Genetic variation in four maturity genes affects photoperiod insensitivity and PHYA-regulated post-flowering responses of soybean

Abstract

BackgroundAbsence of or low sensitivity to photoperiod is necessary for short-day crops, such as rice and soybean, to adapt to high latitudes. Photoperiod insensitivity in soybeans is controlled by two genetic systems and involves three important maturity genes: E1, a repressor for two soybean orthologs of Arabidopsis FLOWERING LOCUS T (GmFT2a and GmFT5a), and E3 and E4, which are phytochrome A genes. To elucidate the diverse mechanisms underlying photoperiod insensitivity in soybean, we assessed the genotypes of four maturity genes (E1 through E4) in early-flowering photoperiod-insensitive cultivars and their association with post-flowering responses.ResultsWe found two novel dysfunctional alleles in accessions originally considered to have a dominant E3 allele according to known DNA markers. The E3 locus, together with E1 and E4, contained multiple dysfunctional alleles. We identified 15 multi-locus genotypes, which we subdivided into 6 genotypic groups by classifying their alleles by function. Of these, the e1-as/e3/E4 genotypic group required an additional novel gene (different from E1, E3, and E4) to condition photoperiod insensitivity. Despite their common pre-flowering photoperiod insensitivity, accessions with different multi-locus genotypes responded differently to the post-flowering photoperiod. Cultivars carrying E3 or E4 were sensitive to photoperiod for post-flowering characteristics, such as reproductive period and stem growth after flowering. The phytochrome A–regulated expression of the determinate growth habit gene Dt1, an ortholog of Arabidopsis TERMINAL FLOWER1, was involved in the persistence of the vegetative activity at the stem apical meristem of flower-induced plants under long-day conditions.ConclusionsDiverse genetic mechanisms underlie photoperiod insensitivity in soybean. At least three multi-locus genotypes consisting of various allelic combinations at E1, E3, and E4 conferred pre-flowering photoperiod insensitivity to soybean cultivars but led to different responses to photoperiod during post-flowering vegetative and reproductive development. The phyA genes E3 and E4 are major controllers underlying not only pre-flowering but also post-flowering photoperiod responses. The current findings improve our understanding of genetic diversity in pre-flowering photoperiod insensitivity and mechanisms of post-flowering photoperiod responses in soybean.

The Soybean-Specific Maturity Gene E1 Family of Floral Repressors Controls Night-Break Responses through Down-Regulation of FLOWERING LOCUS T Orthologs

“…The three loci (E1, E3, and E4), together with E2, an ortholog of Arabidopsis GIGANTEA (GI; Watanabe et al, 2011), are major contributors to the variation in flowering time among soybean cultivars (Xu et al, 2013;Tsubokura et al, 2014). Photoperiod insensitivity in cultivars adapted to high-latitude environments has been independently and repeatedly generated through mutations at E1, E3, and E4 (Tsubokura et al, 2013;Xu et al, 2013).…”

“…Photoperiod insensitivity in cultivars adapted to high-latitude environments has been independently and repeatedly generated through mutations at E1, E3, and E4 (Tsubokura et al, 2013;Xu et al, 2013). However, it remains to be determined what molecular mechanisms are involved in the responses of soybean to changes in photoperiod and to short periods of light given during the dark phase.…”

Changing Responses to Changing Seasons: Natural Variation in the Plasticity of Flowering Time

“…Some of these loci represent allelic series, and different subsets of the loci may be combined to produce equivalent day-neutral phenotypes (e.g. Xu et al, 2013;Jiang et al, 2014).…”

“…Spontaneous and induced mutations in the barley (Hordeum vulgare) ELF3 homolog also have contributed to the production of barley breeds cultivated in the short growing seasons of northern regions (Faure et al, 2012;Zakhrabekova et al, 2012). In cultivated soybean (Glycine max), coding polymorphisms at four loci, including variants leading to premature stops in two paralogs homologous to phytochrome A and a homolog of GIGANTEA, combine to build the latitudinal cline such that photoperiod sensitivity decreases with increasing latitude (Zhang et al, 2008;Xu et al, 2013;Jiang et al, 2014). These same alleles do not explain a similar cline in wild soybean, however.…”

“…Many more possible mutations eliminate gene function than selectively reduce, modulate, or add new function. Consequently, when loss of function does confer a favorable phenotype, the adaptive mutation rate is higher, and convergent evolution through allelic series like those seen for FRI in Arabidopsis (Shindo et al, 2005), pseudo-response regulators in grasses (Yan et al, 2004;Xue et al, 2008;Koo et al, 2013), or soybean phytochromes (Xu et al, 2013;Jiang et al, 2014) are more likely. Table I.…”