment groups was used to support the conclusion that chloroplast substitution was not an effective method for breeding improved low-temperature tolerance in tomato (Dolstra et al., 2002). The plastochron was 2 d in the high temperature regime (HTR) and 6 d in the low temperature regime (LTR) and was not significantly influenced by chloroplast type. These workers suggested that differences in PI (4–5 vs 1) for the initial LTR treatment plant population in their experiments compared with the low temperature experiments of Miltau et al. (1986) would suggest that the inhibitory effect of low temperature on the developmental rate of tomato shoots decreases with increasing physiological age. Fleming et al. (1993) employed the PI to standardize the ages of plants undergoing dissection for SAM tissue from which total RNA was extracted before construction of a cDNA library. When the length of the second leaf was between 28 and 45 mm and the length of the third leaf length between 5 and 14 mm, the sixth primordium on the SAM was between 0 and 100 µm (early stage) and 150 and 250 µm (late stage of development). The SAM and sixth primordia tissues were collected for RNA extraction. Approximately 300 plants yielded 2 mg of fresh mass of apical meristem material. In situ hybridization was then done on material 5–7 plastochrons old. Although none of the genes obtained from the cDNA library exhibited localization exclusively in the SAM, six gene expression spatial patterns were recognized in the SAM. Park et al. (2012) used the PI to define vegetative meristem stages in their deep sequencing of transciptomes, which allowed them to identify the dynamics of gene expression in individual tomato SAMs during the gradual transition from vegetative to terminal flower state. Coleman and Greyson (1976) observed

1830

AMERICAN JOURNAL OF BOTANY

that in tomato once the terminal SAM flowered, a useful PI could not be calculated. To compensate for this, Par et al. (2012) developed a time scale based on days after germination plus the initiation number of the youngest leaf primordium visible at the level of the SAM. This time scale permitted plants to be classified into early, middle, and late vegetative, plus transitional and floral stages. These workers profiled the transcriptome of each stage by isolating mRNA and subjecting cDNA to Illumina sequencing. Their study revealed that the genetic program for inflorescence branching was initiated early during meristem maturation. They suggested that evolutionary diversity in inflorescence architecture is modulated by heterochronic shifts in the acquisition of floral fate. Glycine— The PI is considered a very sensitive indicator of plant development and has been used extensively in various physiological studies on legumes grown in controlled environments. The PI allows very precise quantification of shoot growth rates. Hanada and Yong Son (1974) first established a PI for Glycine max L. Merr. (soybean), in a controlled environment. They concluded that the central leaflet (R = 30 mm) was a better organ to use than the entire compound leaf (R = 45 mm) in terms of ease of measurement and size of errors. An absolute prerequisite for studies on nodulation and symbiotic nitrogen fixation is careful selection and standardization of growth media, particularly when uniform plant culture among various participating laboratories is required. Effects of growth media were assessed by measurement of PI, chlorophyll content, and CO2 assimilation rates in soybean (Van Heerden et al., 2007). Shoot growth rates (SGR), defined as the increase in the PI units per day, were determined by linear regression of PI as a function of time for four types of growth media. Results indicated that there was no significant effects on shoot growth and development for these four media. However, large effects on number of nodules and symbiotic nitrogen fixation were observed. Together, these results indicate that shoot phenotype and physiology did not offer any insight to below ground effects of culture media. Van Heerden et al. (2004) used daily measurements of the PI, based on R = 25 mm central leaflet of the trifoliate leaf, to quantify effects of nitrate addition and dark chilling on soybean vegetative development. In one chilling sensitive cultivar of this study, Java 29, this analysis indicated that nitrate supplementation considerably reduced the chilling-induced suppression of vegetative development. These results support the hypothesis that the greater chilling sensitivity of Java 29 is related to the greater sensitivity of symbiotic nitrogen fixation in this genotype. Silvius et al. (1978) studied carbon assimilation, translocation, and associated biochemical characteristics of the second trifoliate leaves that were selected on the basis of LPI to provide uniform study material at select stages of development 10–25 d post emergence using the PI to reduce variability based on reference length R = 20 mm of the midvein of the terminal leaflet. Leaves sampled at six LPIs (1.8, 2.6, 3.6, 4.1, 6.6, and 7.4) constituted their high-resolution developmental study. Snyder and Bunce (1983) used the PI to investigate effects of irradiation levels and duration, temperature, and nitrogen regimes on soybean growth under controlled environmental conditions. An increase in photoperiod from 10 to 16 h increased the plastochron and enhanced axillary growth. Doubling light intensity increased the plastochron and relative proportion of root to total biomass and decreased stem + petiole to total

[Vol. 101

biomass. With an 8-h photoperiod, the plastochron increased, but the duration of leaf expansion decreased with increasing temperature. Tremmel and Patterson (1994) evaluated the interacting effects of temperature and enriched CO2 on development of soybean and five C3 and C4 grass and eudicot weeds by continual measurements of PI during the study. Plastochron rate was higher at higher temperature in all species examined, and was higher at elevated CO2 in all dicots except Abutilon theophrasti Medic (velvetleaf). Calculating plastochron rates on a degreeday basis removed differences between temperature treatments but did not alter responses due to CO2 elevation. The relationship between main stem and branch developmental rates was altered in soybean. Overall, the results indicated that developmental responses to temperature and CO2 depend on both the aspect of development considered and the species. For soybean, Amaranthus retroflexus L. (red root pigweed), Cassia obtusifolia L. (sicklepod), and velvetleaf plants, the PI of the main stem was calculated and numbers of branches and branch leaves counted. The reference length R was 10 mm for all but redroot pigweed, for which R = 15 mm was used. Central leaflets were measured for soybean and sicklepod; leaf lengths were used for the other species. Polynomial regression for each plant was used to examine PI as a function of days after planting, and an ANOVA or MANOVA comparison of regression coefficients was used to test for effects of CO2, temperature, and interactions. Degree day (DD) was also used in these analyses: DD   ¢¡ Td hd Tn hn 24¯±° – Tb, where Td and Tn are day and night time temperatures, hd and hn are hours duration of day and night temperatures, Tb is the base line temperature for species for which no leaf initiation occurs. For Glycine max, Tb was 5°C, 6°C for Abutilon theophrasti, and 13°C for Cassia obtusifolia L. Because the Tb was not known for the other species, a DD analysis was not done. DD, substituted for the time variable, and PI were used in similar linear and quadratic regression analyses. Plastochron rates for dicots were also determined by substituting PI for time in calculating branching rates: BR = Bf  Bo tf  to , where to is time of first measurement day that branches were first present, tf is time of final harvest, and Bf and Bo are number of tillers, branches, and branch leaves at to and tf, respectively. Higher temperatures significantly increased plastochron rates in all species except quack grass at ambient CO2 levels. Calculating plastochron rates on a degree-day basis eliminated effects of temperature but not the effects of CO2. Elevated CO2 increased plastochron rates where significant effects were found. These results support the conclusion of Ackerly et al. (1992) that developmental responses to elevated CO2 depend on growth temperature and furthermore suggests that such responses also depend on species and the aspect of development being considered. This kind of information is necessary to develop crop and weed growth models given expected future higher temperatures and CO2 levels. Strauss et al. (2006, 2007) and Strauss and van Heerden (2011) quantified the vegetative development of soybean by repeated measurement of PIs of treatment plant groups before induction of dark chilling stress using R = 25 mm of central leaflets. Use of the PI insured that plants of all genotypes were at a comparable stage of vegetative development before the dark chilling stress was initiated when a particular genotype

November 2014]

MEICENHEIMER–PLASTOCHRON INDEX REVIEW

reached PI 5. The effect of dark chilling was measured by the increase in PI during the 12-d treatment. Pisum— A challenge with regard to developing a PI for Pisum sativum L. is the heteroblastic morphology of the compound leaf and the terminal foliar tendril component of this leaf. Meicenheimer et al. (1983) used a reference radius of 0.2 mm from the center of the apex to the central protoxylem elements or procambium of leaf primordia as viewed in transverse section at the level of the SAM summits to calculate PI for various P. sativum mutants in which the stipules had reduced morphology (st); tendrils replaced leaflets (af); leaflets terminated tendrils (tl); and wild type. LPI facilitated comparison among leaf primordia of similar morphological ages in each of these mutants and combinations of genotypes. It was observed that the small terminal leaflet lamina of the acacia leaf (tl) was produced by adaxial and marginal meristems that became apparent in the distal portion of the tendril late in leaf ontogeny. The reduced stipule (st) morphology arose from early loss of abaxial and adaxial stipule marginal meristems. The enhanced final width of stipules in the triple recessive combination was attributed to the persistence of the adaxial stipular marginal meristem in this phenotype, compared with the single and double st combinations. Kara and Zamolodchikov (1991) assessed the plastochron of cultured SAMs of P. sativum as the time that elapsed between the attainment of equal lengths of primordia 9 and 10 on the cultured SAMs. Wimmers and Turgeon (1991) used a 10-mm reference length on peas grown under controlled environmental conditions to calculate PI and LPI, which were used to pool similarly aged leaves from which disks were removed to assess sucrose influx as a function of leaf age under different light conditions. These workers determined that pea leaves attained 50% and 100% final area at 1.2 and 2.0 LPI, respectively. The increase in sucrose flux in high-light leaves compared with lowlight leaves was explicable on the basis of an increase in plasmalemma surface area under high-light conditions. It was concluded that in the intact leaves a standing osmotic gradient might facilitate transport of solute into transfer cells with extensive cell wall ingrowths. The rate of sucrose influx depended on leaf age. No difference in uptake was detected in high- and lowlight leaf disks until after 1.5 LPI. The uptake of sucrose declined between 1.5 and 2.0 LPI under both light conditions and was relatively constant between 2.0 and 3.0 LPI. A greater decrease in uptake in disks from low-light leaves accounted for the difference in mature leaf uptake. Leaves reached full expansion at 2.0–2.2 LPI and the sink to source transition occurs between 1.5–1.8 LPI (Wimmers and Turgeon, 1991). Baigorri et al. (1999) used R = 20 mm reference leaf length of two cultivars, one with normal leaflet and stipule sizes and the other, a semileafless variety in which leaflets were replaced with tendrils, but stipules were normal size, in glasshousegrown plants. These workers concluded that drought affected the plastochron as indicated by the PI. In normal and semi leafless types leaves, drought stress prolonged the plastochron, but by experiment end, both control and drought-stressed plants had produced the same number of leaves in normal type, but significantly fewer leaves in the semi leafless variety. Ade-Ademilua and Botha (2005) investigated the use of internode length to calculate PI, as suggested by Erickson and Michelini (1957), with each leaf assigned the same serial number as that of the subtending leaf and R = 20 mm. These workers observed that Pisum internodes and stipules were not prime

1831

candidates for PI calculations in that there were not two accessible organs spanning the exponential phase of growth that could be nondestructively measured. These workers concluded that R = 20 mm for the average of the two basal leaflets worked well for nondestructive determination of PI in Pisum sativum. The standard error of PI, calculated on this basis, was less than an hour. The plastochron of P. sativum was defined as the time between initiation of successive first pairs of leaflets. The use of mean length of successive leaflets was suggested for other plants with compound leaves, with the caveat that the same leaflet pair be used. It would also seem appropriate to consider the developmental sequence of leaflets along the rachis in selecting the best leaflets to use in this regard. Ade-Ademilua and Botha (2005) noted that this method of PI calculation was inappropriate before node 5, since node 0 = cotyledons, 1 and 2 are scale leaves, and 3 and 4, although the first true compound leaves, remain small throughout development. Ludidi et al. (2007) began PI measurement of various graft combinations, 20 d after grafting. A considerable difference in PI of different graft combinations was observed after 20 d, as well as considerable differences in stem growth rates of different graft combinations. A strong linear correlation was demonstrated between shoot length and nodule numbers among these different graft combinations. Arabidopsis— Groot and Meicenheimer (2000) established the validity of a PI for the Columbia-1 ecotype and serrate (se) mutant of Arabidopsis thaliana (L.) Heynh., based on a reference leaf length of 3 mm. Detailed statistical analysis revealed that when these plants were grown under a 10-h light/14-h dark photoperiod at constant 22°C, leaves 11–37 successfully fulfilled the three PI assumptions and could be used to investigate the developmental basis for the more prominent tooth formation in serrate leaves. That study revealed that the relative growth rate (RGR) of Col-1 was 1.25 greater than that of the se mutant and its plastochron was 1.5 longer than that of Col-1. Using the 30-plastochron window of study, Groot and Meicenheimer (2000) subsequently determined that the teeth of the se mutant were initiated 15 plastochrons earlier than in Col-1. In addition, while the RGR of Col-1 leaves was constant throughout development, the RGR of the se mutant leaves was biphasic, with the latter phase of growth equal to that of Col-1, but the early phase was one half the value of this RGR. The interactions between time of leaf and tooth initiation and the early phase of leaf expansion were obscured when only allometric analysis of Col-1 and se mutant leaf development was conducted, thereby reinforcing the utility of the PI in elucidating the developmental basis of vegetative mutants. Crone and Lord (1993) developed an inflorescence plastochron index for Arabidopsis thaliana Landsberg erecta to compare development in clavata1-1 mutants and wild-type flowers, based on a 4-mm reference length. Use of this index allowed them to observe that mutant clavata1-1 initiated flowers faster but these grew slower than wild-type flowers. Stages of sepal and stamen initiation were prolonged whereas carpel initiation was similar to wild type. These workers proposed that clavata1-1 was a heterochronic mutant, where the increase in number of floral organs partially resulted from the prolongation of floral organ initiation stages. Interestingly, these authors thanked R. O. Erickson for a discussion that led to the development of their inflorescence index. Allometric analysis revealed clearly that clavata1-1 gynoecia were shorter and wider than wild type. Use of the plastochron index enabled these workers

1832

[Vol. 101

AMERICAN JOURNAL OF BOTANY

to recognize that the mechanism for the clavata1-1 gene was to prolong apical growth during the organ initiation stages. Crone and Lord (1994) used an inflorescence floral plastochron index associated with the main shoot axis to study the timing of cytological events associated with the initiation of the four types of floral primordia in A. thaliana Landsberg erecta. They determined that floral organs produced by the homeotic mutants, apetala2-1 and agamous-1 were similar to wild-type floral organs with regard to cell division events associated with the initiation, size, and number of cells and that the phenotypes of the floral organs characteristic of these mutants arose by changes in tissue differentiation events that diverged from wild type events after the initiation and early development of the primordia (Crone and Lord, 1994). An excellent review of the use of the PI in studies on heterochronic mutants in flower development was provided by Lord et al. (1994). CONCLUSIONS AND PROJECTIONS I have tried to provide an overview of studies conducted on a number of taxa to illustrate the widespread utility of the PI and LPI concepts in furthering our progress in both applied and basic plant science. Previous reviews and users of the PI have repeatedly pointed out that the PI allows investigators to detect developmental trends that might be confounded by environmental variation. So this fundamental utility of the PI, while reflected and substantiated in this review, will not be reiterated, save to say, that the PI literature bears out this observation. I foresee that this fundamental aspect of the PI will continue to be used by future researchers to great advantage. It is easy to project that the utility of the PI and LPI will continue far into the future. These concepts will enhance the temporal resolution of studies on plants using an ever-expanding repertoire of analytic techniques. Once the three underlying assumptions of the PI have been verified and a workable reference organ length, R, established, there are various ways in which the PI and LPI/SUPI have and can be used. For convenience, and hopefully, a source of inspiration, this concluding section describes the general experimental schemes of such employment, which the interested reader can adapt for their own studies. Rigorous selection of experimental plant groups—The PI has often been employed to carefully match individual plants from a large population to establish closely matched experimental and control groups. The LPI has often been used to carefully treat organs of closely similar stages of development to receive experimental treatments within these groups. Assessment of the PI before and after experimental treatments can be used to reveal the effect of such treatments on the plastochron, relative plastochron, and chronologic growth rates of the organs under study. This analysis is quite instructive, since as we accumulate more information on gene function, those that influence the plastochron and relative rates of development continue to emerge. Enhanced temporal resolution— In studies designed to reveal the chronology of development of wild-type and mutant phenotypes, the PI can be used to detect periods of similar or divergent development. Within periods of similar development, the LPI can be used to more finely discriminate the temporal changes that occur at the genetic, physiologic, and structural levels of the organ under study. Within periods of divergent

development, comparisons of the plastochron, relative plastochron, and chronologic rates of change, allow us to detect to a more precise level exactly what has been altered between the different phases of development. Amassing sufficient quantities— One common problem in fine-tuning studies at physiological and/or genetic levels is the relative “massive” amounts of plant tissue required to isolate molecules of potential interest from organs of inordinately small dimensions. The PI and LPI can be used to advantage in these endeavors to diminish the variation within such laboriously collected samples, thereby enhancing the temporal resolution of the final analyses. Evolutionary-developmental studies— I would be remiss not to include Love’s (2010) philosophical observation, that while the PI has provided, and will continue to provide, a way to circumvent variability with regard to chronologic age and environmental conditions, we should ultimately strive to understand phenotypic plasticity within the broader context of evolution. How such a lofty endeavor might be achieved, at a quantitative level, is in the hands and minds of future investigators. Control of the plastochron—While the utility of the plastochron index appears to break down during critical stage transformations during development, this fact, serves to focus our attention, on those aspects of development that control the plastochron, as yet not understood. Why does the plastochron shorten between seedling and vegetative growth? Why does it further shorten between vegetative growth and reproductive growth? The plastochron index has been useful in documenting that it is the plastochron that is altered, not the relative chronological rates of growth, during these transitional periods. The underlying causality of this phenomenon remains to be elucidated. LITERATURE CITED ACKERLY, D. D., J. S. COLEMAN, S. R. MORSE, AND F. A. BAZZAZ. 1992. CO2 and temperature effects on leaf area production in two annual plant species. Ecology 73: 1260–1269. ADE-ADEMILUA, O. E., AND C. E. J. BOTHA. 2005. A re-evaluation of plastochron index determination in peas—A case for using leaflet length. South African Journal of Botany 71: 76–80. ASKENASY, E. 1880. Uber eine neue Methode, um die Vertheilung der Wachsthumsintensitat in wachsenden Theilen zu bestimmen. Naturhistorisch-Medizinischer Verein, Heidelberg Verhandlungen, neue serie 2: 70–153. BAIGORRI, H., M. C. ANTOLÍN, AND M. SÁNCHEZ-DIAZ. 1999. Reproductive response of two morphologically different pea cultivars to drought. European Journal of Agronomy 10: 119–128. BALLACH, H. J. 1997. Suitability and use of poplars as bioindicators—A new concept. Environmental Science and Pollution Research International 4: 37–45. BARLOW, P. W. 1994. Rhythm, periodicity and polarity as bases for morphogenesis in plants. Biological Reviews of the Cambridge Philosophical Society 69: 475–525. BEEMSTER, G. T. S., AND J. MASLE. 1996. The role of apical development around the time of leaf initiation in determining leaf width at maturity in wheat seedlings (Triticum aestivum L.) with impeded roots. Journal of Experimental Botany 47: 1679–1688. BROUNS, J. J. W. M. 1985. The plastochrone interval method for the study of the productivity of seagrasses; possibilities and limitations. Aquatic Botany 21: 71–88. BRÜGGEMANN, W., T. A. W. VAN DER KOOIJ, AND P. R. VAN HASSELT. 1992. Long-term chilling of young tomato plants under low light and subsequent

November 2014]

MEICENHEIMER–PLASTOCHRON INDEX REVIEW

recovery. 1. Growth, development and photosynthesis. Planta 186: 172–178. BURUNDUKOVA, O. L., M. V. SAPOTSKY, A. V. KOCHETOV, E. A. TRIFONOVA, AND V. I. MALINOVSKY. 2009. Dark and light green tissues of tobacco leaves systemically infected with tobacco mosaic virus. Biologia Plantarum 53: 294–300. CEULEMANS, R., AND I. IMPENS. 1979. Study of CO2 exchange processes, resistances to carbon-dioxide and chlorophyll content during leaf ontogenesis in poplar. Biologia Plantarum 21: 302–306. CEULEMANS, R., AND I. IMPENS. 1980. Leaf gas-exchange processes and related characteristics of 7 popular clones under laboratory conditions. Canadian Journal of Forest Research 10: 429–435. CEULEMANS, R., I. IMPENS, F. HEBRANT, AND R. MOERMANS. 1980. Evaluation of field productivity for several poplar clones based on their gas-exchange variables determined under laboratory conditions. Photosynthetica 14: 355–362. CEULEMANS, R., I. IMPENS, AND V. STEENACKERS. 1988. Genetic variation in aspects of leaf growth of Populus clones, using the leaf plastochron index. Canadian Journal of Forest Research 18: 1069–1077. CHEN, C. C., H. CHEN, AND Y. R. CHEN. 2009. A new method to measure leaf age: Leaf measuring-interval index. American Journal of Botany 96: 1313–1318. CHEN, S. L., AND L. R. TOWILL. 1970. Isoenzyme patterns in developing Xanthium leaves. Physiologia Plantarum 23: 434–443. CIARDI, J. A., J. DEIKMAN, AND M. D. ORZOLEK. 1997. Increased ethylene synthesis enhances chilling tolerance in tomato. Physiologia Plantarum 101: 333–340. CLIMENT, J., A. K. DANTAS, R. ALIA, AND J. MAJADA. 2013. Clonal variation for shoot ontogenetic heteroblasty in maritime pine (Pinus pinaster Ait.). Trees—Structure and Function 27: 1813–1819. COLEMAN, W. K., AND R. I. GREYSON. 1976. Growth and development of leaf in tomato (Lycopersicon esculentum). 1. Plastochron index, a suitable basis for description. Canadian Journal of Botany-Revue 54: 2421–2428. CORDERO, R. E., AND J. E. GUNCKEL. 1982. The effects of acute and chronic gamma-irradiation on Lupinus albus L. 2. Effects of acute irradiation on floral development. Environmental and Experimental Botany 22: 127–137. CRONE, W., AND E. M. LORD. 1993. Flower development in the organ number mutant clavata1-1 of Arabidopsis thaliana (Brassicaceae). American Journal of Botany 80: 1419–1426. CRONE, W., AND E. M. LORD. 1994. Floral organ initiation and development in wild-typr Arabidopsis thaliana (Brassicaceae) and in the organ identity mutants apetala2-1 and agamous-1. Canadian Journal of Botany 72: 384–401. DAGOSTINO, G., A. APPIANO, AND S. PENNAZIO. 1982. Cytological observations on natural senescence in tobacco leaves. Caryologia 35: 364–365. DALE, J. E. 1988. The control of leaf expansion. Annual Review of Plant Physiology and Plant Molecular Biology 39: 267–295. DEKANKOVA, K., AND T. JESKO. 1987. A method of average plastochrone index determination for plants of the maize type. Biologia 42: 27–32. DERRICK, P. M., S. A. CARTER, AND R. S. NELSON. 1997. Mutation of the tobacco mosaic tobamovirus 126- and 183-kDa proteins: Effects on phloem-dependent virus accumulation and synthesis of viral proteins. Molecular Plant-Microbe Interactions 10: 589–596. DOLSTRA, O., J. H. VENEMA, P. J. GROOT, AND P. R. VAN HASSELT. 2002. Low-temperature-related growth and photosynthetic performance of alloplasmic tomato (Lycopersicon esculentum Mill.) with chloroplasts from L. hirsutum Humb. & Bonpl. Euphytica 124: 407–421. DUARTE, C. M., N. MARBA, N. AGAWIN, J. CEBRIAN, S. ENRIQUEZ, M. D. FORTES, M. E. GALLEGOS, ET AL. 1994. Reconstruction of seagrass dynamics—Age determinations and associated tools for seagrass. Marine Ecology Progress Series 107: 195–209. ECHAVARRÍA-HERAS, H., E. SOLANA-ARELLANO, C. LEAL-RAMÍREZ, AND O. CASTILLO. 2013. Using allometric procedures to substantiate the plastochrone method for eelgrass leaf growth assessments. Theoretical Biology & Medical Modelling 10: 34. ERICKSON, R. O. 1960. Nomogram for the plastochron index. American Journal of Botany 47: 350–351.

1833

ERICKSON, R. O. 1976. Modeling of plant growth. Annual Review of Plant Physiology and Plant Molecular Biology 27: 407–434. ERICKSON, R. O. 1991. How does your garden grow—a citation classic commentary on the plastochron index by Erickson, R. O. and Michelini, F. J. Current Contents/Agriculture Biology &. Environmental Sciences 6: 10. ERICKSON, R. O., AND R. D. MEICENHEIMER. 1977. Photoperiod induced change in phyllotaxis in Xanthium. American Journal of Botany 64: 981–988. ERICKSON, R. O., AND F. J. MICHELINI. 1957. The plastochron index. American Journal of Botany 44: 297–305. ESAU, K. 1953. Plant anatomy. John Wiley, New York, New York, USA. ESAU, K. 1965. Plant anatomy, 2nd ed. John Wiley, New York, New York, USA. FLEMING, A. J., T. MANDEL, I. ROTH, AND C. KUHLEMIER. 1993. The patterns of gene expression in the tomato shoot apical meristem. Plant Cell 5: 297–309. FROST, C. J., B. NYAMDARI, C. J. TSAI, AND S. A. HARDING. 2012. The tonoplast- localized sucrose transporter in Populus (ptasut4) regulates whole-plant water relations, responses to water stress, and photosynthesis. PLOS ONE 7: 10. GAUDILLERE, J. P., AND M. MOUSSEAU. 1989. Short term effect of CO2 enrichment on leaf development and gas exchange of young poplars (Populus euramericana CV-I-214). Acta Oecologica-Oecologia Plantarum 10: 95–105. GOODYEAR, S. N., AND D. P. ORMROD. 1988. Tomato response to concurrent and sequential NO2 and O3 exposures. Environmental Pollution 51: 315–326. GOODYEAR, S. N., AND D. P. ORMROD. 1991. Within photoperiod differences in ozone sensitivity of soybean and tomato. Canadian Journal of Plant Science 71: 269–278. GOULD, G. G., C. G. JONES, P. RIFLEMAN, A. PEREZ, AND J. S. COLEMAN. 2007. Variation in eastern cottonwood (Populus deltoides Bartr.) phloem sap content caused by leaf development may affect feeding site selection behavior of the aphid, Chaitophorous populicola Thomas (Homoptera: Aphididae). Environmental Entomology 36: 1212–1225. GROOT, E. J., AND R. D. MEICENHEIMER. 2000. Short-day-grown Arabidopsis thaliana satisfies the assumptions of the plastochron index as a time variable in development. International Journal of Plant Sciences 161: 749–756. HALE, J. C., D. P. ORMROD, P. J. LAFFEY, AND O. B. ALLEN. 1985. Effects of nickel and copper mixtures on tomato in sand culture. Environmental Pollution Series A, Ecological and Biological 39: 53–69. HANADA, K., AND S. YONG SON. 1974. On the expression of plant age of soybean by means of plastochron index. Proceedings of Crop Science Society Japan 43: 8–28. HANSON, P. J., R. E. DICKSON, J. G. ISEBRANDS, T. R. CROW, AND R. K. DIXON. 1986. A morphological index of Quercus seedling ontogeny for use in studies of physiology and growth. Tree Physiology 2: 273–281. HAUN, J. R. 1973. Visual quantification of wheat development. Agronomy Journal 65: 116–119. HICKLENTON, P. R., AND P. A. JOLLIFFE. 1978. Effects of greenhouse CO2 enrichment on yield and photosynthetic physiology of tomato plants. Canadian Journal of Plant Science 58: 801–817. HICKLENTON, P. R., AND P. A. JOLLIFFE. 1980. Alterations in the physiology of CO2 exchange in tomato plants grown in CO2-enriched atmospheres. Canadian Journal of Botany 58: 2181–2189. HILL, J. P., AND E. M. LORD. 1990. A method for determining plastochron indexes during heteroblastic shoot growth. American Journal of Botany 77: 1491–1497. HILL, J. P., AND R. L. MALMBERG. 1991. Rates of corolla growth in tobacco determined with the plastochron index. Planta 185: 472–478. HORSLEY, S. B., AND K. W. GOTTSCHALK. 1989. Ontogenic changes in leaf development and photosynthesis of Prunus serotina seedlings. Annales des Sciences Forestieres 46: S490–S492. JAIN, T. C. 1970. Morphological aspects of leaf growth in Zea mays. Israel Journal of Botany 19: 42–45.

1834

AMERICAN JOURNAL OF BOTANY

JACOBS, R. F. W. M. 1979. Distribution and aspects of the production and biomass of eelgrass, Zostera marina L., at Roscoff, France. Aquatic Botany 7: 151–172. JENNINGS, D. H. 1976. Effects of sodium chloride on higher plants. Biological Reviews of the Cambridge Philosophical Society 51: 453–486. KARA, A. N., AND D. G. ZAMOLODCHIKOV. 1991. Effects of gibberellin and kinetin on development of pea shoot apices invitro. Soviet Plant Physiology 38: 814–821. LAMOREAUX, R. J., W. R. CHANEY, AND K. M. BROWN. 1978. The plastochron index: A review after two decades of use. American Journal of Botany 65: 586–593. LARSON, P. R. 1975. Development and organization of primary vascular system in Populus deltoides according to phyllotaxy. American Journal of Botany 62: 1084–1099. LARSON, P. R. 1976. Procambium v. cambium and protoxylem vs. metaxylem in Populus deltoides seedlings. American Journal of Botany 63: 1332–1348. LARSON, P. R. 1977. Phyllotactic transitions in vascular system of Populus deltoides Bartr. as determined by C14 Labeling. Planta 134: 241–249. LARSON, P. R. 1980a. Control of vascularization by developing leaves. In C. H. A. Little [ed.], Control of shoot growth in trees, Proceedings of the joint workshop of IUFRO working parties on Xylem Physiology (S2.01-10) and Shoot Growth Physiology (S2.01-11: July 20-24, 1980, Fredericton, New Brunswick, Canada, 157–172. International Union of Forest Research Organizations; Maritimes Forest Research Centre, Fredericton, New Brunswick, Canada. LARSON, P. R. 1980b. Interrelations between phyllotaxis, leaf development and the primary- secondary vascular transition in Populus deltoides. Annals of Botany 46: 757–769. LARSON, P. R., AND J. G. ISEBRANDS. 1971. The plastochron index as applied to developmental studies of cottonwood. Canadian Journal of Forest Research 1: 1–11. LASCOUX, D., E. PAINO, R. SIERRA DE GRADO, A. KREMER, AND I. DORMLING. 1993. Maturation of maritime pine (Pinus pinaster Ait.) seedlings after exposure to a period of continuous light. Tree Physiology 12: 363–378. LORD, E. M., W. CRONE, AND J. P. HILL. 1994. Timing of events during flower organogenesis: Arabidopsis as a model system. Current Topics in Developmental Biology 29: 325–356. LOVE, A. C. 2010. Idealization in evolutionary developmental investigation: A tension between phenotypic plasticity and normal stages. Philosophical Transactions of the Royal Society, B, Biological Sciences 365: 679–690. LUDIDI, N. N., T. K. PELLNY, G. KIDDLE, C. DUTILLEUL, K. GROTEN, P. D. R. VAN HEERDEN, S. DUTT, ET AL. 2007. Genetic variation in pea (Pisum sativum L.) demonstrates the importance of root but not shoot C/N ratios in the control of plant morphology and reveals a unique relationship between shoot length and nodulation intensity. Plant, Cell & Environment 30: 1256–1268. MAKSYMOWYCH, R., J. O. BROOKS, AND F. B. SALISBURY. 1990. Analysis of growth and development of Xanthium. Cambridge University Press, Cambridge, UK. MAKSYMOWYCH, R., R. E. CORDERO, AND R. O. ERICKSON. 1976. Long term developmental changes in Xanthium induced by gibberellic acid. American Journal of Botany 63: 1047–1053. MAKSYMOWYCH, R., AND R. O. ERICKSON. 1977. Phyllotaxis in Xanthium shoots altered by gibberellic acid. Science 196: 1201–1203. MAKSYMOWYCH, R., A. B. MAKSYMOWYCH, AND J. A. J. ORKWISZEWSKI. 1985. Stem elongation of Xanthium plants presented in terms of relative elemental rates. American Journal of Botany 72: 1114–1119. MAKSYMOWYCH, R., AND J. A. J. ORKWISZEWSKI. 1993. The role of nodal regions in growth of Xanthium (Compositae) stem. American Journal of Botany 80: 1318–1322. MAKSYMOWYCH, R., J. A. J. ORKWISZEWSKI, AND A. B. MAKSYMOWYCH. 1989. Regions of cell division and elongation during stem growth of Xanthium. American Journal of Botany 76: 1556–1558. MALINOVSKII, V. I., L. D. SELETSKAYA, L. A. VARFOLOMEEVA, AND N. S. KUGUK. 1993. Effect of tobacco mosaic virus on the viability of protoplasts and cells isolated from the leaves of sensitive and hypersensitive tobacco plants. Russian Journal of Plant Physiology:

[Vol. 101

A Comprehensive Russian Journal on Modern Phytophysiology 40: 678–682. MALINOVSKII, V. I., L. D. SELETSKAYA, L. A. VARFOLOMEEVA, N. S. KUGUK, AND Y. N. ZHURAVLEV. 1994. Effect of hypersensitive stock infection on the transport and accumulation of tobacco mosaic virus in leaves of sensitive and hypersensitive tobacco grafts. Russian Journal of Plant Physiology: A Comprehensive Russian Journal on Modern Phytophysiology 41: 103–107. MCCAULEY, M., AND J. CROXDALE. 1984. Establishment of a plastochron index for Dianthus chinensis L. American Journal of Botany 71: 1373–1381. MCCOOL, P. M., AND J. A. MENGE. 1983. Influence of ozone on carbon partitioning in tomato: Potential role of carbon flow in regulation of the mycorrhizal symbiosis under conditions of stress. New Phytologist 94: 241–247. MCCOOL, P. M., J. A. MENGE, AND O. C. TAYLOR. 1982. Effect of ozone injury and light stress on response of tomato to infection by the vesicular arbuscular mycorrhizal fungus, Glomus fasciculatus. Journal of the American Society for Horticultural Science 107: 839–842. MCMASTER, G. S. 1997. Phenology, development, and growth of the wheat (Triticum aestivum L) shoot apex: A review. In D. L. Sparks [ed.], Advances in Agronomy 59: 63–118. Elsevier Academic Press, San Diego, California, USA. MCMASTER, G. S. 2005. Phytomers, phyllochrons, phenology and temperate cereal development. Journal of Agricultural Science 143: 137–150. MEICENHEIMER, R. D. 1979. Relationships between shoot growth and changing phyllotaxy of Ranunculus. American Journal of Botany 66: 557–569. MEICENHEIMER, R. D. 1981. Changes in Epilobium phyllotaxy induced by N-1-naphthylphthalamic acid and α-4-chlorophenoxyisobutyric acid. American Journal of Botany 68: 1139–1154. MEICENHEIMER, R. D. 1992. Cellular basis for growth and tissue differentiation patterns in Linum usitatissimum (Linaceae) stems: The stem unit. American Journal of Botany 79: 914–920. MEICENHEIMER, R. D. 2006. Stem unit growth analysis of Linum usitatissimum (Linaceae) internode development. American Journal of Botany 93: 55–63. MEICENHEIMER, R. D., AND P. R. LARSON. 1983. Empirical models for xylogenesis in Populus deltoides. Annals of Botany 51: 491–502. MEICENHEIMER, R. D., AND P. R. LARSON. 1985. Exogenous auxin and N-1naphthylphthalamic acid effects on Populus deltoides xylogenesis. Journal of Experimental Botany 36: 320–329. MEICENHEIMER, R. D., F. J. MUEHLBAUER, J. L. HINDMAN, AND E. T. GRITTON. 1983. Meristem characteristics of genetically modified pea (Pisum sativum) leaf primordia. Canadian Journal of Botany 61: 3430–3437. MERRILL, E. K. 1986. Heteroblastic seedlings of green ash. 1. Predictability of leaf form and primordia length. Canadian Journal of Botany 64: 2645–2649. MICHELINI, F. J. 1958. The plastochron index in developmental studies of Xanthium italicum Moretti. American Journal of Botany 45: 525–533. MILTAU, O., D. ZAMIR, AND J. RUDICH. 1986. Growth rates of Lycopersicon species at low temperatures. Zeitschrift Fur Pflanzenzuchtung-Journal of Plant Breeding 96: 193–199. MIYAMOTO, N., M. GOTO, Y. MATSUI, Y. UKAI, M. MORITA, AND K. NEMOTO. 2004. Quantitative trait loci for phyllochron and tillering in rice. Theoretical and Applied Genetics 109: 700–706. NIKLAS, K. J. 1991. The elastic moduli and mechanics of Populus tremuloides (Salicaceae) petioles in bending and torsion. American Journal of Botany 78: 989–996. PARDOS, M., R. CALAMA, AND J. CLIMENT. 2009. Difference in cuticular transpiration and sclerophylly in juvenile and adult pine needles relates to the species-specific rates of development. Trees—Structure and Function 23: 501–508. PARK, S. J., K. JIANG, M. C. SCHATZ, AND Z. B. LIPPMAN. 2012. Rate of meristem maturation determines inflorescence architecture in tomato. Proceedings of the National Academy of Sciences, USA 109: 639–644. PATRIQUIN, D. G. 1973. Estimation of growth rate, production and age of the marine angiosperm Thalassia testudinum Konig. Caribbean Journal of Science 13: 111–123.

November 2014]

MEICENHEIMER–PLASTOCHRON INDEX REVIEW

PRUSINKIEWICZ, P. 1998. Modeling of spatial structure and development of plants: A review. Scientia Horticulturae 74: 113–149. RICHARDS, F. J. 1951. Phyllotaxis: Its quantitative expression and relation to growth in the apex. Proceedings of the Royal Society of Edinburgh, B, Biology 235: 510–564. ROWAN, B. A., AND A. J. BENDICH. 2009. The loss of DNA from chloroplasts as leaves mature: Fact or artefact? Journal of Experimental Botany 60: 3005–3010. SCHMIDT, A. 1924. Histologische Studien an phanerogamen Vegetationspunkte. Botanical Archives 8: 345–404. SILK, W. K. 1980. Plastochron indexes in cantaloupe grown on an irrigation line source. Botanical Gazette 141: 73–78. SILK, W. K. 1984. Quantitative descriptions of development. Annual Review of Plant Physiology and Plant Molecular Biology 35: 479–518. SILVIUS, J. E., D. F. KREMER, AND D. R. LEE. 1978. Carbon assimilation and translocation in soybean leaves at different stages of development. Plant Physiology 62: 54–58. SINHA, N., S. HAKE, AND M. FREELING. 1993. Genetic and molecular analysis of leaf development. Current Topics in Developmental Biology 28: 47–80. SNYDER, F. W., AND J. A. BUNCE. 1983. Use of the plastochron index to evaluate effects of light, temperature and nitrogen on growth of soya bean (Glycine max L. Merr.). Annals of Botany 52: 895–903. STRAUSS, A. J., AND P. D. R. VAN HEERDEN. 2011. Effects on both the roots and shoots of soybean during dark chilling determine the nature and extent of photosynthesis inhibition. Environmental and Experimental Botany 74: 261–271. STRAUSS, A. J., G. H. J. KRUGER, R. J. STRASSER, AND P. D. R. VAN HEERDEN. 2006. Ranking of dark chilling tolerance in soybean genotypes probed by the chlorophyll a fluorescence transient O-J-I-P. Environmental and Experimental Botany 56: 147–157. STRAUSS, A. J., G. H. J. KRUGER, R. J. STRASSER, AND P. D. R. VAN HEERDEN. 2007. The role of low soil temperature in the inhibition of growth and PSII function during dark chilling in soybean genotypes of contrasting tolerance. Physiologia Plantarum 131: 89–105. SWAN, D., D. M. BROWN, AND M. C. COLIGADO. 1981. Leaf emergence rates of corn (Zea mays L.) as affected by temperature and photoperiod. Agricultural Meteorology 24: 57–73.

1835

TREMMEL, D. C., AND D. T. PATTERSON. 1994. Effects of elevated CO2 and temperature on development in soybean and five weeds. Canadian Journal of Plant Science 74: 43–50. TRULL, M. C., AND R. L. MALMBERG. 1994. Puzzle box, a tobacco line with flowers that mix floral and inflorescence characteristics. American Journal of Botany 81: 582–588. TSAI, C. H., A. MILLER, M. SPALDING, AND S. RODERMEL. 1997. Source strength regulates an early phase transition of tobacco shoot morphogenesis. Plant Physiology 115: 907–914. TURGEON, R. 1984. Termination of nutrient import and development of vein loading capacity in albino tobacco leaves. Plant Physiology 76: 45–48. TURGEON, R. 1987. Phloem unloading in tobacco sink leaves: Insensitivity to anoxia indicates a symplastic pathway. Planta 171: 73–81. VALLEJOS, C. E., J. M. LYONS, R. W. BREIDENBACH, AND M. F. MILLER. 1983. Characterization of a differential low-temperature growth-response in 2 species of Lycopersicon: The plastochron as a tool. Planta 159: 487–496. VAN HEERDEN, P. D. R., M. DE BEER, D. J. MELLET, H. S. MAPHIKE, AND W. FOIT. 2007. Growth media effects on shoot physiology, nodule numbers and symbiotic nitrogen fixation in soybean. South African Journal of Botany 73: 600–605. VAN HEERDEN, P. D. R., R. J. STRASSER, AND G. H. J. KRUGER. 2004. Reduction of dark chilling stress in N2-fixing soybean by nitrate as indicated by chlorophyll a fluorescence kinetics. Physiologia Plantarum 121: 239–249. VENDELAND, J. S., T. R. SINCLAIR, S. C. SPAETH, AND P. M. CORTES. 1982. Assumptions of plastochron index: Evaluation with soya bean under field drought conditions. Annals of Botany 50: 673–680. VENEMA, J. H., P. LINGER, A. W. VAN HEUSDEN, P. R. VAN HASSELT, AND W. BRÜGGEMANN. 2005. The inheritance of chilling tolerance in tomato (Lycopersicon spp.). Plant Biology 7: 118–130. WIMMERS, L. E., AND R. TURGEON. 1991. Transfer cells and solute uptake in minor veins of Pisum sativum leaves. Planta 186: 2–12. ZHURAVLEV, Y. N., N. F. PISETSKAYA, AND V. A. LEDNEVA. 1983. Inhibition of tobacco mosaic-virus reproduction in isolated tobacco protoplasts by means of pancreatic ribonuclease. Phytopathologische ZeitschriftJournal of Phytopathology 106: 35–44.

The plastochron index: still useful after nearly six decades.

The plastochron index (PI) introduced by Erickson and Michelini in 1957 provides a solution to a long-standing problem, of how to measure time in grow...
793KB Sizes 2 Downloads 25 Views