Modeling developmental plasticity in variable environments through gene duplication: a case for phytochromes and gibberellin3-oxidases’ role in temperature-dependent seed germination

Abstract

Seed germination is a critical developmental transition in plants and is regulated by complex combinations of environmental cues that restrict its timing to occur over the widest possible range of conditions suitable for subsequent survival. To investigate the genetic mechanisms by which seeds achieve this restriction, we characterized the functional diversification of two duplicated gene families, phytochromes and gibberellin3-oxdiases, involved in temperature dependent seed germination. Germination responses were recorded of single and multiple PHY and GA3ox functional knockout mutants after exposure to various temperature treatments reflecting seasonal conditions. PHYE was the only copy necessary for germination in cold temperatures after a cold imbibition treatment, while PHYB was an important contributor to germination after seeds did not experience a dormancy-breaking imbibition treatment. GA3ox2 was the most important GA3ox contributor to germination in a range of temperature conditions while GA3ox1 and GA3ox3 appeared to contribute redundantly to germination with GA3ox2, the first evidence of GA3ox3’s role during temperature-dependent germination. The diversification of these genes during germination suggests that gene duplication plays an important role in regulating a plant’s response to complex seasonal environments. We then constructed a basic two-step genetic pathway model to investigate how environmental sensitive and/or functionally diversified duplicated genes are able to restrict a physiological response, such as germination, to combinations of environmental cues. Identical diversifications in duplicated upstream and downstream genes resulted in the most precise restriction of responses around optimal environmental conditions. Moreover, environmental sensitive diversification within duplicated genes was required in order to elicit a physiological response to more than one set of optimal environmental conditions supporting the importance of diversified duplicated genes in achieving developmental plasticity in variable seasonal environments.