Strong photoperiod sensitivity is controlled by cooperation and competition among Hd1, Ghd7 and DTH8 in rice heading

Abstract

Rice (Oryza sativa) is a short-day (SD) plant originally having strong photoperiod sensitivity (PS), with SDs promoting and long days (LDs) suppressing flowering. Although the evolution of PS in rice has been extensively studied, there are few studies that combine the genetic effects and underlying mechanism of different PS gene combinations with variations in PS. We created a set of isogenic lines among the core PS-flowering genes Hd1, Ghd7 and DTH8 using CRISPR mutagenesis, to systematically dissect their genetic relationships under different day-lengths. We investigated their monogenic, digenic, and trigenic effects on target gene regulation and PS variation. We found that Hd1 and Ghd7 have the primary functions for promoting and repressing flowering, respectively, regardless of day-length. However, under LD conditions, Hd1 promotes Ghd7 expression and is recruited by Ghd7 and/or DTH8 to form repressive complexes that collaboratively suppress the Ehd1-Hd3a/RFT1 pathway to block heading, but under SD conditions Hd1 competes with the complexes to promote Hd3a/RFT1 expression, playing a tradeoff relationship with PS flowering. Natural allelic variations of Hd1, Ghd7 and DTH8 in rice populations have resulted in various PS performances. Our findings reveal that rice PS flowering is controlled by crosstalk of two modules-Hd1-Hd3a/RFT1 in SD conditions and (Hd1/Ghd7/DTH8)-Ehd1-Hd3a/RFT1 in LD conditions and the divergences of these genes provide the basis for rice adaptation to broad regions.

Characterization of the Ghd8 Flowering Time Gene in a Mini-Core Collection of Miscanthus sinensis

“…In A. thaliana, HAP3b subunits can directly interact with Hd1/CO through its CCT-domain, forming CCAAT-binding CBF complexes that bind to FT promoters and activate transcription to promote flowering under LD [66,67]. In rice, the grass-specific gene Ghd7 is upregulated by a Ghd8-OsHAP5b-Hd1 complex under LD, enabling Ghd7 to suppress Ehd1 and delay flowering [36,63,[68][69][70][71][72]. However, Hd1/CO also competes with the complexes to promote Hd3a/RFT1 expression, creating a tradeoff relationship for photoperiod sensitive flowering under SD conditions.…”

Transcriptional and post‐transcriptional regulation of heading date in rice

“…This view is supported by the observation that a functional Ghd7 , DTH8 and Hd1 combination showed significantly stronger photoperiod sensitivity than other combinations in both near‐isogenic lines and natural populations (Zhang et al ., 2015; Wang et al ., 2019; Z.Y. Zhang et al ., 2019; Zong et al ., 2021), although there might be other types of transcriptional or post‐transcriptional regulation involving one or more of them (Wang et al ., 2019). For example, Hd1, DTH8 and distinct NF‐YC subunits reported to form a trimeric complex that bound to the CO Response Element 2 ( CORE2 ) in the Hd3a promoter, and Days to heading 7 (DTH7, also known as Hd2, OsPRR37 or Ghd7.1, another CCT domain‐containing protein strongly repressing flowering) can replace Hd1 in the complex (Goretti et al ., 2017).…”

“…Hd1 also loses LD heading suppression function and consistently promotes flowering under SD and LD in Ghd7 ‐ or DTH8 ‐deficient backgrounds (Nemoto et al ., 2016; Du et al ., 2017; Zhang et al ., 2017; Zong et al ., 2021). Transcriptional analyses revealed that Ghd7 and Hd1 do not regulate each other’s transcription levels, suggesting that the observed genetic interaction might occur post‐transcriptionally (Nemoto et al ., 2016).…”

“…Several recent studies have revealed that both Ghd7 and DTH8 can interact with Hd1 and that DTH8 also interacts with Ghd7. Therefore, although Hd1 has the primary function for promoting expression of Hd3a/RFT1 and flowering regardless of day length, it can form a ternary repressive complex with DTH8 and Ghd7 to mediate photoperiodic heading (Cai et al ., 2019; Zong et al ., 2021). This view is supported by the observation that a functional Ghd7 , DTH8 and Hd1 combination showed significantly stronger photoperiod sensitivity than other combinations in both near‐isogenic lines and natural populations (Zhang et al ., 2015; Wang et al ., 2019; Z.Y.…”

“…Hd1 , Ghd7 , DTH8 , Hd16 , DTH7 and PhyB are flowering repressor genes under LDs. Combined Hd1 , Ghd7 and DTH8 alleles produce strong photoperiod sensitivity, and are preferably distributed to low latitudes (Zong et al ., 2021). Deletion or weakened alleles of these genes are associated with early flowering under natural day length and are preferably distributed to high latitudes (Xue et al ., 2008; Takahashi et al ., 2009; Wei et al ., 2010; Huang et al ., 2012; Koo et al ., 2013; Gao et al ., 2014; Kwon et al ., 2014).…”