Environmental control of rice flowering time

Abstract

Correct measurement of environmental parameters is fundamental for plant fitness and survival, as well as for timing developmental transitions, including the switch from vegetative to reproductive growth. Important parameters that affect flowering time include day length (photoperiod) and temperature. Their response pathways have been best described in Arabidopsis, which currently offers a detailed conceptual framework and serves as a comparison for other species. Rice, the focus of this review, also possesses a photoperiodic flowering pathway, but 150 million years of divergent evolution in very different environments have diversified its molecular architecture. The ambient temperature perception pathway is strongly intertwined with the photoperiod pathway and essentially converges on the same genes to modify flowering time. When observing network topologies, it is evident that the rice flowering network is centered on EARLY HEADING DATE 1, a rice-specific transcriptional regulator. Here, we summarize the most important features of the rice photoperiodic flowering network, with an emphasis on its uniqueness, and discuss its connections with hormonal, temperature perception, and stress pathways.

Keywords: florigens; flowering; photoperiod; rice; stress; temperature.

Figure 1

Gene regulatory networks controlling rice photoperiodic flowering. The networks represent the transcriptional relationships that take place under LDs and SDs. Regulatory signals ultimately converge on Ehd1 and florigen transcription. Genes indicated in purple act as flowering inhibitors, and those in green act as promoters. Genes indicated in bold have a stronger impact on flowering time, as inferred from the effects of their corresponding loss-of-function mutants. Some positive and negative regulators of Ehd1 and Ghd7 have been grouped in boxes to simplify graphical representation. Arrows and flat-ended arrows indicate transcriptional activation and repression, respectively. The interaction of light with gene expression is indicated by lightning symbols.

Figure 2

Diurnal accumulation patterns of major flowering regulators under LD (boxes on the left) and SD (boxes on the right) show the central position of Ghd7 in the external coincidence model of rice flowering. The peak of GI transcription tracks dusk under LDs and SDs. The GI protein interacts with Ghd7 and contributes to its degradation in a 26S proteasome–dependent manner. Transcription of Ghd7 is sensitive to red light, with a gate of inducibility (red shading) that occurs during the morning under LDs. The gate shifts to the night under SDs, and although few publications have reported reduced transcription under SDs, a larger consensus indicates a transcriptional peak in the morning, not different from the one detected under LDs. Irrespective of transcription, the Ghd7 protein does not accumulate under SDs or in phyB mutants, but it does show reduced accumulation in GI overexpressors. Thus, light- and photoperiod-dependent regulatory layers determine Ghd7 abundance. Ehd1 expression is gated in the morning by blue light signals (blue shading). OsGI can induce Ehd1 transcription under SDs when not antagonized by the Ghd7 protein. The diurnal profile of Ehd1 transcription is also determined by Hd1 and PRR37, which promote its expression under SDs and repress it under LDs. Finally, Hd3a and RFT1 are transcribed under SDs by a combination of Hd1- and Ehd1-mediated induction. Under LDs, florigen expression is repressed by Hd1, and induction by Ehd1 is limited. Eventually, RFT1 escapes repression under LDs and is transcribed to promote flowering. Solid and dashed lines indicate protein and mRNA accumulation patterns, respectively. A clock symbol indicates that the gene is under circadian clock control.

Figure 3

Post-transcriptional levels of regulation in the flowering-time network. We identified four hubs corresponding to Hd1, PRR37, Ehd1, and the florigens. (A) Hd1 hub. Hd1 forms Hd1/NF-Y complexes that directly repress expression of florigens under LDs. Repression is released in SDs, and Hd1 becomes an activator. Hd1 stability depends on HAF1 and on components of the autophagy pathway, including ATG proteins, in the vacuole. Hd1 can be phosphorylated by OsK4, and this modification might impact Hd1 stability. (B) OsPRR37 hub. OsPRR37 can replace Hd1 in an NF-Y complex and repress florigen expression under LDs. It can be phosphorylated by CKI and CKIIα. Phosphorylation might affect PRR37 stability or activity. (C) Ehd1 hub. Ehd1 is repressed under LDs by the Ghd7/Hd1 and OsRE1/OsRIP1 complexes. Phosphorylation is essential for Ehd1 dimerization and activity. OsRR1 interacts with Ehd1 to form an inactive complex and inhibit its capacity to induce expression of the florigens. Phosphorylation of Ghd7 by CKI enhances its repressor activity. (D) Florigen hub. Activity of the florigens depends on their transport in the phloem, which takes place by physical interaction with OsFTIP proteins and OsTPR075. Proteins are indicated by ovals and genes by rectangles. Names of DNA motifs bound by proteins or protein complexes are indicated below the double helix. Red and blue arrows indicate LD and SD regulation, respectively. Dashed arrows/flat-ended arrows indicate transcriptional activation/repression. Continuous arrows +P indicate phosphorylation. Continuous flat-ended arrows indicate protein degradation.

Figure 4

Balancing signals during the meristematic switch to reproductive growth. Meristems on top represent the approximate stages during which the molecular events represented below occur. (A) The balance between SPLs and miR156/529 determines the branching pattern and vegetative features of the inflorescence. (B) Florigens transported from the leaves form FACs that induce transcription of MADS-box genes and switch the developmental fate of the meristem. DHD4 competes with OsFD1 to bind Gf14 under LDs. (C) The reproductive switch is antagonized by FRCs, and RCNs transported from the leaves compete with the florigens for binding to Gf14s.

Figure 5

Gene regulatory networks controlling flowering under drought stress. (A) A rice paddy field experiencing severe drought during summer 2022 in northern Italy. Droughts hit several countries in 2022. (B) Molecular network controlling Ehd1 expression in response to mild and severe drought stress. Arrows and flat-ended arrows indicate transcriptional activation and repression, respectively. Genes indicated in purple act as flowering inhibitors, and those in green act as promoters. Green arrows indicate increased biosynthesis.