Mutations in LTP2 give rise to stochastic variation in a young seedling phenotype

Isogenic individuals often display seemingly random phenotypic differences which limit the accuracy of genotype-to-phenotype predictions. Since the range of possible phenotypes is genotype-dependent, a key question is which genes most contribute to phenotypic variability. Focusing on hypocotyl elongation in the dark, a trait relevant for seedling establishment, we found that strong knock-downs of the cuticle-related gene LTP2 greatly increased non-genetic variability in Arabidopsis hypocotyl phenotypes, including length, gravitropism and cuticle permeability. Most ltp2 hypocotyls were shorter than wild-type, and showed strong activation of stress and defense response genes. Differences in epidermal properties and gene expression between ltp2 seedlings with long and short hypocotyls are compatible with loss of cuticle integrity as the primary determinant of phenotypic variability. We identified environmental conditions that revealed or masked variability in the ltp2 background, and found that upregulation of its closest paralog LTP1 contributes to ltp2 phenotypes. Our results exemplify how reduced stress tolerance can generate phenotypic variability under an otherwise constant environment, and highlight the role of epidermal structural integrity in buffering random variation. alternative: Our results illustrate the potential of plant cuticles to generate non-heritable variation in growth phenotypes, and highlight the general role of environmentally-responsive genes in shaping individual phenotypes.