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ScienceDirect Regulation of plant root system architecture: implications for crop advancement Eric D Rogers1 and Philip N Benfey1,2 Root system architecture (RSA) plays a major role in plant fitness, crop performance, and grain yield yet only recently has this role been appreciated. RSA describes the spatial arrangement of root tissue within the soil and is therefore crucial to nutrient and water uptake. Recent studies have identified many of the genetic and environmental factors influencing root growth that contribute to RSA. Some of the identified genes have the potential to limit crop loss caused by environmental extremes and are currently being used to confer drought tolerance. It is hypothesized that manipulating these and other genes that influence RSA will be pivotal for future crop advancements worldwide. Addresses 1 Department of Biology and Duke Center for Systems Biology, Duke University, Durham, NC 27708, USA 2 Howard Hughes Medical Institute, Duke University, Durham, NC 27708, USA Corresponding author: Benfey, Philip N ([email protected])
Current Opinion in Biotechnology 2015, 32:93–98 This review comes from a themed issue on Plant biotechnology Edited by Inge Broer and George N Skaracis
http://dx.doi.org/10.1016/j.copbio.2014.11.015 0958-1669/# 2014 Elsevier Ltd. All rights reserved.
Introduction Root system architecture (RSA) describes the shape and spatial arrangement of a root system within the soil. It is a created by modulating the angle, rate of growth and type of individual roots contributing to the root system. RSA is pivotal for plant anchorage and efficient uptake of water and nutrients, and can have a major impact on fertilizer usage and yield in crops worldwide. The heterogeneous nature of the surrounding environment results in an RSA that is highly plastic and be composed of many root types with specific functions [1,2]. RSA is shaped by the interactions between genetic and environmental components that establish a framework with which the plant explores the soil and responds to external cues that dictate future growth patterns (Figure 1). RSA can provide a growth advantage in specific environmental settings (e.g. drought) and directly influences the aerial parts of the www.sciencedirect.com
plant that impact yield. Poor soil fertility and environmental stress suppress crop yields in many parts of the world; therefore, much effort has gone into identifying the genetic programs that underlie RSA with the goal of developing crops with improved performance, which would have profound significance for agriculture and food security. Several genetic components influencing RSA and root growth have been characterized at the molecular level but their effects on yield have yet to be tested in crop species [3]. This review will highlight some of the recently identified genetic components and environmental factors influencing RSA that have a direct application to plants of agronomic importance, with the hope that these factors could be exploited to advance food production.
Cereal root types are formed by specific genetic components The RSA of cereal crops is composed of multiple embryonic (primary and seminal) and postembryonic (lateral, crown and brace) roots (Figure 2). The primary root is formed at the basal pole of the embryo, whereas seminal roots are formed at the scutellar node. Many cereal species such as rice lack seminal roots entirely. The primary and seminal roots are important for early vigor and establish a framework to explore the soil for nutrients and water. Crown and brace roots (also called nodal roots) emerge from underground and aboveground shoot nodes, respectively, providing lodging resistance and play an important role in the uptake of water and nutrients. Lateral roots are formed on all roots within the soil and function to increase water and nutrient uptake. Transcriptional profiling has been a useful tool to study both the function and developmental pathways of the individual root types (Figure 2). In maize and sorghum brace roots, the most abundant transcripts encode enzymes related to metabolism and energy production [4]. Many additional genes have been identified that are involved in the formation of postembryonic roots in maize and rice [5,6]. The hormone strigolactone has recently been shown to impact various aspects of shoot growth but also appears to be a general mediator of root growth. In rice, strigolactone is required for crown root elongation and nutrient mediated primary and lateral root growth [7,8,9]. Many additional hormones and genes have been identified that influence root type-specific growth as a result of symbiotic interactions within the soil rhizosphere [3,10,11]. These studies suggest that RSA is influenced by interactions between genes, signaling molecules, and Current Opinion in Biotechnology 2015, 32:93–98
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Figure 1
Figure 3
Genes Genes
Immature RSA
(a) Phosphorus Nitrogen Water
Mature RSA
Environment
RSA Deep roots
Current Opinion in Biotechnology
RSA is shaped by the interactions between genes and the environment. Immature RSA is primarily established as a result of genetic components. Once RSA is established, RSA response to environmental extremes is determined by a combination of genetic and environmental components.
Yield ?
(b) Phosphorus Nitrogen Water
nutrient and water availability. Further knowledge of these interactions could allow RSA to be altered to achieve greater performance in a specific environment. For example, increasing crown root elongation or lateral root development to enhance phosphorus uptake, without limiting water acquisition (Figure 3).
Figure 2
Brace root
Crown root
Seminal root
Lateral root Primary root Current Opinion in Biotechnology
Root system architecture in cereals. Schematic of cereal RSA showing embryonic (primary and seminal) and postembryonic (lateral, crown and brace) roots. RSA is complicated by the fact that not all root types exist in all cereals. Maize has multiple seminal roots that emerge from the scutellar node whereas rice and sorghum lack seminal roots. The crown and brace roots emerge from consecutive shoot nodes located underground or aboveground, respectively. Maize, sorghum and rice all have crown roots, but only maize and sorghum have brace roots. Lateral roots can form from all roots that penetrate the soil, but are only depicted on the primary root for clarity. Current Opinion in Biotechnology 2015, 32:93–98
RSA Shallow roots
Yield ?
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Relationship between RSA, yield and soil heterogeneity. (a,b) Depiction of two plants having deep RSA (a) or shallow RSA (b). The relationship between RSA and yield is complicated by soil heterogeneity. There is not an optimal RSA that will confer a high yield in every environment. Phosphorus is primarily located near the soil surface, whereas nitrogen and water are frequently found deeper in the soil, especially late in the growing season. Phosphorus, nitrogen, and water are indicated by yellow, green, and blue dots, respectively.
Cereal RSA impacts yield and adult fitness As technology has improved many approaches have been taken to study quantitative aspects of the various root types. A non-invasive imaging technique has been developed that uses 3D imaging and digital phenotyping to quantify the shape, distribution, intrinsic root network size, and exploration of RSA [12]. This method was used to identify many quantitative trait loci (QTL) controlling RSA as well as central genomic regions controlling root growth in immature rice plants. Additional studies have complimented this approach by focusing on specialized root types in soil-grown plants. One such study combined shovelomics, a process of excavating and quantifying individual washed roots, with digital imaging to analyze the RSA in mature maize and cowpea grown under field conditions [13]. This method was capable of distinguishing ecotypes based on RSA changes and thus could be a powerful new tool to analyze RSA in field grown crops. Because RSA encompasses many root types with distinct functions (Figure 2), the individual roots of immature soil-grown maize were analyzed and several root type-specific QTLs were identified that could explain the correlation between RSA in immature plants and crop yield [12,14,15]. Many QTLs and root traits www.sciencedirect.com
Regulation of plant root system architecture Rogers and Benfey 95
have been identified that suggest there is a biological tradeoff in root growth allocation during root establishment that directly impacts nutrient acquisition and yield (Figure 1 and Table 1). These new methods provide a foundation to identify the genetic components contributing to RSA at any developmental stage, which could be used to improve crop performance.
Modulation of RSA confers drought tolerance Extremes in water availability are a major limiting factor to crop production worldwide. This section will focus on the impacts of drought on RSA, for a detailed review on root responses to flooding see [16]. Recent research has identified several genes in rice related to RSA that confer a yield advantage during conditions of drought (Table 1) [17,18,19,20,21]. In addition, several transcription factor gene families have been shown to influence abiotic stress tolerance (NAC, WRKY, AP2/ERF and DREB) [22–25]. The NAC family of transcription factors is best characterized with regard to RSA growth and root-specific overexpression of several members of this family in rice can provide a growth advantage during conditions of drought or high salinity [19–21]. The rate of root growth and root angle is a key factor contributing to water and nutrient uptake; RSA that is narrower and vertically oriented is typically more drought tolerant (Figure 3). Several QTLs for seminal root angle in wheat were recently shown to have major impacts on deep rooting and root growth angle [26]. The molecular mechanisms of nodal root growth are largely unknown, but several overlapping QTLs have been identified in rice, maize and sorghum that show a correlation between root angles and yield [27,28]. These overlapping QTLs suggest a conserved genetic mechanism for controlling Table 1 Genomic loci that confer advantageous RSA and yield Species
Gene/QTL
Wheat Sorghum Rice Rice Rice Rice Rice
QTL QTL HVA1 NAC10 NAC9 DRO1 NAC045
Sorghum
QTL
Maize
QTL
Rice Rice
LTN1 PSTOL1
Brachypodium
QTL
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RSA advantage
Reference
Drought tolerance Drought tolerance Drought tolerance Drought tolerance Drought tolerance Drought tolerance Salinity and drought tolerance Yield, lodging resistance and water/nutrient uptake Yield, lodging resistance and water/nutrient uptake Phosphorus uptake Yield in low phosphorus Growth in low nutrient conditions
[26] [28] [17] [19] [20] [30] [21] [27]
[29]
[38] [36] [40]
root angle in grasses. Additionally, several epistatic QTLs have been identified in maize brace root indicating that a complex genetic network controls nodal root formation and angles [29]. In rice, DEEPER ROOTING 1 (DRO1) has been shown to control deep root exploration, which increases yield under drought conditions [30]. DRO1 has gained much attention in the scientific community because its introduction into a shallow rooting cultivar resulted in deeper rooting and improved yield under drought conditions without adverse effects during nondrought conditions. Deeper rooting has a large genetic component that could be integrated into marker assisted breeding programs to optimize RSA in drought conditions. Identification of additional RSA genes that confer drought tolerance will provide more potential genetic targets for improving crop yield.
RSA responds to nutrient heterogeneity Because soil heterogeneity occurs in space and time, plants have adapted mechanisms to deal with limitations during both root establishment and late stage development. Nitrogen (N) and phosphorus (P) are vital to plant survival and therefore the dynamics of RSA response to these nutrients has been studied in great detail using experimental data and computer modeling [31,32,33]. Response to low P is species dependent but the general observations include primary root growth inhibition, increase in lateral roots and root hairs, and cluster root formation. The general response to low N includes an increase in vertical, deep roots with fewer roots near the soil surface. However, modeling N uptake predicts a dynamic RSA in response to N and suggests shallow roots are advantageous during root establishment but deep roots are preferential later in development [34]. Based on these and other observations, it has recently been proposed that an ideotype exists to maximize soil exploration for optimum water and nutrient acquisition termed ‘steep, cheap and deep’ (SCD) [35]. There are tradeoffs to the allocation of root biomass near the soil surface versus deep exploration (Figure 3). Rapid primary root growth plays a major role in nutrient uptake, thus it has been hypothesized that genes for early root growth may facilitate selection for efficient nutrient use. In agreement with this hypothesis, the PSTOL1 gene was recently identified as a crown root-specific kinase controlling root growth during low P [36,37]. In rice, a mutation in leaf tip necrosis1 (ltn1) results in longer crown roots and increased P uptake and accumulation [38]. Several QTLs in wheat have been identified that have major effects on seminal and lateral root growth, which are also associated with yield and N and P acquisition [39]. Characterization of RSA in two Brachypodium accessions under different N and P conditions identified key genetic and environmental-specific growth responses in response to low nutrients [40]. Collectively, these studies Current Opinion in Biotechnology 2015, 32:93–98
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indicate that specific root growth is crucial to efficient nutrient uptake. Arabidopsis has been a powerful tool to dissect the molecular mechanisms controlling root growth response to limiting nutrients. Two recent studies analyzed various combinations of nutrient deficiencies to show that RSA response is dependent on which combination of nutrients is deficient [41,42]. Plasticity in RSA was observed and responsive genes could be grouped into clusters, suggesting the presence of multiple nutrient-dependent developmental programs [43]. Although not directly applicable, these results resemble what is observed in many crop species. Therefore, it is hypothesized that RSA responses are conserved at the genetic level. Evidently studies in Arabidopsis may identify important orthologous genes in crop species. These studies show that RSA response to nutrient conditions is largely controlled by genetic components and that there may be an optimal RSA for each nutrient deficiency. RSA exhibits a high level of plasticity as a result of the environmental heterogeneity. Therefore, identifying the molecular mechanisms that control root growth response will be valuable to future food production.
Soil properties influence RSA Soil properties such as density and particle size vary greatly within a field and across a growing season, and greatly impact RSA and yield [44]. Recent studies using wheat and tomato show that higher soil compaction produces roots that are short with a large diameter resulting in an RSA that is very shallow and narrow effectively decreasing the extent of soil exploration [45,46]. In addition, root elongation is more influenced by mechanical and physical properties rather than chemical properties of soil [47–50]. It has been hypothesized that the shape of root tips and presence of root hairs aids in penetration and anchoring of roots within the soil. The ground slope also impacts RSA. For example, black locust trees grown in pots at a 458 slope developed shallow, welldeveloped roots, at the expense of depth [51]. Full understanding of how the physical properties of soil impact RSA will allow for the development of crops that can thrive in different soil types. High salinity is a major stress for crops worldwide. As a result, plants have devised mechanisms to avoid soil regions of high salinity and to alter RSA in response [3]. A recent study used Arabidopsis, tomato and sorghum to elucidate the molecular mechanism behind salt avoidance [52]. Although these experiments were performed on flat plates, one can extrapolate the results to field grown plants, which could have a great impact on soil exploration and subsequent yield. Comprehensive understanding of how RSA is influenced by high salinity will allow for selection of plants that have enhanced salt avoidance. About 20% of the world’s cropland is impacted Current Opinion in Biotechnology 2015, 32:93–98
by high salinity. Therefore, identifying an RSA that is better suited for growth under this condition could have a huge impact on food production worldwide.
Conclusions Over the past decade, many QTLs, genes and molecular pathways that control RSA have been discovered that have agronomical impact. However, very few have been successfully used to advance crop production. We have discussed a small subset of the recent discoveries that impact RSA with the belief that manipulating RSA will aid in developing crops with improved performance in many parts of the world. Different types of RSA provide growth advantages under different environmental conditions yet RSA has been largely under utilized in the breeding of many crops. There is a wealth of information regarding stress response genes and their impact on shoot development. However, the RSA response is largely unexplored and could be of great significance to yield. Therefore, RSA is a promising field that can be incorporated into existing breeding programs and has great potential to influence future food production.
Acknowledgements We thank members of the Benfey laboratory and the reviewers for helpful comments on this manuscript. Work in the Benfey lab is funded by grant GBMF3405 from the Howard Hughes Medical Institute and the Gordon and Betty Moore Foundation (to P.N.B.), and grant NSF-IOS-14-11750 from the National Science Foundation.
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39. Ren Y, He X, Liu D, Li J, Zhao X, Li B, Tong Y, Zhang A, Li Z: Major quantitative trait loci for seminal root morphology of wheat seedlings. Mol Breed 2012, 30:139-148. 40. Ingram PA, Zhu J, Shariff A, Davis IW, Benfey PN, Elich T: Highthroughput imaging and analysis of root system architecture in Brachypodium distachyon under differential nutrient availability. Philos Trans R Soc Lond B Biol Sci 2012, 367:1559-1569. 41. Gruber BD, Giehl RF, Friedel S, von Wiren N: Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 2013, 163:161-179. 42. Kellermeier F, Armengaud P, Seditas TJ, Danku J, Salt DE, Amtmann A: Analysis of the root system architecture of arabidopsis provides a quantitative readout of crosstalk between nutritional signals. Plant Cell 2014, 26:1480-1496. Characterized 13 Arabidopsis RSA traits using 32 binary combinations of nutrient deficiencies. Shows a very extensive analysis of how different combinations of nutrient deficiencies impact RSA.
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Current Opinion in Biotechnology 2015, 32:93–98
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ScienceDirect Regulation of plant root system architecture: implications for crop advancement Eric D Rogers1 and Philip N Benfey1,2 Root system architecture (RSA) plays a major role in plant fitness, crop performance, and grain yield yet only recently has this role been appreciated. RSA describes the spatial arrangement of root tissue within the soil and is therefore crucial to nutrient and water uptake. Recent studies have identified many of the genetic and environmental factors influencing root growth that contribute to RSA. Some of the identified genes have the potential to limit crop loss caused by environmental extremes and are currently being used to confer drought tolerance. It is hypothesized that manipulating these and other genes that influence RSA will be pivotal for future crop advancements worldwide. Addresses 1 Department of Biology and Duke Center for Systems Biology, Duke University, Durham, NC 27708, USA 2 Howard Hughes Medical Institute, Duke University, Durham, NC 27708, USA Corresponding author: Benfey, Philip N ([email protected])
Current Opinion in Biotechnology 2015, 32:93–98 This review comes from a themed issue on Plant biotechnology Edited by Inge Broer and George N Skaracis
http://dx.doi.org/10.1016/j.copbio.2014.11.015 0958-1669/# 2014 Elsevier Ltd. All rights reserved.
Introduction Root system architecture (RSA) describes the shape and spatial arrangement of a root system within the soil. It is a created by modulating the angle, rate of growth and type of individual roots contributing to the root system. RSA is pivotal for plant anchorage and efficient uptake of water and nutrients, and can have a major impact on fertilizer usage and yield in crops worldwide. The heterogeneous nature of the surrounding environment results in an RSA that is highly plastic and be composed of many root types with specific functions [1,2]. RSA is shaped by the interactions between genetic and environmental components that establish a framework with which the plant explores the soil and responds to external cues that dictate future growth patterns (Figure 1). RSA can provide a growth advantage in specific environmental settings (e.g. drought) and directly influences the aerial parts of the www.sciencedirect.com
plant that impact yield. Poor soil fertility and environmental stress suppress crop yields in many parts of the world; therefore, much effort has gone into identifying the genetic programs that underlie RSA with the goal of developing crops with improved performance, which would have profound significance for agriculture and food security. Several genetic components influencing RSA and root growth have been characterized at the molecular level but their effects on yield have yet to be tested in crop species [3]. This review will highlight some of the recently identified genetic components and environmental factors influencing RSA that have a direct application to plants of agronomic importance, with the hope that these factors could be exploited to advance food production.
Cereal root types are formed by specific genetic components The RSA of cereal crops is composed of multiple embryonic (primary and seminal) and postembryonic (lateral, crown and brace) roots (Figure 2). The primary root is formed at the basal pole of the embryo, whereas seminal roots are formed at the scutellar node. Many cereal species such as rice lack seminal roots entirely. The primary and seminal roots are important for early vigor and establish a framework to explore the soil for nutrients and water. Crown and brace roots (also called nodal roots) emerge from underground and aboveground shoot nodes, respectively, providing lodging resistance and play an important role in the uptake of water and nutrients. Lateral roots are formed on all roots within the soil and function to increase water and nutrient uptake. Transcriptional profiling has been a useful tool to study both the function and developmental pathways of the individual root types (Figure 2). In maize and sorghum brace roots, the most abundant transcripts encode enzymes related to metabolism and energy production [4]. Many additional genes have been identified that are involved in the formation of postembryonic roots in maize and rice [5,6]. The hormone strigolactone has recently been shown to impact various aspects of shoot growth but also appears to be a general mediator of root growth. In rice, strigolactone is required for crown root elongation and nutrient mediated primary and lateral root growth [7,8,9]. Many additional hormones and genes have been identified that influence root type-specific growth as a result of symbiotic interactions within the soil rhizosphere [3,10,11]. These studies suggest that RSA is influenced by interactions between genes, signaling molecules, and Current Opinion in Biotechnology 2015, 32:93–98
94 Plant biotechnology
Figure 1
Figure 3
Genes Genes
Immature RSA
(a) Phosphorus Nitrogen Water
Mature RSA
Environment
RSA Deep roots
Current Opinion in Biotechnology
RSA is shaped by the interactions between genes and the environment. Immature RSA is primarily established as a result of genetic components. Once RSA is established, RSA response to environmental extremes is determined by a combination of genetic and environmental components.
Yield ?
(b) Phosphorus Nitrogen Water
nutrient and water availability. Further knowledge of these interactions could allow RSA to be altered to achieve greater performance in a specific environment. For example, increasing crown root elongation or lateral root development to enhance phosphorus uptake, without limiting water acquisition (Figure 3).
Figure 2
Brace root
Crown root
Seminal root
Lateral root Primary root Current Opinion in Biotechnology
Root system architecture in cereals. Schematic of cereal RSA showing embryonic (primary and seminal) and postembryonic (lateral, crown and brace) roots. RSA is complicated by the fact that not all root types exist in all cereals. Maize has multiple seminal roots that emerge from the scutellar node whereas rice and sorghum lack seminal roots. The crown and brace roots emerge from consecutive shoot nodes located underground or aboveground, respectively. Maize, sorghum and rice all have crown roots, but only maize and sorghum have brace roots. Lateral roots can form from all roots that penetrate the soil, but are only depicted on the primary root for clarity. Current Opinion in Biotechnology 2015, 32:93–98
RSA Shallow roots
Yield ?
Current Opinion in Biotechnology
Relationship between RSA, yield and soil heterogeneity. (a,b) Depiction of two plants having deep RSA (a) or shallow RSA (b). The relationship between RSA and yield is complicated by soil heterogeneity. There is not an optimal RSA that will confer a high yield in every environment. Phosphorus is primarily located near the soil surface, whereas nitrogen and water are frequently found deeper in the soil, especially late in the growing season. Phosphorus, nitrogen, and water are indicated by yellow, green, and blue dots, respectively.
Cereal RSA impacts yield and adult fitness As technology has improved many approaches have been taken to study quantitative aspects of the various root types. A non-invasive imaging technique has been developed that uses 3D imaging and digital phenotyping to quantify the shape, distribution, intrinsic root network size, and exploration of RSA [12]. This method was used to identify many quantitative trait loci (QTL) controlling RSA as well as central genomic regions controlling root growth in immature rice plants. Additional studies have complimented this approach by focusing on specialized root types in soil-grown plants. One such study combined shovelomics, a process of excavating and quantifying individual washed roots, with digital imaging to analyze the RSA in mature maize and cowpea grown under field conditions [13]. This method was capable of distinguishing ecotypes based on RSA changes and thus could be a powerful new tool to analyze RSA in field grown crops. Because RSA encompasses many root types with distinct functions (Figure 2), the individual roots of immature soil-grown maize were analyzed and several root type-specific QTLs were identified that could explain the correlation between RSA in immature plants and crop yield [12,14,15]. Many QTLs and root traits www.sciencedirect.com
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have been identified that suggest there is a biological tradeoff in root growth allocation during root establishment that directly impacts nutrient acquisition and yield (Figure 1 and Table 1). These new methods provide a foundation to identify the genetic components contributing to RSA at any developmental stage, which could be used to improve crop performance.
Modulation of RSA confers drought tolerance Extremes in water availability are a major limiting factor to crop production worldwide. This section will focus on the impacts of drought on RSA, for a detailed review on root responses to flooding see [16]. Recent research has identified several genes in rice related to RSA that confer a yield advantage during conditions of drought (Table 1) [17,18,19,20,21]. In addition, several transcription factor gene families have been shown to influence abiotic stress tolerance (NAC, WRKY, AP2/ERF and DREB) [22–25]. The NAC family of transcription factors is best characterized with regard to RSA growth and root-specific overexpression of several members of this family in rice can provide a growth advantage during conditions of drought or high salinity [19–21]. The rate of root growth and root angle is a key factor contributing to water and nutrient uptake; RSA that is narrower and vertically oriented is typically more drought tolerant (Figure 3). Several QTLs for seminal root angle in wheat were recently shown to have major impacts on deep rooting and root growth angle [26]. The molecular mechanisms of nodal root growth are largely unknown, but several overlapping QTLs have been identified in rice, maize and sorghum that show a correlation between root angles and yield [27,28]. These overlapping QTLs suggest a conserved genetic mechanism for controlling Table 1 Genomic loci that confer advantageous RSA and yield Species
Gene/QTL
Wheat Sorghum Rice Rice Rice Rice Rice
QTL QTL HVA1 NAC10 NAC9 DRO1 NAC045
Sorghum
QTL
Maize
QTL
Rice Rice
LTN1 PSTOL1
Brachypodium
QTL
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RSA advantage
Reference
Drought tolerance Drought tolerance Drought tolerance Drought tolerance Drought tolerance Drought tolerance Salinity and drought tolerance Yield, lodging resistance and water/nutrient uptake Yield, lodging resistance and water/nutrient uptake Phosphorus uptake Yield in low phosphorus Growth in low nutrient conditions
[26] [28] [17] [19] [20] [30] [21] [27]
[29]
[38] [36] [40]
root angle in grasses. Additionally, several epistatic QTLs have been identified in maize brace root indicating that a complex genetic network controls nodal root formation and angles [29]. In rice, DEEPER ROOTING 1 (DRO1) has been shown to control deep root exploration, which increases yield under drought conditions [30]. DRO1 has gained much attention in the scientific community because its introduction into a shallow rooting cultivar resulted in deeper rooting and improved yield under drought conditions without adverse effects during nondrought conditions. Deeper rooting has a large genetic component that could be integrated into marker assisted breeding programs to optimize RSA in drought conditions. Identification of additional RSA genes that confer drought tolerance will provide more potential genetic targets for improving crop yield.
RSA responds to nutrient heterogeneity Because soil heterogeneity occurs in space and time, plants have adapted mechanisms to deal with limitations during both root establishment and late stage development. Nitrogen (N) and phosphorus (P) are vital to plant survival and therefore the dynamics of RSA response to these nutrients has been studied in great detail using experimental data and computer modeling [31,32,33]. Response to low P is species dependent but the general observations include primary root growth inhibition, increase in lateral roots and root hairs, and cluster root formation. The general response to low N includes an increase in vertical, deep roots with fewer roots near the soil surface. However, modeling N uptake predicts a dynamic RSA in response to N and suggests shallow roots are advantageous during root establishment but deep roots are preferential later in development [34]. Based on these and other observations, it has recently been proposed that an ideotype exists to maximize soil exploration for optimum water and nutrient acquisition termed ‘steep, cheap and deep’ (SCD) [35]. There are tradeoffs to the allocation of root biomass near the soil surface versus deep exploration (Figure 3). Rapid primary root growth plays a major role in nutrient uptake, thus it has been hypothesized that genes for early root growth may facilitate selection for efficient nutrient use. In agreement with this hypothesis, the PSTOL1 gene was recently identified as a crown root-specific kinase controlling root growth during low P [36,37]. In rice, a mutation in leaf tip necrosis1 (ltn1) results in longer crown roots and increased P uptake and accumulation [38]. Several QTLs in wheat have been identified that have major effects on seminal and lateral root growth, which are also associated with yield and N and P acquisition [39]. Characterization of RSA in two Brachypodium accessions under different N and P conditions identified key genetic and environmental-specific growth responses in response to low nutrients [40]. Collectively, these studies Current Opinion in Biotechnology 2015, 32:93–98
96 Plant biotechnology
indicate that specific root growth is crucial to efficient nutrient uptake. Arabidopsis has been a powerful tool to dissect the molecular mechanisms controlling root growth response to limiting nutrients. Two recent studies analyzed various combinations of nutrient deficiencies to show that RSA response is dependent on which combination of nutrients is deficient [41,42]. Plasticity in RSA was observed and responsive genes could be grouped into clusters, suggesting the presence of multiple nutrient-dependent developmental programs [43]. Although not directly applicable, these results resemble what is observed in many crop species. Therefore, it is hypothesized that RSA responses are conserved at the genetic level. Evidently studies in Arabidopsis may identify important orthologous genes in crop species. These studies show that RSA response to nutrient conditions is largely controlled by genetic components and that there may be an optimal RSA for each nutrient deficiency. RSA exhibits a high level of plasticity as a result of the environmental heterogeneity. Therefore, identifying the molecular mechanisms that control root growth response will be valuable to future food production.
Soil properties influence RSA Soil properties such as density and particle size vary greatly within a field and across a growing season, and greatly impact RSA and yield [44]. Recent studies using wheat and tomato show that higher soil compaction produces roots that are short with a large diameter resulting in an RSA that is very shallow and narrow effectively decreasing the extent of soil exploration [45,46]. In addition, root elongation is more influenced by mechanical and physical properties rather than chemical properties of soil [47–50]. It has been hypothesized that the shape of root tips and presence of root hairs aids in penetration and anchoring of roots within the soil. The ground slope also impacts RSA. For example, black locust trees grown in pots at a 458 slope developed shallow, welldeveloped roots, at the expense of depth [51]. Full understanding of how the physical properties of soil impact RSA will allow for the development of crops that can thrive in different soil types. High salinity is a major stress for crops worldwide. As a result, plants have devised mechanisms to avoid soil regions of high salinity and to alter RSA in response [3]. A recent study used Arabidopsis, tomato and sorghum to elucidate the molecular mechanism behind salt avoidance [52]. Although these experiments were performed on flat plates, one can extrapolate the results to field grown plants, which could have a great impact on soil exploration and subsequent yield. Comprehensive understanding of how RSA is influenced by high salinity will allow for selection of plants that have enhanced salt avoidance. About 20% of the world’s cropland is impacted Current Opinion in Biotechnology 2015, 32:93–98
by high salinity. Therefore, identifying an RSA that is better suited for growth under this condition could have a huge impact on food production worldwide.
Conclusions Over the past decade, many QTLs, genes and molecular pathways that control RSA have been discovered that have agronomical impact. However, very few have been successfully used to advance crop production. We have discussed a small subset of the recent discoveries that impact RSA with the belief that manipulating RSA will aid in developing crops with improved performance in many parts of the world. Different types of RSA provide growth advantages under different environmental conditions yet RSA has been largely under utilized in the breeding of many crops. There is a wealth of information regarding stress response genes and their impact on shoot development. However, the RSA response is largely unexplored and could be of great significance to yield. Therefore, RSA is a promising field that can be incorporated into existing breeding programs and has great potential to influence future food production.
Acknowledgements We thank members of the Benfey laboratory and the reviewers for helpful comments on this manuscript. Work in the Benfey lab is funded by grant GBMF3405 from the Howard Hughes Medical Institute and the Gordon and Betty Moore Foundation (to P.N.B.), and grant NSF-IOS-14-11750 from the National Science Foundation.
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