Planta (BEE.) 91,285--290 (1970)
Effect of Oxygen Concentration on Leaf Photosynthesis and Resistances to Carbon Dioxide Diffusion M. M. LUDLOW Botany Department, University of Queensland, Australia Received January 17, 1970
Summary. Net photosynthesis of tropical legume leaves increased by 44 % and that of tropical grass leaves was unaffected when oxygen concentration was reduced from 21 to 0.2%. Stomatal resistance to carbon dioxide diffusion was unaltered in both cases but mesophyll resistance of legume leaves decreased with oxygen concentration. It is proposed that the decrease in mesophyll resistance is accompanied by decreases in excitation and carboxylation resistances. Introduction Leaf net photosynthetic rate of most dicotyledons measured at normal C02 concentration (300 ~l/1) and in bright light is increased by 30--50% when O 2 concentration is reduced from 21% to less than 1%, whereas net photosynthesis of tropical grasses and some dicotyledons is unaffected (BjSrkman, 1966, 1968; Forrester etal., 1966a, b; Hesketh, 1967; Downes and ttesketh, 1968; Downton and Tregunna, 1968; Poskuta, 1968 ; Hofstra and Hesketh, 1969 ; Gauhl and BjSrkman, 1969). The stimulation of net photosynthesis has been attributed to an inhibition of photorespiration and is used as a measure of it (Ludlow and Jarvis, 1970). However, the possibility t h a t the stimulation results from removal of an inhibition of photosynthesis b y molecular oxygen cannot be discounted. D a t a of Gauhl and BjSrkman (1969) indicate t h a t the sum of boundary layer and stomatal resistances to CO 2 diffusion of two species of Atriplex, one with and one without the Cd-dicarboxylic acid p a t h w a y and photorespiration (as measured b y the effect of O 2 on net photosynthesis), is unaffected b y 02 concentration. Therefore 02 appears to act within the mesophyll cells. I n this paper, data for tropical grasses and legumes are presented which support Gauhl and BjSrkman's findings and which demonstrate t h a t mesophyll resistance is affected b y O 3 concentration. Particular emphasis is given to the definition and method of calculating mesophyll resistance, and the influence of 02 concentration on it and its components. Tropical grasses have the Cd-dicarboxylic acid p a t h w a y and apparently lack photorespiration (as measured b y the CO S efflux into 20
Planta (Berl.), Bd. 91
286
M.M. Ludlow:
CO2-free air, a n d t h e e f f e c t of 0 2 on n e t p h o t o s y n t h e s i s ) a n d t r o p i c a l l e g u m e s h a v e t h e Calvfil p a t h w a y a n d p h o t o r e s p i r a t i o n (Wilson a n d L u d l o w , 1970). Materials and Methods Measurements were made on the youngest fully-expanded leaves of four grasses (Brachiaria ruzizensis Germain and Evrard cv. Kennedy; P a n i c u m m a x i m u m Jacq. ev. Hamfl; P e n n i s e t u m p u r p u r e u m Schum. Q5088; S o r g h u m a l m u m Parodi cv. Crooble) and four legumes [Calopogonium mucunoides Desv. ; Glycine ]avanica L. ev. Cooper; Phaseolus atro2urpureus D. C. cv. Siratro; Vigna luteola (Jacq.) Benth.
cv. Dalrymple] grown in a controlled environment cabinet (14 hr. light of 182 to 193 Wm -2, 30 ~: 1~C constant temperature, and 70 ~ 10 % relative humidity). The plants had an adequate supply of water and mineral nutrients. Net photosynthesis and transpiration of attached leaves were measured in an open system (]3jSrkman and Holmgren, 1963) containing an infra-red gas analyser and a differential psychrometer. Air of 21% and 0.2% 02 was obtained by mixing either CO~-free air or nitrogen (containing 0.2% 02) with CO 2. The leaf chamber contained a variable-speed fan, and the flow rate through the chamber was controlled so that the ambient CO2 concentration was 3 0 0 ~ 1 tzl/1. Leaf and air temperatures were measured with thermocouples, and the light source was a quartz-iodide lamp with filters (Sehott KG1 and 8 cm of water). Net photosynthetic rate (P/c) and transpiration rate were calculated from the changes CO2 and H20 concentration of the air as it passed over the leaf. Stomatal (rs) and boundary layer (ra) resistance to CO2 diffusion were determined as described by Holmgren (1968). Mesophyll resistance (rl~) was calculated from the equation given by Lake (1967): Ca--/~ ri p/c (r~ + r~) (1) where C a is the ambient CO 2 concentration and F is the CO 2 compensation concentration, rM is the sum of physical and chemical resistances to CO 2 transfer between the mesophyll cell wall and the site of earboxylation where the CO2 concentration is zero: rM=rm+re+r x (2) where r m is physical resistance to CO 2 diffusion, r e is excitation resistance, and r x is carboxylation resistance (Monteith, 1963). In Eq. (1), F is an allowance for intercellular respiratory CO 2 flux and does not represent the CO 2 concentration at the photosynthetic site. This equation neglects intracellular respiratory COz flux, the magnitude of the error depends upon the concentration gradient and the diffusive resistances within the cell. In addition, the assumption is made that the total respiratory C02 flux and rM are independent of P/c (Lake, 1967). Before the effect of 02 concentration on rM can be analysed, the effect of 02 on the components of Eq. (1) and the assumptions on which it is based must be assessed. The influence of 02 concentration on P/c and rs can be measured, and ra and C a are controlled. F is zero for grass leaves and is unaffected by 02 concentration, whereas the values for legume leaves are 40 and 0 ~l/1 CO2 for 21% and 0.2 % 02, respectively (Ludlow and Wilson, unpublished), l~eglecting intracellular respiratory flux overestimates rM in 21% 02 and if removal of 02 inhibits photorespiration the error in 0.2 % is probably negligible. I t seems reasonable to assume that the physical resistance between the respiratory and photosynthetic sites is
Oxygen Concentration and Diffusion Resistances
287
unaffected by 02 concentration (see Discussion). The effect of 02 concentration on the relationship between Ply, rM and total respiratory flux is uncertain and neglect of it may result in an error in the analysis which follows. Results and Discussion
I n accordance with published data for other species, net photosynthesis of tropical legumes increased b y 44 % and t h a t of tropical grasses was unaltered when 02 concentration was reduced from 21% to 0.2 % (table). StomatM resistance of both groups of plants was unaffected by O~ concentration, as data of Gauhl and Bj6rkman (1969) suggest. Therefore the stimulation of net photosynthesis of legumes results from decreases in both r i and F. If the effect of Ou concentration o n / " was neglected, rl~ was underestimated b y 27 %. When allowance was made for the change in F from 40 to 0 ~l/1 C02, rM was reduced b y 30% at low 02 concentrations [Eq. (1)]. D a t a of Bj5rkman and Gauhl (1969) for M a r c h a n t i a p o l y m o r p h a which lacks stomata also indicate t h a t 02 concentration affects r M. Mesophyll resistance of tropical grasses was not influenced b y 02 concentration (table). I t seems reasonable to assume t h a t the physical resistance, ~ , is unaffected b y 02 concentration, therefore r e and rx must either have remained constant or undergone compensatory changes. r e is defined b y Monteith (1963) :
Ce
re = O -
(3)
where Ce is the CO~ concentration at the chloroplast surface, s is the photochemical efficiency and I is illuminancc. I n tropical grasses, e is unaffected b y 02 concentration (Bull, 1969). C~ is determined by the respiratory flux (RL), net photosynthetic flux and physical resistances within the cell. Cc = Ci
rm Pjy -E- R L
(4)
where C~ is the CO 2 concentration at the mesophyll cell wall :
p~
(5)
R L was calculated from the CO 2 efflux into CO~-free air, corrected for intercellular reassimflation (Lake, 1967). Because the magnitude of the intracellular respiratory flux was unknown it was neglected. None of the components in Eqs. (4) and (5) appear to be affected b y O 2 concentration in tropical grasses, indicating t h a t Co, r e and hence rx remain constant and are not subject to compensatory changes. The relationship between r~, r~ and r~n for both grasses and legumes are shown in Fig. 1. r~ was calculated from Eqs. (3), (4) and (5), using 20*
288
M.M. Ludlow:
Table. E//ect o/oxygen concentration on net photosynthetic rate ( PN ), stomatal (rs) and mesophyll (rM) resistance to carbon dioxide di//usion o/ tropical grass and legume leaves. Values are means o] two and three replicates/or grasses and legumes, respectively. ra = boundary layer resistance to carbon dioxide di/]usion. 380 W m -z (0.4---0.7 nm), 300 i I ~I/l C02, 12 • 2 mm Hg lea/-air vapour pressure di]]erence Species
Oxygen concentration
(%)
Grasses: B. ruzizensls t 9. maximum P. purpursum S. almum Mean Legumes: C. mucunoides G. ]avanica P. atropurpureus F. luteola Mean
a Enhancement :
192r ra rs (rag C02 dm -2 hr -1) (see cm-1)
rM
Enhance lnen~ a
(%)
21 0.2 21 0.2 21 0.2 21 0.2
42.2 40.5 53.3 52.7 67.7 67.0 40.0 38.6
0.98 0.98 0.86 0.86 0.87 0.87 0.86 0.86
3.20 3.03 1.92 1.87 1.51 1.53 3.28 3.45
0.56 0.90 0.97 1.08 0.60 0.58 0.80 1.18
21 0.2
50.6 49.7
0.89 0.89
2.48 2.47
0.74 0.93
21 0.2 21 0.2 21 0.2 21 0.2
29.1 42.5 24.0 32.7 39.7 59.4 39.4 56.2
0.73 0.68 1.08 0.87 0.68 0.68 0.69 0.68
1.62 1.39 1.68 2.08 1.08 1.14 1.15 1.11
3.68 2.86 4.46 3.16 2.63 1.58 2.49 1.69
43
21 0.2
33.0 47.7
0.78 0.72
1.43 1.42
3.31 2.32
44
( P2r
-- 3.9 -- 1.2 0 -- 3.5 -- 0.9
46 36 50
100 P~r 21
a r b i t r a r y v a l u e s for r~ (assuming it to be u n a f f e c t e d b y 0 2 concentration), d a t a f r o m t h e table, a n d u n p u b l i s h e d d a t a on R L an d e. rx was c a l c u l a t e d b y difference f r o m re, rx a n d r M [Eq. (2)]. I t also seems reasonable to assume t h a t r m of tropical legumes is i n d e p e n d e n t of 02 c o n c e n t r a t i o n . E v e n if this was n o t t h e ease, a t low 02 c o n c e n t r a t i o n p r o t o p l a s m i c s t r e a m i n g (Meyer et al., 1960) a n d a c t i v e t r a n s p o r t across m e m b r a n e s (Collander, 1959) are i n h i b i t e d r a t h e r t h a n s t i m u l a t e d , w h ic h w o u l d be e x p e c t e d to lead to an increase, r a t h e r t h a n a decrease, in r~. T h e decline in rM m a y t her ef o r e result f r o m decreases in either or b o t h r e a n d r~. A t low O z c o n c e n t r a t i o n s t h e p h o t o c h e m i c a l
Oxygen Concentration and Diffusion Resistances a
"%.b \\
2
2-
\
,%. \\21 \%. \ %.\ \ %'%
u ~,
\ \ %. 0"2
3
11,0.2
~
XNN
I
"%.,, 0
289
1
21
~ N ,
0
%.',%.
\\ \
"%. \
NX
~---~----.~,.
1
2. 3 rm[sec cm -1) Fig. l a and b. Relationship between excitation (re, solid line) and earboxylation (rx, broken line) resistances, and physical mesophyll resistance (rm) of tropical (a) grasses and (b) legumes at 21% and 0.2% 0~. Excitation and carboxylation resistances were caleulaf~d from arbitrary values of r m . Other environmental conditions are given in the Table efficiency of m o s t dicotyledons increases (BjSrkman, 1966; B j 6 r k m a n and Gauhl, 1969; Bull, 1969) and C e decreases, p a r t l y because photorespiration is inhibited. F r o m Eq. (3) it can be seen t h a t r e decreases with Oe concentration, as does rx at all values of r m (Fig. 1). I f the assumptions on which this analysis is based are correct it would appear t h a t the decrease in r M of tropical legume leaves at 02 concentrations is accompanied b y decreases in b o t h r e and r x , and t h a t the sensitivity of r e and r z of tropicalgrasses and legumes to 03 concentration are different. This m a y indicate t h a t the Calvin and C4-dicarboxylic acid p a t h w a y s have different sensitivities to 0~. However, if the assumptions are incorrect, or if oxygen does not p r o m o t e photorespiration b u t directly inhibits photosynthesis (Ozbun et a l . , 1965 ; Bj6rkman, 1966) these conclusions m a y have to be modified. References BjSrkman, 0.: The effect of oxygen concentration on photosynthesis in higher plants. Physiol. Plantarum (Cph.) 19, 618--633 (1966). - - Further studies of the effect of oxygen concentration on photosynthetic COs uptake in higher plants. Carnegie Inst. Wash. Year Book 66, 220--228 (1968). - - Gauhl, E. ; Effect of temperaVure and oxygen concentration on photosynthesis in M a r c h a n t i a p o l y m o r p h a . Carnegie Inst. Wash. Year Book 67, 479--482 (1969). - - Holmgren, P. : Adaptability of the photosynthetic apparatus to light intensity in ecotypes from exposed and shaded habitats. Physiol. Plantarum (Cph.) 16, 889--914 (1963).
290
NI. M. Ludlow: Oxygen Concentration and Diffusion Resistances
]3ull, T. A. : Photosynthetic efficiencies and photorespiration in Calvin cycle and Ct-dicarboxylic acid plants. Crop Sei. 9, 126--129 (1969). Collander, R. : Cell membranes, their resistance to penetration and their capacity for transport (F. C. Steward, ed.), p. 3--102. New York-London: Academic Press 1959. Downes, R. W., Hesketh, J.: Enhanced photosynthesis at low oxygen concentrations: differential response of temperature and tropical grasses. Planta (BEE.) 78, 79--84 (1968). Downton, W. J. S., Tregunna, E. ]3. : Photorespiration and glycollate metabolism: a re-examin~tion and correlation of some previous studies. P1. Physiol. (Lancaster) 48, 923--929 (1968). Forrester, M. L., Krotkov, G., Nelson, C. D. : Effect of oxygen on photosynthesis, photorespiration and respiration in detached leaves. I. Soybean. P1. Physiol. (Lancaster) 41, 422--427 (1966a). - - - - - - Effect of oxygen on photosynthesis, photorespiration and respiration in detached leaves. II. Corn and other monocotyledons. P1. Physiol. (Lancaster) 41, 428--431 (1966b). Gauhl, E., Bj6rkman, 0.: Simultaneous measurements on the effect of oxygen concentration on water vapour and carbon dioxide exchange in leaves. Planta (]3erl.) 88, 187--191 (1969). ttesketh, J. D. : Enhancement of photosynthetic C02-assimilation in the absence of oxygen, as affected by species and temperature. Planta (Berl.) 76, 371--374 (1967). Hofstra, G., ttesketh, J. D. : Effects of temperature on the gas exchange of leaves in the light and dark. Planta (Berl.) 85, 228--237 (1969). Holmgren, P. : Leaf factors affecting light-saturated photosynthesis in ecotypes of Sotidago virgaurea irom exposed and shaded habitats. Physiol. Plantarum (Cph.) 21, 676--698 (1968). Lake, J. V. : Respiration of leaves during photosynthesis. II. Effects on the estimation of mesophyll resistance. Aust. J. biol. Sei. 20, 495--499 (1967). Ludlow, M.M., Jarvis, P. G.: Methods of measuring photorespiration rates of leaves. Plant photosynthetic prodnetion, a manual of methods (Z. Sestak, J. Catsky and P. G. Jarvis, eds.). The Hague: Dr. W. Junk 1970 (in press). Meyer, ]3. S., Anderson, D. B., ]35hning, R. H. : Introduction to plant physiology, p. 38. New Jersey: D. van Nostrand 1960. Monteith, J. L.: Gas exchange on plant communities. Environmental control of plant growth (L. T. Evans, ed.), p. 95--112. New York-London: Academic Press 1963. Ozbun, J.L., Volk, 1%. J., Jackson, W.A.: Effect of potassium deficiency on photosynthesis, respiration and the utilization of photosynthetic reductant by immature bean leaves. P1. Physiol. (Lancaster) 5, 69--75 (1965). Poskuta, J. : Photosynthesis, photorespiration and respiration of detached spruce twigs as influenced by oxygen concentration and light intensity. Physiol. Plantarnm (Cph.) 21, 1129--1136 (1968). Wilson, G. L., Ludlow, M. M. : Leaf photosynthetic rates of tropical grasses and legumes. XIth Int. Grassld. Congr. Surfers Paradise, Australia. In press (1970). Dr. IV[.M. Ludlow Division of Tropical Pastures CSII~O Mill Road St. Lucia Q'ld, 4067, Australia
Effect of Oxygen Concentration on Leaf Photosynthesis and Resistances to Carbon Dioxide Diffusion M. M. LUDLOW Botany Department, University of Queensland, Australia Received January 17, 1970
Summary. Net photosynthesis of tropical legume leaves increased by 44 % and that of tropical grass leaves was unaffected when oxygen concentration was reduced from 21 to 0.2%. Stomatal resistance to carbon dioxide diffusion was unaltered in both cases but mesophyll resistance of legume leaves decreased with oxygen concentration. It is proposed that the decrease in mesophyll resistance is accompanied by decreases in excitation and carboxylation resistances. Introduction Leaf net photosynthetic rate of most dicotyledons measured at normal C02 concentration (300 ~l/1) and in bright light is increased by 30--50% when O 2 concentration is reduced from 21% to less than 1%, whereas net photosynthesis of tropical grasses and some dicotyledons is unaffected (BjSrkman, 1966, 1968; Forrester etal., 1966a, b; Hesketh, 1967; Downes and ttesketh, 1968; Downton and Tregunna, 1968; Poskuta, 1968 ; Hofstra and Hesketh, 1969 ; Gauhl and BjSrkman, 1969). The stimulation of net photosynthesis has been attributed to an inhibition of photorespiration and is used as a measure of it (Ludlow and Jarvis, 1970). However, the possibility t h a t the stimulation results from removal of an inhibition of photosynthesis b y molecular oxygen cannot be discounted. D a t a of Gauhl and BjSrkman (1969) indicate t h a t the sum of boundary layer and stomatal resistances to CO 2 diffusion of two species of Atriplex, one with and one without the Cd-dicarboxylic acid p a t h w a y and photorespiration (as measured b y the effect of O 2 on net photosynthesis), is unaffected b y 02 concentration. Therefore 02 appears to act within the mesophyll cells. I n this paper, data for tropical grasses and legumes are presented which support Gauhl and BjSrkman's findings and which demonstrate t h a t mesophyll resistance is affected b y O 3 concentration. Particular emphasis is given to the definition and method of calculating mesophyll resistance, and the influence of 02 concentration on it and its components. Tropical grasses have the Cd-dicarboxylic acid p a t h w a y and apparently lack photorespiration (as measured b y the CO S efflux into 20
Planta (Berl.), Bd. 91
286
M.M. Ludlow:
CO2-free air, a n d t h e e f f e c t of 0 2 on n e t p h o t o s y n t h e s i s ) a n d t r o p i c a l l e g u m e s h a v e t h e Calvfil p a t h w a y a n d p h o t o r e s p i r a t i o n (Wilson a n d L u d l o w , 1970). Materials and Methods Measurements were made on the youngest fully-expanded leaves of four grasses (Brachiaria ruzizensis Germain and Evrard cv. Kennedy; P a n i c u m m a x i m u m Jacq. ev. Hamfl; P e n n i s e t u m p u r p u r e u m Schum. Q5088; S o r g h u m a l m u m Parodi cv. Crooble) and four legumes [Calopogonium mucunoides Desv. ; Glycine ]avanica L. ev. Cooper; Phaseolus atro2urpureus D. C. cv. Siratro; Vigna luteola (Jacq.) Benth.
cv. Dalrymple] grown in a controlled environment cabinet (14 hr. light of 182 to 193 Wm -2, 30 ~: 1~C constant temperature, and 70 ~ 10 % relative humidity). The plants had an adequate supply of water and mineral nutrients. Net photosynthesis and transpiration of attached leaves were measured in an open system (]3jSrkman and Holmgren, 1963) containing an infra-red gas analyser and a differential psychrometer. Air of 21% and 0.2% 02 was obtained by mixing either CO~-free air or nitrogen (containing 0.2% 02) with CO 2. The leaf chamber contained a variable-speed fan, and the flow rate through the chamber was controlled so that the ambient CO2 concentration was 3 0 0 ~ 1 tzl/1. Leaf and air temperatures were measured with thermocouples, and the light source was a quartz-iodide lamp with filters (Sehott KG1 and 8 cm of water). Net photosynthetic rate (P/c) and transpiration rate were calculated from the changes CO2 and H20 concentration of the air as it passed over the leaf. Stomatal (rs) and boundary layer (ra) resistance to CO2 diffusion were determined as described by Holmgren (1968). Mesophyll resistance (rl~) was calculated from the equation given by Lake (1967): Ca--/~ ri p/c (r~ + r~) (1) where C a is the ambient CO 2 concentration and F is the CO 2 compensation concentration, rM is the sum of physical and chemical resistances to CO 2 transfer between the mesophyll cell wall and the site of earboxylation where the CO2 concentration is zero: rM=rm+re+r x (2) where r m is physical resistance to CO 2 diffusion, r e is excitation resistance, and r x is carboxylation resistance (Monteith, 1963). In Eq. (1), F is an allowance for intercellular respiratory CO 2 flux and does not represent the CO 2 concentration at the photosynthetic site. This equation neglects intracellular respiratory COz flux, the magnitude of the error depends upon the concentration gradient and the diffusive resistances within the cell. In addition, the assumption is made that the total respiratory C02 flux and rM are independent of P/c (Lake, 1967). Before the effect of 02 concentration on rM can be analysed, the effect of 02 on the components of Eq. (1) and the assumptions on which it is based must be assessed. The influence of 02 concentration on P/c and rs can be measured, and ra and C a are controlled. F is zero for grass leaves and is unaffected by 02 concentration, whereas the values for legume leaves are 40 and 0 ~l/1 CO2 for 21% and 0.2 % 02, respectively (Ludlow and Wilson, unpublished), l~eglecting intracellular respiratory flux overestimates rM in 21% 02 and if removal of 02 inhibits photorespiration the error in 0.2 % is probably negligible. I t seems reasonable to assume that the physical resistance between the respiratory and photosynthetic sites is
Oxygen Concentration and Diffusion Resistances
287
unaffected by 02 concentration (see Discussion). The effect of 02 concentration on the relationship between Ply, rM and total respiratory flux is uncertain and neglect of it may result in an error in the analysis which follows. Results and Discussion
I n accordance with published data for other species, net photosynthesis of tropical legumes increased b y 44 % and t h a t of tropical grasses was unaltered when 02 concentration was reduced from 21% to 0.2 % (table). StomatM resistance of both groups of plants was unaffected by O~ concentration, as data of Gauhl and Bj6rkman (1969) suggest. Therefore the stimulation of net photosynthesis of legumes results from decreases in both r i and F. If the effect of Ou concentration o n / " was neglected, rl~ was underestimated b y 27 %. When allowance was made for the change in F from 40 to 0 ~l/1 C02, rM was reduced b y 30% at low 02 concentrations [Eq. (1)]. D a t a of Bj5rkman and Gauhl (1969) for M a r c h a n t i a p o l y m o r p h a which lacks stomata also indicate t h a t 02 concentration affects r M. Mesophyll resistance of tropical grasses was not influenced b y 02 concentration (table). I t seems reasonable to assume t h a t the physical resistance, ~ , is unaffected b y 02 concentration, therefore r e and rx must either have remained constant or undergone compensatory changes. r e is defined b y Monteith (1963) :
Ce
re = O -
(3)
where Ce is the CO~ concentration at the chloroplast surface, s is the photochemical efficiency and I is illuminancc. I n tropical grasses, e is unaffected b y 02 concentration (Bull, 1969). C~ is determined by the respiratory flux (RL), net photosynthetic flux and physical resistances within the cell. Cc = Ci
rm Pjy -E- R L
(4)
where C~ is the CO 2 concentration at the mesophyll cell wall :
p~
(5)
R L was calculated from the CO 2 efflux into CO~-free air, corrected for intercellular reassimflation (Lake, 1967). Because the magnitude of the intracellular respiratory flux was unknown it was neglected. None of the components in Eqs. (4) and (5) appear to be affected b y O 2 concentration in tropical grasses, indicating t h a t Co, r e and hence rx remain constant and are not subject to compensatory changes. The relationship between r~, r~ and r~n for both grasses and legumes are shown in Fig. 1. r~ was calculated from Eqs. (3), (4) and (5), using 20*
288
M.M. Ludlow:
Table. E//ect o/oxygen concentration on net photosynthetic rate ( PN ), stomatal (rs) and mesophyll (rM) resistance to carbon dioxide di//usion o/ tropical grass and legume leaves. Values are means o] two and three replicates/or grasses and legumes, respectively. ra = boundary layer resistance to carbon dioxide di/]usion. 380 W m -z (0.4---0.7 nm), 300 i I ~I/l C02, 12 • 2 mm Hg lea/-air vapour pressure di]]erence Species
Oxygen concentration
(%)
Grasses: B. ruzizensls t 9. maximum P. purpursum S. almum Mean Legumes: C. mucunoides G. ]avanica P. atropurpureus F. luteola Mean
a Enhancement :
192r ra rs (rag C02 dm -2 hr -1) (see cm-1)
rM
Enhance lnen~ a
(%)
21 0.2 21 0.2 21 0.2 21 0.2
42.2 40.5 53.3 52.7 67.7 67.0 40.0 38.6
0.98 0.98 0.86 0.86 0.87 0.87 0.86 0.86
3.20 3.03 1.92 1.87 1.51 1.53 3.28 3.45
0.56 0.90 0.97 1.08 0.60 0.58 0.80 1.18
21 0.2
50.6 49.7
0.89 0.89
2.48 2.47
0.74 0.93
21 0.2 21 0.2 21 0.2 21 0.2
29.1 42.5 24.0 32.7 39.7 59.4 39.4 56.2
0.73 0.68 1.08 0.87 0.68 0.68 0.69 0.68
1.62 1.39 1.68 2.08 1.08 1.14 1.15 1.11
3.68 2.86 4.46 3.16 2.63 1.58 2.49 1.69
43
21 0.2
33.0 47.7
0.78 0.72
1.43 1.42
3.31 2.32
44
( P2r
-- 3.9 -- 1.2 0 -- 3.5 -- 0.9
46 36 50
100 P~r 21
a r b i t r a r y v a l u e s for r~ (assuming it to be u n a f f e c t e d b y 0 2 concentration), d a t a f r o m t h e table, a n d u n p u b l i s h e d d a t a on R L an d e. rx was c a l c u l a t e d b y difference f r o m re, rx a n d r M [Eq. (2)]. I t also seems reasonable to assume t h a t r m of tropical legumes is i n d e p e n d e n t of 02 c o n c e n t r a t i o n . E v e n if this was n o t t h e ease, a t low 02 c o n c e n t r a t i o n p r o t o p l a s m i c s t r e a m i n g (Meyer et al., 1960) a n d a c t i v e t r a n s p o r t across m e m b r a n e s (Collander, 1959) are i n h i b i t e d r a t h e r t h a n s t i m u l a t e d , w h ic h w o u l d be e x p e c t e d to lead to an increase, r a t h e r t h a n a decrease, in r~. T h e decline in rM m a y t her ef o r e result f r o m decreases in either or b o t h r e a n d r~. A t low O z c o n c e n t r a t i o n s t h e p h o t o c h e m i c a l
Oxygen Concentration and Diffusion Resistances a
"%.b \\
2
2-
\
,%. \\21 \%. \ %.\ \ %'%
u ~,
\ \ %. 0"2
3
11,0.2
~
XNN
I
"%.,, 0
289
1
21
~ N ,
0
%.',%.
\\ \
"%. \
NX
~---~----.~,.
1
2. 3 rm[sec cm -1) Fig. l a and b. Relationship between excitation (re, solid line) and earboxylation (rx, broken line) resistances, and physical mesophyll resistance (rm) of tropical (a) grasses and (b) legumes at 21% and 0.2% 0~. Excitation and carboxylation resistances were caleulaf~d from arbitrary values of r m . Other environmental conditions are given in the Table efficiency of m o s t dicotyledons increases (BjSrkman, 1966; B j 6 r k m a n and Gauhl, 1969; Bull, 1969) and C e decreases, p a r t l y because photorespiration is inhibited. F r o m Eq. (3) it can be seen t h a t r e decreases with Oe concentration, as does rx at all values of r m (Fig. 1). I f the assumptions on which this analysis is based are correct it would appear t h a t the decrease in r M of tropical legume leaves at 02 concentrations is accompanied b y decreases in b o t h r e and r x , and t h a t the sensitivity of r e and r z of tropicalgrasses and legumes to 03 concentration are different. This m a y indicate t h a t the Calvin and C4-dicarboxylic acid p a t h w a y s have different sensitivities to 0~. However, if the assumptions are incorrect, or if oxygen does not p r o m o t e photorespiration b u t directly inhibits photosynthesis (Ozbun et a l . , 1965 ; Bj6rkman, 1966) these conclusions m a y have to be modified. References BjSrkman, 0.: The effect of oxygen concentration on photosynthesis in higher plants. Physiol. Plantarum (Cph.) 19, 618--633 (1966). - - Further studies of the effect of oxygen concentration on photosynthetic COs uptake in higher plants. Carnegie Inst. Wash. Year Book 66, 220--228 (1968). - - Gauhl, E. ; Effect of temperaVure and oxygen concentration on photosynthesis in M a r c h a n t i a p o l y m o r p h a . Carnegie Inst. Wash. Year Book 67, 479--482 (1969). - - Holmgren, P. : Adaptability of the photosynthetic apparatus to light intensity in ecotypes from exposed and shaded habitats. Physiol. Plantarum (Cph.) 16, 889--914 (1963).
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]3ull, T. A. : Photosynthetic efficiencies and photorespiration in Calvin cycle and Ct-dicarboxylic acid plants. Crop Sei. 9, 126--129 (1969). Collander, R. : Cell membranes, their resistance to penetration and their capacity for transport (F. C. Steward, ed.), p. 3--102. New York-London: Academic Press 1959. Downes, R. W., Hesketh, J.: Enhanced photosynthesis at low oxygen concentrations: differential response of temperature and tropical grasses. Planta (BEE.) 78, 79--84 (1968). Downton, W. J. S., Tregunna, E. ]3. : Photorespiration and glycollate metabolism: a re-examin~tion and correlation of some previous studies. P1. Physiol. (Lancaster) 48, 923--929 (1968). Forrester, M. L., Krotkov, G., Nelson, C. D. : Effect of oxygen on photosynthesis, photorespiration and respiration in detached leaves. I. Soybean. P1. Physiol. (Lancaster) 41, 422--427 (1966a). - - - - - - Effect of oxygen on photosynthesis, photorespiration and respiration in detached leaves. II. Corn and other monocotyledons. P1. Physiol. (Lancaster) 41, 428--431 (1966b). Gauhl, E., Bj6rkman, 0.: Simultaneous measurements on the effect of oxygen concentration on water vapour and carbon dioxide exchange in leaves. Planta (]3erl.) 88, 187--191 (1969). ttesketh, J. D. : Enhancement of photosynthetic C02-assimilation in the absence of oxygen, as affected by species and temperature. Planta (Berl.) 76, 371--374 (1967). Hofstra, G., ttesketh, J. D. : Effects of temperature on the gas exchange of leaves in the light and dark. Planta (Berl.) 85, 228--237 (1969). Holmgren, P. : Leaf factors affecting light-saturated photosynthesis in ecotypes of Sotidago virgaurea irom exposed and shaded habitats. Physiol. Plantarum (Cph.) 21, 676--698 (1968). Lake, J. V. : Respiration of leaves during photosynthesis. II. Effects on the estimation of mesophyll resistance. Aust. J. biol. Sei. 20, 495--499 (1967). Ludlow, M.M., Jarvis, P. G.: Methods of measuring photorespiration rates of leaves. Plant photosynthetic prodnetion, a manual of methods (Z. Sestak, J. Catsky and P. G. Jarvis, eds.). The Hague: Dr. W. Junk 1970 (in press). Meyer, ]3. S., Anderson, D. B., ]35hning, R. H. : Introduction to plant physiology, p. 38. New Jersey: D. van Nostrand 1960. Monteith, J. L.: Gas exchange on plant communities. Environmental control of plant growth (L. T. Evans, ed.), p. 95--112. New York-London: Academic Press 1963. Ozbun, J.L., Volk, 1%. J., Jackson, W.A.: Effect of potassium deficiency on photosynthesis, respiration and the utilization of photosynthetic reductant by immature bean leaves. P1. Physiol. (Lancaster) 5, 69--75 (1965). Poskuta, J. : Photosynthesis, photorespiration and respiration of detached spruce twigs as influenced by oxygen concentration and light intensity. Physiol. Plantarnm (Cph.) 21, 1129--1136 (1968). Wilson, G. L., Ludlow, M. M. : Leaf photosynthetic rates of tropical grasses and legumes. XIth Int. Grassld. Congr. Surfers Paradise, Australia. In press (1970). Dr. IV[.M. Ludlow Division of Tropical Pastures CSII~O Mill Road St. Lucia Q'ld, 4067, Australia
