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

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.

SUBMITTER: Maire V

PROVIDER: S-EPMC3369925 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Light intensity (I) is the most dynamic and significant environmental variable affecting photosynthesis (A n), stomatal conductance (g s), transpiration (T r), and water-use efficiency (WUE). Currently, studies characterizing leaf-scale WUE-I responses are rare and key questions have not been answered. In particular, (1) What shape does the response function take? (2) Are there maximum intrinsic (WUEi; WUEi-max) and instantaneous WUE (WUEinst; WUEinst-max) at the corresponding saturation irradiances (I i-sat and I inst-sat)? This study developed WUEi-I and WUEinst-I models sharing the same non-asymptotic function with previously published A n-I and g s-I models. Observation-modeling intercomparison was conducted for field-grown plants of soybean (C3) and grain amaranth (C4) to assess the robustness of our models versus the non-rectangular hyperbola models (NH models). Both types of models can reproduce WUE-I curves well over light-limited range. However, at light-saturated range, NH models overestimated WUEi-max and WUEinst-max and cannot return I i-sat and I inst-sat due to its asymptotic function. Moreover, NH models cannot describe the down-regulation of WUE induced by high light, on which our models described well. The results showed that WUEi and WUEinst increased rapidly within low range of I, driven by uncoupled photosynthesis and stomatal responsiveness. Initial response rapidity of WUEi was higher than WUEinst because the greatest increase of A n and T r occurred at low g s. C4 species showed higher WUEi-max and WUEinst-max than C3 species-at similar I i-sat and I inst-sat. Our intercomparison highlighted larger discrepancy between WUEi-I and WUEinst-I responses in C3 than C4 species, quantitatively characterizing an important advantage of C4 photosynthetic pathway-higher A n gain but lower T r cost per unit of g s change. Our models can accurately return the wealth of key quantities defining species-specific WUE-I responses-besides A n-I and g s-I responses. The key advantage is its robustness in characterizing these entangled responses over a wide I range from light-limited to light-inhibitory light intensities, through adopting the same analytical framework and the explicit and consistent definitions on these responses. Our models are of significance for physiologists and modelers-and also for breeders screening for genotypes concurrently achieving maximized photosynthesis and optimized WUE.

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

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