Natural variation in Arabidopsis shoot branching plasticity in response to nitrate supply affects fitness

Author summary Many organisms adjust their development depending on environmental conditions. This is particularly striking in plants, with development constantly tuned throughout their lives. A good example is the modulation of shoot branching in response to external environmental cues. We characterised hundreds of genetically distinct Arabidopsis thaliana lines for their branching response to the availability of a key nutrient, nitrogen. We found that some lines adjusted their degree of branching according to the level of nitrogen available, whereas others did not. These latter low plasticity genotypes constitutively produce an intermediate number of branches and also flower earlier than the more plastic genotypes that responded to the nutrient treatment. One interpretation of these results is that flowering time and branch number are traded off in some way, reflecting at the extremes alternative strategies to cope with low nitrogen availability: an escape strategy of early flowering, and a mitigation strategy involving additional nutrient foraging. Using quantitative genetics methods, we found that the genetic basis for this response is likely to be complex, although not intractable when analysis methods that take into account genetic variability at the relevant candidate loci are used. The capacity of organisms to tune their development in response to environmental cues is pervasive in nature. This phenotypic plasticity is particularly striking in plants, enabled by their modular and continuous development. A good example is the activation of lateral shoot branches in Arabidopsis, which develop from axillary meristems at the base of leaves. The activity and elongation of lateral shoots depends on the integration of many signals both external (e.g. light, nutrient supply) and internal (e.g. the phytohormones auxin, strigolactone and cytokinin). Here, we characterise natural variation in plasticity of shoot branching in response to nitrate supply using two diverse panels of Arabidopsis lines. We find extensive variation in nitrate sensitivity across these lines, suggesting a genetic basis for variation in branching plasticity. High plasticity is associated with extreme branching phenotypes such that lines with the most branches on high nitrate have the fewest under nitrate deficient conditions. Conversely, low plasticity is associated with a constitutively moderate level of branching. Furthermore, variation in plasticity is associated with alternative life histories with the low plasticity lines flowering significantly earlier than high plasticity lines. In Arabidopsis, branching is highly correlated with fruit yield, and thus low plasticity lines produce more fruit than high plasticity lines under nitrate deficient conditions, whereas highly plastic lines produce more fruit under high nitrate conditions. Low and high plasticity, associated with early and late flowering respectively, can therefore be interpreted alternative escape vs mitigate strategies to low N environments. The genetic architecture of these traits appears to be highly complex, with only a small proportion of the estimated genetic variance detected in association mapping.