Coincident light and clock regulation of pseudoresponse regulator protein 37 ( PRR37 ) controls photoperiodic flowering in sorghum

Abstract

Optimal flowering time is critical to the success of modern agriculture. Sorghum is a short-day tropical species that exhibits substantial photoperiod sensitivity and delayed flowering in long days. Genotypes with reduced photoperiod sensitivity enabled sorghum's utilization as a grain crop in temperate zones worldwide. In the present study, Ma 1 , the major repressor of sorghum flowering in long days, was identified as the pseudoresponse regulator protein 37 (PRR37) through positional cloning and analysis of SbPRR37 alleles that modulate flowering time in grain and energy sorghum. Several allelic variants of SbPRR37 were identified in early flowering grain sorghum germplasm that contain unique loss-of-function mutations. We show that in long days SbPRR37 activates expression of the floral inhibitor CONSTANS and represses expression of the floral activators Early Heading Date 1, FLOWERING LOCUS T, Zea mays CENTRORADIALIS 8, and floral induction. Expression of SbPRR37 is light dependent and regulated by the circadian clock, with peaks of RNA abundance in the morning and evening in long days. In short days, the evening-phase expression of SbPRR37 does not occur due to darkness, allowing sorghum to flower in this photoperiod. This study provides insight into an external coincidence mechanism of photoperiodic regulation of flowering time mediated by PRR37 in the short-day grass sorghum and identifies important alleles of SbPRR37 that are critical for the utilization of this tropical grass in temperate zone grain and bioenergy production.is a C4 grass native to Africa that provides an indispensable food source for over 300 million people inhabiting food-insecure regions worldwide (1). Although primarily grown for its grain and forage, highbiomass sorghum is also an excellent drought-tolerant energy crop for sustainable production of lignocellulosic-based biofuels (2). Forage and energy sorghums are selected for delayed flowering to increase biomass yield through longer duration of vegetative growth, whereas grain sorghums are selected for early flowering to ensure sufficient time for grain maturation and to avoid drought and frost. Optimal production of each of these sorghum crops requires the precise regulation of flowering time, which varies depending on planting location and climate. Differences in photoperiod sensitivity confer a wide range of flowering times on diverse accessions of the sorghum germplasm collection (3). Due to its critical importance to crop yield and hybrid seed production, photoperiodic regulation of flowering has been an important trait characterized by sorghum improvement programs dating back to the early 1900s (4).In Arabidopsis, flowering is induced in long days (LD) that expose plants to light in the evening during a phase of circadian clock oscillation required for induction of floral genes, consistent with the external coincidence model (5-7). Rhythmic expression of the core circadian clock components CIRCADIAN CLOCK ASSOCIATED 1 (CCA1)/LATE ELONGATED HYPOCOTYL (LHY) and TIMING OF CAB 1...

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

“…3). A similar convergence has been described in the regulation of the sorghum PPD1 homolog PRR37 (= Ma 1 ), a gene that has a large impact on sorghum flowering time and has been critical for the early domestication and dispersal of this species (58). 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.…”

“…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.…”

ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize

“…For example, in the self-fertilizing tropical cereal crop sorghum, a handful of genes control most of the variation for photoperiod response in cultivated varieties, and allelic variation at the Ma1 locus alone can change flowering time by 60 d under long day lengths (30). In contrast, we discovered 14 maize QTLs for photoperiod response at which the strongest allele changes flowering time by only approximately 3 d when homozygous under long day lengths (7).…”

Transcriptome Profiling of Tiller Buds Provides New Insights into PhyB Regulation of Tillering and Indeterminate Growth in Sorghum

“…Grain sorghum is classified as weakly perennial (Dewet and Huckabay, 1967), but sorghum germplasm can exhibit a wide range of annual to perennial growth habits. Sorghum and maize florigens are produced in leaves by ZCN8/ SbCN8 and ZCN12/SbCN12 (Danilevskaya et al, 2010;Murphy et al, 2011). Flowering in sorghum is inhibited in long day photoperiods by repressing the expression of SbCN8 and SbCN12 through a pathway that requires phyB-signaling (Murphy et al, 2011;Yang et al, 2014).…”

“…Sorghum and maize florigens are produced in leaves by ZCN8/ SbCN8 and ZCN12/SbCN12 (Danilevskaya et al, 2010;Murphy et al, 2011). Flowering in sorghum is inhibited in long day photoperiods by repressing the expression of SbCN8 and SbCN12 through a pathway that requires phyB-signaling (Murphy et al, 2011;Yang et al, 2014). Therefore, phyB-1 or shaded plants have greater propensity to produce FT, and increased expression of TFL1 (SbCN2) in axillary buds of these plants may be needed to prevent precocious floral transition.…”