Natural Variation in OsPRR37 Regulates Heading Date and Contributes to Rice Cultivation at a Wide Range of Latitudes

Abstract

Heading date and photoperiod sensitivity are fundamental traits that determine rice adaptation to a wide range of geographic environments. By quantitative trait locus (QTL) mapping and candidate gene analysis using whole-genome re-sequencing, we found that Oryza sativa Pseudo-Response Regulator37 (OsPRR37; hereafter PRR37) is responsible for the Early heading7-2 (EH7-2)/Heading date2 (Hd2) QTL which was identified from a cross of late-heading rice 'Milyang23 (M23)' and early-heading rice 'H143'. H143 contains a missense mutation of an invariantly conserved amino acid in the CCT (CONSTANS, CO-like, and TOC1) domain of PRR37 protein. In the world rice collection, different types of nonfunctional PRR37 alleles were found in many European and Asian rice cultivars. Notably, the japonica varieties harboring nonfunctional alleles of both Ghd7/Hd4 and PRR37/Hd2 flower extremely early under natural long-day conditions, and are adapted to the northernmost regions of rice cultivation, up to 53° N latitude. Genetic analysis revealed that the effects of PRR37 and Ghd7 alleles on heading date are additive, and PRR37 down-regulates Hd3a expression to suppress flowering under long-day conditions. Our results demonstrate that natural variations in PRR37/Hd2 and Ghd7/Hd4 have contributed to the expansion of rice cultivation to temperate and cooler regions.

PHYTOCHROME C plays a major role in the acceleration of wheat flowering under long-day photoperiod

“…The PHYC-mediated light activation of PPD1 results in the convergence of light and circadian clock signals in the transcriptional regulation of PPD1, which is critical for measurement of day length, according to the external coincidence model (blue arrow). Under LD, PPD1/PRR37 up-regulates FT1 in barley and wheat (25) but down-regulates FT homologs in rice and sorghum (58,59). Upregulation of FT1 in wheat is associated with the up-regulation of FT2 (43,71), which also promotes flowering (72).…”

“…Mutations in PPD1/PRR37 are associated with photoperiod insensitivity genotypes both in sorghum and wheat, suggesting that this gene is critical for the perception of day-length differences in different grass species. In rice, natural variation in PRR37 also contributes to differences in photoperiodic response and to its ability to grow in a wide range of latitudes (59). The duplication that originated PRR37 and PRR73 in the grasses is independent of the duplication that generated PRR3 and PRR7 genes in Arabidopsis (60).…”

“…Under LD, CO/HD1 acts as a promoter of FT and flowering in Arabidopsis (47) but as a suppressor of HD3A and flowering in rice (56,61,62). Similarly, PPD1/PRR37 induces FT1 and accelerates flowering in barley and wheat (25,42) but suppresses FT and delays flowering in sorghum and rice (58,59). This signal reversal in PPD1/PRR37 may explain why phyC mutations accelerate flowering under LD in rice (13) but delay flowering in wheat (Fig.…”

PSEUDO RESPONSE REGULATORs stabilize CONSTANS protein to promote flowering in response to day length

“…In A. thaliana, they appear to influence the time‐keeping mechanism associated with CO transcription in the photoperiodic flowering pathway indirectly through their role in the circadian clock (Nakamichi et al , 2007; Ito et al , 2008). On the other hand, in crops such as barley and rice, their effects on CO transcription are relatively weak, whereas they strongly affect FT transcription (Turner et al , 2005; Campoli et al , 2012; Koo et al , 2013). Therefore, these PRRs are likely to have a more direct effect on the regulation of the photoperiodic flowering pathway.…”

A Drought-Inducible Transcription Factor Delays Reproductive Timing in Rice

“…Ehd1 encodes a rice-specific B-type response factor that acts in both LDs and SDs to promote Hd3a and RFT1 mRNA expression, thus inducing floral initiation (Doi et al, 2004;Komiya et al, 2009;Sun et al, 2014). Many repressors or activators, including Ehd2, Ehd3, Ehd4, Ghd7, OsMADS51, OsLFL1, and OsPPR37/ DTH7, regulate the expression and activity of Ehd1 itself in day length-dependent or -independent manners (Doi et al, 2004;Kim et al, 2007;Peng et al, 2007;Xue et al, 2008;Wei et al, 2010;Matsubara et al, 2011;Koo et al, 2013;Tsuji et al, 2013;Yan et al, 2013;Kwon et al, 2015). It appears that Ehd1 is under the convergent regulation of SD activators, LD repressors, and photoperiod-independent regulators to control the heading date of rice in response to the internal development "clock" and environmental cues.…”