A conserved molecular basis for photoperiod adaptation in two temperate legumes

Abstract

Legumes were among the first plant species to be domesticated, and accompanied cereals in expansion of agriculture from the Fertile Crescent into diverse environments across the Mediterranean basin, Europe, Central Asia, and the Indian subcontinent. Although several recent studies have outlined the molecular basis for domestication and eco-geographic adaptation in the two main cereals from this region, wheat and barley, similar questions remain largely unexplored in their legume counterparts. Here we identify two major loci controlling differences in photoperiod response between wild and domesticated pea, and show that one of these, HIGH RESPONSE TO PHOTOPERIOD (HR), is an ortholog of EARLY FLOWERING 3 (ELF3), a gene involved in circadian clock function. We found that a significant proportion of flowering time variation in global pea germplasm is controlled by HR, with a single, widespread functional variant conferring altered circadian rhythms and the reduced photoperiod response associated with the spring habit. We also present evidence that ELF3 has a similar role in lentil, another major legume crop, with a distinct functional variant contributing to reduced photoperiod response in cultivars widely deployed in short-season environments. Our results identify the factor likely to have permitted the successful prehistoric expansion of legume cultivation to Northern Europe, and define a conserved genetic basis for major adaptive changes in flowering phenology and growth habit in an important crop group.crop adaptation | Pisum sativum | Lens culinaris M any of the world's earliest agricultural systems were based around crops from two important groups: cereals and legumes. Although molecular and genetic analyses have led to considerable progress in understanding the genetic changes underlying domestication and adaptation in several cereal crops, similar efforts in legumes are in general much less advanced. Among the legumes domesticated in the world's oldest farming culture in the Neolithic Near East, the temperate long-day (LD) species lentil (Lens culinaris Medik.), pea (Pisum sativum L.), and chickpea (Cicer arietinum L.) all persist as crops of global economic importance. Of these crops, pea has the widest distribution, the most diverse phenology, and is the best understood genetically, and offers prospects for a detailed exploration of molecular events important in early cultivation and spread (1, 2).P. sativum is now generally viewed as a complex species that includes a wide variety of cultivated and wild forms with pink, purple, or white flowers (1). Wild P. sativum lines are characterized by dehiscent pods and a rough, thick seed coat, and include both tall, climbing forms distributed around the Mediterranean (P. sativum var. elatius) and shorter forms restricted to the Near East (P. sativum var. humile), which intergrade in their areas of overlap. Cytogenetic differences and analyses of genetic diversity support the view that the majority of cultivated peas originated from a distinct gene pool within var....

EARLY FLOWERING3 Redundancy Fine-Tunes Photoperiod Sensitivity

“…We subsequently identified a third recessive mutant allele, ppd-3, from EMS mutagenesis of the pea line NGB5839 (Hecht et al, 2007), which has been widely used as a reference wild-type line. Both of these parental lines carry the same hr mutation (Weller et al, 2012). Figure 1 and Supplemental Figure S1 confirm that in contrast to the photoperiod-responsive wild type (P , 0.001), the ppd-3 allele confers early flowering (P , 0.001) regardless of photoperiod, equivalent to ppd-1 and ppd-2 (Taylor and Murfet, 1996) and to sn and dne mutants (Murfet, 1971;King and Murfet, 1985;Liew et al, 2009Liew et al, , 2014.…”

“…In the closely syntenic region of Medicago truncatula chromosome 1, these markers correspond to gene models Medtr1g009200 and Medtr1g018840 and define an interval of around 4.3 Mb containing ;900 genes. Within this region we identified several genes potentially related to flowering time control, including two miR156 genes, the CONSTANS-like gene COLb (Wong et al, 2014), and a gene with strong similarity to the previously described HR/ELF3 gene (Weller et al, 2012), which we termed ELF3b. In view of the circadian clockrelated role of PPD, we considered only the last two sequences as plausible candidates.…”

“…In the long-day legume species pea, the ELF3 ortholog HR has a central role in photoperiod adaptation, with a null mutation conferring partial loss of photoperiod responsiveness and earlier flowering under short photoperiods, and this appears to have been central to adaptation of the crop to spring sowing and expansion to higher latitudes (Weller et al, 2012). Naturally occurring and induced mutations in the LUX ortholog SN completely eliminate responsiveness to photoperiod (Liew et al, 2014), whereas a mutant for the ELF4 ortholog DNE enhances the effect of the hr mutation but has little effect when functional HR is present (Liew et al, 2009(Liew et al, , 2014.…”

“…Interestingly, in both crop groups, mutations in ELF3 genes have been shown to contribute to the expansion in range of species through alteration of photoperiod responsiveness and the associated impact on yield (Faure et al, 2012;Matsubara et al, 2012;Weller et al, 2012;Zakhrabekova et al, 2012;Alvarez et al, 2016;Lu et al, 2017). In crop species, a role for ELF4 function has been clearly established only in the legume species pea (Pisum sativum; Liew et al, 2009), but mutations in LUX orthologs have also been shown to cause early flowering and impaired photoperiod response in pea and in the cereals einkorn wheat (Triticum aestivum) and barley (Hordeum vulgare; Mizuno et al, 2012;Campoli et al, 2013;Liew et al, 2014), suggesting that the EC genes are likely to be intimately linked to the photoperiod response mechanism in both crop groups.…”

Molecular characterisation of flowering genes in Pongamia Pinnata

“…In legumes such as Pisum sativum (pea), Glycine max (Soybean) and Medicago truncatula (Medicago), studies on flowering gene orthologues have discovered several genes with a conserved role in the regulation of flowering time in response to photoperiod. However, the function of these CO homologues in photoperiod response is still not clear (Hecht et al, 2005;Hecht et al, 2007;Jiang et al, 2011;Liu et al, 2011;Watanabe et al, 2011;Weller et al, 2012;Wong et al, 2014).…”