Fine-tuning of the setting of critical day length by two casein kinases in rice photoperiodic flowering

Journal of Experimental Botany, Vol. 69, No. 3 pp. 553–565, 2018 doi:10.1093/jxb/erx412 Advance Access publication 10 December 2017 This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details) RESEARCH PAPER Fine-tuning of the setting of critical day length by two casein kinases in rice photoperiodic flowering Yasue Nemoto1,3, Kiyosumi Hori2,† and Takeshi Izawa1,4,* 1 Functional Plant Research Unit, National Institute of Agrobiological Sciences, 2-1-2 Kannondai, 305–8602 Tsukuba, Japan Rice Applied Genomics Research Unit, National Institute of Agrobiological Sciences, 2-1-2 Kannondai, 305–8602 Tsukuba, Japan 3 Institute of Crop Science, National Agriculture and Food Research Organization, Kannondai 2-1-2, 305–8602 Tsukuba, Japan 4 University of Tokyo, Faculty of Agriculture, Laboratory of Plant Genetics and Breeding, Bunkyo-ku, Yayoi 1-1-1, 113–8657 Tokyo, Japan 2 Present address: Institute of Crop Science, National Agriculture and Food Research Organization, Kannondai 2-1-2, 305–8602 Tsukuba, Japan * Correspondence: Received 12 September 2017; Editorial decision 24 October 2017; Accepted 3 November 2017 Editor: Zoe Wilson, University of Nottingham, UK Abstract Many short-day plants have a critical day length that fixes the schedule for flowering time, limiting the range of natural growth habitats (or growth and cultivation areas). Thus, fine-tuning of the critical day-length setting in photoperiodic flowering determines ecological niches within latitudinal clines; however, little is known about the molecular mechanisms controlling the fine-tuning of the critical day-length setting in plants. Previously, we determined that florigen genes are regulated by day length, and identified several key genes involved in setting the critical day length in rice. Using a set of chromosomal segment substitution lines with the genetic background of an elite temperate japonica cultivar, we performed a series of expression analyses of flowering-time genes to identify those responsible for setting the critical day-length in rice. Here, we identified two casein kinase genes, Hd16 and Hd6, which modulate the expression of florigen genes within certain restricted ranges of photoperiod, thereby fine-tuning the critical day length. In addition, we determined that Hd16 functions as an enhancer of the bifunctional action of Hd1 (the Arabidopsis CONSTANS ortholog) in rice. Utilization of the natural variation in Hd16 and Hd6 was only found among temperate japonica cultivars adapted to northern areas. Therefore, this fine-tuning of the setting of the critical day length may contribute to the potential northward expansion of rice cultivation areas. Keywords: Casein kinase, critical day-length, photoperiodic flowering, rice, short-day plants. Introduction Floral transition, the major developmental switch from the vegetative to reproductive phase in plants, is regulated by both endogenous and environmental signals. Photoperiodic flowering, one of the most important biological systems in controlling floral transition, is regulated by light signals and the plant’s endogenous circadian rhythm (Thomas and Vince-Prue, 1997). Rice photoperiodic flowering has been investigated extensively as a model system of short-day (SD) plants. The rice florigen gene Heading date 3a (Hd3a) is regulated according to the recognition of critical day length, and several key genes have been identified that are necessary for setting this day length (Itoh et al., 2010). The critical day length determines whether a plant will flower under certain cultivation environments. For example, © The Author(s) 2017. Published by Oxford University Press on behalf of the Society for Experimental Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. † 554 | Nemoto et al. with or phosphorylate the Hd1 gene product in vitro (Ogiso et al., 2010). It has been reported that Hd16 and Hd6 gene products interacted with the Hd2/OsPRR37 protein in vivo, and phosphorylated different regions of this protein in vitro (Kwon et al., 2015). Hd2 has been detected previously in an F2 population derived from a cross between Nipponbare and Kasalath (Yano et al., 1997; Yamamoto et al., 1998) and isolated as the OsPRR37 gene, an Arabidopsis TOC1 homolog (or a pseudo-response regulator gene) (Koo et al., 2013). Recently, a genetic resource termed ‘chromosomal segment substitution lines’ (CSSLs) has been developed in rice for detection of QTLs with small effects, and is a set of genetic lines that have distinct genomic fragments introgressed from a recurrent cultivar into a background parent cultivar so as to span the entire region of the genome with the introgressed fragments (Ebitani et al., 2005, Keurentjes et al., 2007). An indica cultivar, ‘Nona Bokra’, showed extremely late flowering compared to the japonica cultivar Koshihikari under LD conditions (Uga et al., 2007). CSSLs with Nona Bokra as the donor and Koshihikari as the recipient background cultivar were developed and QTL analysis was performed for flowering time in the field in Tsukuba, Japan (Takai et al., 2007). Although several flowering-time QTLs have been detected and candidate genes have been proposed for a few of them, it has so far been experimentally confirmed that Nona Bokra has a defective allele of one of the florigen genes, RFT1, due to an amino acid substitution (Ogiso-Tanaka et al., 2013). In this study, using further analysis of the Nona Bokra– Koshihikari CSSLs and a set of newly developed nearly isogenic lines (NILs) of the Hd6 and Hd16 genes, we demonstrate that the fine-tuning of critical day length is set by these two CK genes. Mutations in the CK genes has no effect on the rice circadian clocks. Furthermore, we show that Hd6 and Hd16 are involved in the actions of both Hd1 and Ghd7 to control Ehd1, Hd3a, and RFT1.Our results suggest that this fine-tuning of the setting of the critical day length by natural variation in Hd6 and Hd16 may contribute to a potential northward expansion of rice cultivation areas. Materials and methods Plant material and growth conditions We used CSSLs derived from a cross between the Oryza sativa temperate japonica cultivar Koshihikari as the recipient and the indica cultivar Nona Bokra as the donor produced by Takai et al. (2007). A set of four new NILs for Hd16 and Hd6 in the genetic background of Koshihikari were developed, including NILs for Hd16 with the functional allele of Hd6, by crossing ‘Kanto IL5’ by marker-assisted selection (see Supplementary Fig. S1 at JXB online; Hori et al., 2013). Kanto IL5 is one of the isogenic lines derived from crosses between Koshihikari and Kasalath. It has a 170-kb segment of the Kasalath chromosome (...truncated)