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The coordination of leaf photosynthesis links C and N fluxes in C3 plant species.

Maire V, Martre P, Kattge J, Gastal F, Esser G, Fontaine S, Soussana JF - PLoS ONE (2012)

Bottom Line: The resulting model linking leaf photosynthesis, stomata conductance and nitrogen investment provides testable hypotheses about the physiological regulation of these processes.A calibration by plant functional type of k(3) and J(fac) still leads to accurate model prediction of N(a), while SLA calibration is essentially required at species level.Observed variations in k(3) and J(fac) are partly explained by environmental and phylogenetic constraints, while SLA variation is partly explained by phylogeny.

View Article: PubMed Central - PubMed

Affiliation: INRA, UR874 UREP, Clermont-Ferrand, France. vmaire24@gmail.com

ABSTRACT
Photosynthetic capacity is one of the most sensitive parameters in vegetation models and its relationship to leaf nitrogen content links the carbon and nitrogen cycles. Process understanding for reliably predicting photosynthetic capacity is still missing. To advance this understanding we have tested across C(3) plant species the coordination hypothesis, which assumes nitrogen allocation to photosynthetic processes such that photosynthesis tends to be co-limited by ribulose-1,5-bisphosphate (RuBP) carboxylation and regeneration. The coordination hypothesis yields an analytical solution to predict photosynthetic capacity and calculate area-based leaf nitrogen content (N(a)). The resulting model linking leaf photosynthesis, stomata conductance and nitrogen investment provides testable hypotheses about the physiological regulation of these processes. Based on a dataset of 293 observations for 31 species grown under a range of environmental conditions, we confirm the coordination hypothesis: under mean environmental conditions experienced by leaves during the preceding month, RuBP carboxylation equals RuBP regeneration. We identify three key parameters for photosynthetic coordination: specific leaf area and two photosynthetic traits (k(3), which modulates N investment and is the ratio of RuBP carboxylation/oxygenation capacity (V(Cmax)) to leaf photosynthetic N content (N(pa)); and J(fac), which modulates photosynthesis for a given k(3) and is the ratio of RuBP regeneration capacity (J(max)) to V(Cmax)). With species-specific parameter values of SLA, k(3) and J(fac), our leaf photosynthesis coordination model accounts for 93% of the total variance in N(a) across species and environmental conditions. A calibration by plant functional type of k(3) and J(fac) still leads to accurate model prediction of N(a), while SLA calibration is essentially required at species level. Observed variations in k(3) and J(fac) are partly explained by environmental and phylogenetic constraints, while SLA variation is partly explained by phylogeny. These results open a new avenue for predicting photosynthetic capacity and leaf nitrogen content in vegetation models.

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Tests of the coordination hypothesis using experimental values of leaf photosynthetic traits (Vcmax, Jmax, Jfac, k3 and SLA).A) Relationship between the predicted rates of RuBP carboxylation/oxygenation (Wc) and RuBP regeneration (Wj) under plant growth conditions. B) Relationship between predicted (Nac) and observed (Na) leaf N content. Na was calculated as the sum of the leaf photosynthetic and structural N contents. Leaf photosynthetic N content was predicted using Eqn 2 with the species-specific parameters k3 and Jfac. C) Relationship between predicted (Npac) and observed (Npa) photosynthetic leaf N content. D) Relationship between predicted and observed leaf C/N ratio. A common leaf structural N content was used (fns  = 0.012 gN g−1 DM). Solid lines are the regressions. Short-dashed and long-dashed lines indicate the confidence (at 95%) and prediction intervals, respectively. The insert in Fig. 1B shows the same relationship without the very high observed Na values for the PFT1. ***, P<0.001.
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pone-0038345-g001: Tests of the coordination hypothesis using experimental values of leaf photosynthetic traits (Vcmax, Jmax, Jfac, k3 and SLA).A) Relationship between the predicted rates of RuBP carboxylation/oxygenation (Wc) and RuBP regeneration (Wj) under plant growth conditions. B) Relationship between predicted (Nac) and observed (Na) leaf N content. Na was calculated as the sum of the leaf photosynthetic and structural N contents. Leaf photosynthetic N content was predicted using Eqn 2 with the species-specific parameters k3 and Jfac. C) Relationship between predicted (Npac) and observed (Npa) photosynthetic leaf N content. D) Relationship between predicted and observed leaf C/N ratio. A common leaf structural N content was used (fns  = 0.012 gN g−1 DM). Solid lines are the regressions. Short-dashed and long-dashed lines indicate the confidence (at 95%) and prediction intervals, respectively. The insert in Fig. 1B shows the same relationship without the very high observed Na values for the PFT1. ***, P<0.001.

Mentions: We assessed the level of photosynthetic co-limitation by comparing dark (Wc) to light-driven (Wj) biochemical processes under growth conditions experienced by the leaves in the month prior to observations. Wc strongly correlated with Wj (Fig. 1A, n = 293, P<0.001, intercept not significantly different from zero) across species and growth environments (characterized by Tg, PPFD, hs and Cg). An ANOVA on the regression residuals revealed a significant PFT effect (d.f. = 5, 283; P<0.001; data not shown). The calculated Wc/Wj ratio was not significantly different from one (t-test at P<0.05, n = 293). This ratio varied neither with species parameters, nor with environmental growth conditions.


The coordination of leaf photosynthesis links C and N fluxes in C3 plant species.

Maire V, Martre P, Kattge J, Gastal F, Esser G, Fontaine S, Soussana JF - PLoS ONE (2012)

Tests of the coordination hypothesis using experimental values of leaf photosynthetic traits (Vcmax, Jmax, Jfac, k3 and SLA).A) Relationship between the predicted rates of RuBP carboxylation/oxygenation (Wc) and RuBP regeneration (Wj) under plant growth conditions. B) Relationship between predicted (Nac) and observed (Na) leaf N content. Na was calculated as the sum of the leaf photosynthetic and structural N contents. Leaf photosynthetic N content was predicted using Eqn 2 with the species-specific parameters k3 and Jfac. C) Relationship between predicted (Npac) and observed (Npa) photosynthetic leaf N content. D) Relationship between predicted and observed leaf C/N ratio. A common leaf structural N content was used (fns  = 0.012 gN g−1 DM). Solid lines are the regressions. Short-dashed and long-dashed lines indicate the confidence (at 95%) and prediction intervals, respectively. The insert in Fig. 1B shows the same relationship without the very high observed Na values for the PFT1. ***, P<0.001.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3369925&req=5

pone-0038345-g001: Tests of the coordination hypothesis using experimental values of leaf photosynthetic traits (Vcmax, Jmax, Jfac, k3 and SLA).A) Relationship between the predicted rates of RuBP carboxylation/oxygenation (Wc) and RuBP regeneration (Wj) under plant growth conditions. B) Relationship between predicted (Nac) and observed (Na) leaf N content. Na was calculated as the sum of the leaf photosynthetic and structural N contents. Leaf photosynthetic N content was predicted using Eqn 2 with the species-specific parameters k3 and Jfac. C) Relationship between predicted (Npac) and observed (Npa) photosynthetic leaf N content. D) Relationship between predicted and observed leaf C/N ratio. A common leaf structural N content was used (fns  = 0.012 gN g−1 DM). Solid lines are the regressions. Short-dashed and long-dashed lines indicate the confidence (at 95%) and prediction intervals, respectively. The insert in Fig. 1B shows the same relationship without the very high observed Na values for the PFT1. ***, P<0.001.
Mentions: We assessed the level of photosynthetic co-limitation by comparing dark (Wc) to light-driven (Wj) biochemical processes under growth conditions experienced by the leaves in the month prior to observations. Wc strongly correlated with Wj (Fig. 1A, n = 293, P<0.001, intercept not significantly different from zero) across species and growth environments (characterized by Tg, PPFD, hs and Cg). An ANOVA on the regression residuals revealed a significant PFT effect (d.f. = 5, 283; P<0.001; data not shown). The calculated Wc/Wj ratio was not significantly different from one (t-test at P<0.05, n = 293). This ratio varied neither with species parameters, nor with environmental growth conditions.

Bottom Line: The resulting model linking leaf photosynthesis, stomata conductance and nitrogen investment provides testable hypotheses about the physiological regulation of these processes.A calibration by plant functional type of k(3) and J(fac) still leads to accurate model prediction of N(a), while SLA calibration is essentially required at species level.Observed variations in k(3) and J(fac) are partly explained by environmental and phylogenetic constraints, while SLA variation is partly explained by phylogeny.

View Article: PubMed Central - PubMed

Affiliation: INRA, UR874 UREP, Clermont-Ferrand, France. vmaire24@gmail.com

ABSTRACT
Photosynthetic capacity is one of the most sensitive parameters in vegetation models and its relationship to leaf nitrogen content links the carbon and nitrogen cycles. Process understanding for reliably predicting photosynthetic capacity is still missing. To advance this understanding we have tested across C(3) plant species the coordination hypothesis, which assumes nitrogen allocation to photosynthetic processes such that photosynthesis tends to be co-limited by ribulose-1,5-bisphosphate (RuBP) carboxylation and regeneration. The coordination hypothesis yields an analytical solution to predict photosynthetic capacity and calculate area-based leaf nitrogen content (N(a)). The resulting model linking leaf photosynthesis, stomata conductance and nitrogen investment provides testable hypotheses about the physiological regulation of these processes. Based on a dataset of 293 observations for 31 species grown under a range of environmental conditions, we confirm the coordination hypothesis: under mean environmental conditions experienced by leaves during the preceding month, RuBP carboxylation equals RuBP regeneration. We identify three key parameters for photosynthetic coordination: specific leaf area and two photosynthetic traits (k(3), which modulates N investment and is the ratio of RuBP carboxylation/oxygenation capacity (V(Cmax)) to leaf photosynthetic N content (N(pa)); and J(fac), which modulates photosynthesis for a given k(3) and is the ratio of RuBP regeneration capacity (J(max)) to V(Cmax)). With species-specific parameter values of SLA, k(3) and J(fac), our leaf photosynthesis coordination model accounts for 93% of the total variance in N(a) across species and environmental conditions. A calibration by plant functional type of k(3) and J(fac) still leads to accurate model prediction of N(a), while SLA calibration is essentially required at species level. Observed variations in k(3) and J(fac) are partly explained by environmental and phylogenetic constraints, while SLA variation is partly explained by phylogeny. These results open a new avenue for predicting photosynthetic capacity and leaf nitrogen content in vegetation models.

Show MeSH
Related in: MedlinePlus