Genetic variation in stomatal and biochemical limitations to photosynthesis in the annual plant, Polygonum arenastrum

Terrestrial plant photosynthesis may be limited both by stomatal behavior and leaf biochemical capacity. While inferences have been made about the importance of stomatal and biochemical limitations to photosynthesis in a variety of species in a range of environments, genetic variation in these limitations has never been documented in wild plant populations. Genetic variation provides the raw material for adaptive evolution in rates of carbon assimilation. We examined genetic variation in gas exchange physiology and in stomatal and biochemical traits in 16 genetic lines of the annual plant, Polygonum arenastrum. The photosynthesis against leaf internal CO2 (A-ci) response curve was measured on three greenhouse-grown individuals per line. We measured the photosynthetic rate (A) and stomatal conductance (g), and calculated the internal CO2 concentration (ci) at ambient CO2 levels. In addition, the following stomatal and biochemical characteristics were obtained from the A-ci curve on each individual: the degree of stomatal limitation to photosynthesis (L(s)), the maximum ribulose 1,5-biphosphate carboxylase-oxygenase (Rubisco) activity (Vc(max)) and electron transport capacity (J(max)). All physiological traits were genetically variable, with broad sense heritabilities ranging from 0.66 for L(s) to 0.94 for J(max). Strong positive genetic correlations were found between Vc(max) and J(max), between g and biochemical chemical capacity. Path analyses revealed strong causal influences of stomatal conductance and leaf biochemistry on A and ci. Path analysis also indicated that L(s) confounds both stomatal and biochemical effects, and is an appropriate measure of stomatal influences on photosynthesis, only when biochemical variation is accounted for. In total, our results indicate that differences among lines in photosynthesis and ci result from simultaneous changes in biochemical and stomatal characteristics and are consistent with theoretical predictions that there should be co-limitation of photosynthesis by ribulose-1,5-biphosphate (RuBP) utilization and regeneration, and by stomatal conductance and leaf biochemistry. Gas exchange characteristics of genetic lines in the present study were generally consistent with measurements of the same lines in a previous field study. Our new results indicate that the mechanisms underlying variation in gas exchange include variation in both stomatal conductance and biochemical capacity. In addition, A, g, and ci in the present study tended also to be positively correlated with carbon isotope discrimination (Delta), and negatively correlated with time to flowering, life span, and leaf size based on earlier work. The pattern of correlation between physiology and life span among genetic lines of P. arenastrum parallels interspecific patterns of character correlations. We suggest that the range of trait constellations among lines in P. arenastrum represents a continuum between stress avoidance (rapid development, high gas exchange metabolism) and stress tolerance (slow development, low gas exchange metabolism), and that genetic variation in these character combinations may be maintained by environmental variation in stress levels in the species' ruderal habitat.