The evening complex promotes maize flowering and adaptation to temperate regions

Abstract

Maize (Zea mays) originated in southern Mexico and has spread over a wide latitudinal range. Maize expansion from tropical to temperate regions has necessitated a reduction of its photoperiod sensitivity. In this study, we cloned a quantitative trait locus (QTL) regulating flowering time in maize and show that the maize ortholog of Arabidopsis thaliana EARLY FLOWERING3, ZmELF3.1, is the causal locus. We demonstrate that ZmELF3.1 and ZmELF3.2 proteins can physically interact with ZmELF4.1/4.2 and ZmLUX1/2, to form evening complex(es) (EC) in the maize circadian clock. Loss-of-function mutants for ZmELF3.1/3.2 and ZmLUX1/2 exhibited delayed flowering under long-day and short-day conditions. We show that EC directly represses the expression of several flowering suppressor genes, such as the CONSTANS, CONSTANS-LIKE, TOC1 (CCT) genes ZmCCT9 and ZmCCT10, ZmCONSTANS-LIKE 3, and the PSEUDORESPONSE REGULATOR (PRR) genes ZmPRR37a and ZmPRR73, thus alleviating their inhibition, allowing florigen gene expression and promoting flowering. Further, we identify two closely linked retrotransposons located in the ZmELF3.1 promoter that regulate the expression levels of ZmELF3.1 and may have been positively selected during post-domestication spread of maize from tropical to temperate regions during the pre-Columbian era. These findings provide insights into circadian clock-mediated regulation of photoperiodic flowering in maize and new targets of genetic improvement for breeding.

EARLY FLOWERING 3interactions withPHYTOCHROME BandPHOTOPERIOD1are critical for the photoperiodic regulation of wheat heading time

“…Our ChIP-PCR experiments support the hypothesis that this is the result of the direct transcriptional regulation of PPD1 by ELF3 (Fig 8). A similar interaction has been reported in Brachypodium [72], rice [39] and maize [49] suggesting that is conserved in the grass species.…”

“…The ppd1 mutant delays heading time even in an elf3 background, indicating that it operates downstream of ELF3. This is also evident in the changes of PPD1 transcription profiles observed interaction has been reported in Brachypodium [72], rice [39] and maize [49] suggesting that is conserved in the grass species.…”

“…The role of ELF3 on the regulation of flowering time has been extensively studied given the importance of this trait in the adaptation of crop species to different latitudes [27,30,[45][46][47][48][49]. The early heading time of the elf3 Kronos mutants in LD and SD and the delayed heading time of the UBI::ELF3:HA transgenic plants indicate that ELF3 functions as a heading time repressor in wheat.…”

The battle of crops against drought: Genetic dissection and improvement

“…Some MADS‐box transcription factors also affect flowering time in maize, including ZmMADS1, ZmMADS4 (also named ZMM4 for ZEA MAYS MADS4), ZmMADS15 (ZMM15), ZmMADS67, and ZmMADS69 (Danilevskaya et al, 2008; Alter et al, 2016; Liang et al, 2019; Sun et al, 2020). In addition, several factors involved in photoperiod signaling, such as phytochrome B1 (PhyB1), PhyB2, LONG HYPOCOTYL 2 (ZmHY2), CONSTANS‐like 3 (ZmCOL3), ZmCCT9 (CO, COL, TOC1 9), and ZmCCT10, repress flowering under LDs (Huang et al, 2017; Du et al, 2018; Jin et al, 2018; Su et al, 2021b; Zhao et al, 2022). The circadian clock evening complex promotes flowering by repressing the expression of flowering repressor genes (Zhao et al, 2022).…”

“…In addition, several factors involved in photoperiod signaling, such as phytochrome B1 (PhyB1), PhyB2, LONG HYPOCOTYL 2 (ZmHY2), CONSTANS‐like 3 (ZmCOL3), ZmCCT9 (CO, COL, TOC1 9), and ZmCCT10, repress flowering under LDs (Huang et al, 2017; Du et al, 2018; Jin et al, 2018; Su et al, 2021b; Zhao et al, 2022). The circadian clock evening complex promotes flowering by repressing the expression of flowering repressor genes (Zhao et al, 2022). ZmNF‐YC2 , which was identified by QTL fine mapping, encodes nuclear factor Y (NF‐Y) subunit C‐2, which regulates flowering time in maize under LDs (Su et al, 2021a).…”