Diversification of phytochrome contributions to germination as a function of seed‐maturation environment

Abstract

Summary• Environmental conditions during seed maturation influence germination, but the genetic basis of maternal environmental effects on germination is virtually unknown.• Using single and multiple mutants of phytochromes, it is shown here that different phytochromes contributed to germination differently, depending on seed-maturation conditions.• Arabidopsis thaliana wild-type seeds that were matured under cool temperatures were intensely dormant compared with seeds matured at warmer temperature, and this dormancy was broken only after warm seed-stratification followed by cold seedstratification. The warm-cold stratification broke dormancy in fresh seeds but not in dry after-ripened seeds. Functional PHYB and PHYD were necessary to break cool-induced dormancy, which indicates a previously unknown and ecologically important function for PHYD. Disruption of PHYA in combination with PHYD (but not PHYB) restored germination to near wild-type levels, indicating that PHYA contributes to the maintenance of cool-induced dormancy on a phyD background. Effects of seed-maturation temperature were much stronger than effects of seed-maturation photoperiod. PHYB contributed to germination somewhat more strongly in seeds matured under short days, whereas PHYD contributed to germination somewhat more strongly in seeds matured under long days.• The variable contributions of different phytochromes to germination as a function of seed-maturation conditions reveal further functional diversification of the phytochromes during the process of germination. This study identifies among the first genes to be associated with maternal environmental effects on germination.

Differential control of seed primary dormancy in Arabidopsis ecotypes by the transcription factor SPATULA

“…Arabidopsis seed primary dormancy is promoted by low-temperature conditions during seed development (23)(24)(25). Low temperature also increases seed dormancy in wheat and this correlates with an increase in Ta-MFT gene expression (29).…”

“…Environmental conditions during seed set influence dormancy status. For example, low temperature conditions result in increased primary dormancy of mature Arabidopsis seeds (23)(24)(25) by inducing expression of genes associated with dormancy and influencing ABA and GA levels (24).…”

Evolutionary Studies Illuminate the Structural-Functional Model of Plant Phytochromes

“…Further evidence that the contributions of individual phytochromes are environmentally dependent comes from investigation of the effects of photoperiod and temperature on germination. These studies revealed a role for phyD in breaking cool-induced seed dormancy and in mediating the effects of photoperiod during seed maturation (Donohue et al, 2007). They further revealed that phyD is important in seed germination when seeds were matured (Dechaine et al, 2009) or imbibed (Heschel et al, 2008) under high temperatures, whereas phyE was important when seeds were imbibed in high temperatures followed by low temperatures (Heschel et al, 2008) or when matured under high temperatures (Dechaine et al, 2009).…”

Induction of Dormancy in Arabidopsis Summer Annuals Requires Parallel Regulation of DOG1 and Hormone Metabolism by Low Temperature and CBF Transcription Factors

“…Previous work has shown that lowering seed maturation temperatures induces high levels of dormancy in rapid cycling Arabidopsis ecotypes (Schmuths et al, 2006;Donohue et al, 2008;Chiang et al, 2009) as well as other species (Fenner, 1991;Gu et al, 2006). We confirmed that this was indeed a dormancy phenomenon by stimulating high levels of germination in seeds matured at low temperatures by applying multiple dormancy breaking treatments or by removing coat-imposed dormancy by nicking the seed coat (see Supplemental Figure 1A online) and by showing that embryo and seed coat morphology was normal in seeds developed at 108C (see Supplemental Figures 1B and 1C online).…”

“…During seed maturation, the level of dormancy is highly dependent on the prevailing environmental conditions with low temperatures and to a lesser extent short photoperiods, inducing high levels of dormancy and modifying the cold responsiveness of germination (Munir et al, 2001;Schmuths et al, 2006). Genetic influences on the induction of strong primary dormancy by low seed maturation temperatures have been uncovered, with roles for both phytochrome and FLC having been proposed (Donohue et al, 2008;Chiang et al, 2009).…”