Genes affecting phenotypic plasticity in Arabidopsis: pleiotropic effects and reproductive fitness of photomorphogenic mutants

Abstract

Abstract Many plants exhibit characteristic photomorphogenic shade ’avoidance’ responses to crowding and vegetation shade; this plasticity is often hypothesized to be adaptive. We examined the contribution of specific photomorphogenic loci to plastic shade avoidance responses in the annual crucifer Arabidopsis thaliana by comparing single-gene mutants defective at those loci with wild type plants exhibiting normal photomorphogenesis. The hy1 and hy2 mutants, deficient in all functional phytochromes, were less plastic than the wild type in response to a nearby grass canopy or to a low-red/far-red light ratio characteristic of vegetation shade. These mutants displayed constitutively shade-avoiding phenotypes throughout the life cycle regardless of the treatment: they bolted at an earlier developmental stage and were characterized by reduced branching. In contrast, the hy4 mutant, deficient in blue light reception, exhibited greater plasticity than the wild type in response to vegetation shade after the seedling stage. This mutant produced more leaves before bolting and more basal branches under normal light conditions when compared to the wild type. These results indicate that specific photomorphogenic loci have different and sometimes antagonistic pleiotropic effects on the plastic response to vegetation shade throughout the life cycle of the plant. The fitness of the constitutively shade-avoiding phytochrome-deficient mutants was lower than that of the plastic wild type under normal light, but was not different in the vegetation shade treatments, where all genotypes converged toward similar shade avoidance phenotypes. This outcome supports one key prediction of the adaptive plasticity hypothesis: that inappropriate expression of shade avoidance traits is maladaptive.