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

PLoS Genet. 2019 Sep 20;15(9):e1008366. doi: 10.1371/journal.pgen.1008366. eCollection 2019 Sep.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics*
  • Arabidopsis / metabolism
  • Arabidopsis Proteins / genetics
  • Gene Expression Regulation, Plant / genetics
  • Genes, Plant / genetics
  • Meristem / growth & development
  • Nitrates / metabolism*
  • Phenotype
  • Plant Leaves / metabolism
  • Plant Roots / genetics
  • Plant Shoots / genetics*
  • Plant Shoots / growth & development
  • Plant Shoots / metabolism

Substances

  • Arabidopsis Proteins
  • Nitrates

Grants and funding

This work was funded by a James Burgess Studentship to GG (https://www.york.ac.uk/biology/postgraduate/jamesburgessscholarship/); a Marie Currie Fellowship (PIEF-GA-2009-252761) from the European Commission (https://ec.europa.eu/research/fp7/index_en.cfm) to MdJ; and research grants to OL from the Gatsby Charitable Foundation (GAT3395/PR1 and GAT3071) (https://www.gatsby.org.uk/) and the European Research Council (No. 294514 – EnCoDe) (https://ec.europa.eu/research/fp7/index_en.cfm). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.