Flowering time regulation by the CONSTANS-Like gene OsCOL10

ABSTRACT

Plant flowering at the appropriate time is critical for reproductive success and influenced by a series of environmental factors such as photoperiod and temperature. A number of genes involved in photoperiodic flowering of have been cloned and their roles in modulating expression of the flowering genes have been characterized to a certain extent. However, much less is known about the pathway in transmitting the day length response signal(s) to induce transition to reproductive growth. Recently, we characterized a constitutive flowering repressor OsCOL10 encoding for a member of the CONSTANS-like (COL) family. Through transgenic analysis, we have showed that OsCOL10 repress flowering by reducing expression of the FT-like genes RFT1 and Hd3a through Ehd1. Moreover, we also showed that OsCOL10 acts downstream of Ghd7, a key LD-specific flowering repressor by reducing expression of Ehd1. Collectively, our finding identifies OsCOL10 functioning as a flowering-time repressor that links between Ghd7 and Ehd1 in rice.

Flowering is a complex transition from the vegetative to reproductive phase in plants, and is triggered by both endogenous and environmental signals, such as light and temperature.¹ Among environmental signals, the photoperiod or day length is one of the most important regulators of flowering and is perceived by plant leaves.^1-3 Especially in crops such as Rice, flowering time is a key agronomic trait that determines the cropping season and regional adaptability. Ghd7 (Grain number, plant height, heading date 7), which encodes a COL protein, acts as a strong LD-specific flowering repressor by repressing the expression of downstream Ehd1,⁴ a key flowering activator.⁵ Ehd1 and Ghd7 have no orthologs in the Arabidopsis genome, suggesting that Ghd7–Ehd1–Hd3a evolved as a rice-specific flowering suppression pathway.⁶ However, the mechanism of Ghd7 suppression is not yet known. Recently, we have characterized a rice constitutive flowering repressor, OsCOL10, which belongs to the CO-like family.⁷ OsCOL10 represses the expression of Ehd1 and is positively regulated by upstream Ghd7.⁷ Thus OsCOL10 establishes a functional link between Ghd7 and Ehd1 in the photoperiodic control of flowering.

In the paddy field, overexpression of OsCOL10 or OsCOL10-VP64 can significantly delay the heading date and increase the plant height as well as panicle size (Fig. 1),⁷ like its close homologues Ghd2 and Ghd7,^4,8 which suggests OsCOL10 also acts as a grain number, plant height and heading date-associated gene with a potential application incrop adaptation and breeding. Besides the roles in the regulation of photoperiodic flowering, Ghd2 (OsK) and Ghd7 both can regulate stress tolerance,^8,9 suggesting the possible new role of OsCOL10 in environmental stress. Indeed, OsCOL10 was highly and specifically expressed in leaves⁷ and additionally it was downregulated after treated by drought stress at 7-day-old seedling stage.⁸

Figure 1.

Phenotypic characterization of Kitaake and Pubi::OsCOL10-VP64 transgenic plants at paddy field in Beijing NLD conditions. (A) Phenotypic comparison when Kitaake is heading. (B) Phenotypic comparison when Kitaake is mature.

Under LDs, the expression of OsCOL10 was upregulated by Ghd7 in an indirect way and additionally OsCOL10 repressed the expression of Ehd1.⁷ Thus OsCOL10 passed on the repression signal of Ghd7 to the Ehd1. Since Ghd7 indirectly regulated Ehd1 and knockout of OsCOL10 did not significantly change the flowering time,^7,10 suggesting that other genes function redundantly with OsCOL10 in mediating the repression of Ghd7 to Ehd1 or other pathways are involved in this process. Because the other two members in group II, OsK and OsL, are the two closest homologs of OsCOL10, especially the OsK (Ghd2) which was recently reported to increase the heading date, plant height and grain number in rice.⁸ We had expected these two genes share the functional redundancy with OsCOL10. However, neither of them was regulated by Ghd7.^7,10 Actually they have different rhythmic expression pattern under LDs: OsCOL10 was mainly expressed under daytime with the peak at 4 h after dawn, similar to Ghd7, whereas OsK or Ghd2 expression was enriched at darkness.^4,7,8 Other Ehd1-regulated COL members, containing OsCOL4 and OsCOL13 acting redundantly to mediate the repression of PhyB to Ehd1, were not regulated by Ghd7.^11,12 Therefore, it strongly suggests that there exist other pathways implicated in the repression. Indeed, more recently, it was reported that Ghd7 can interact with Hd1 under LD conditions and the resulting complex specifically binds to a cis-regulatory region in Ehd1 to repress its expression.¹³ Thus, Hd1 partly functions in mediating the inhibition of Ghd7 to Ehd1in a direct way. It is noteworthy that Hd1 and Ghd7 together repressed Ehd1 only in the daytime under LD conditions while Ghd7 itself repressed Ehd1 at anytime in the day.¹³ Thus, it is possible that in the daytime the repression of Ehd1 by Ghd7 was through the two pathways: Hd1- and OsCOL10-mediated pathways, while in the nighttime, the repression was mainly mediated by OsCOL10. In addition, low expression level of OsCOL10 in nighttime and the fact that oscol10 mutants show no significant alteration in flowering time together suggested that there still have other pathways acting in the repression and these different pathways keep Ghd7 continually and efficiently repress Ehd1 under LD conditions.

Despite our results put more insight into the regulation of Ghd7 to Ehd1.How Ghd7 regulates OsCOL10 and how then OsCOL10 regulates Ehd1, especially the identity of effectors involved remained to be discovered. In addition, it remains to be determined how these COL proteins act distinctly and redundantly to coordinate regulation of flowering.

Disclosure of potential conflicts of interest

No potential conflicts of interest were disclosed.

Funding

This work was supported by the National Natural ScienceFoundation [grant Nos.31401466 and 31371601]; the National Transformation Science and Technology Program[2013ZX08009–003].