Abstract
During the diversification of cultivated rice after domestication, rice was grown in diverse geographic regions using genetic variations attributed to the combination of alleles in loci for adaptability to various environmental conditions. To elucidate the key gene for adaptation in rice cultivars to the northern limit of rice cultivation, we conducted genetic analyses of heading date using extremely early-heading cultivars. The Hd5 gene controlling heading date (flowering time) generated variations in heading date among cultivars adapted to Hokkaido, where is the northernmost region of Japan and one of the northern limits of rice cultivation in the world. The association of the Hd5 genotype with heading date and genetical analysis clearly showed that the loss-of-function Hd5 has an important role in exhibiting earlier heading among a local population in Hokkaido. Distinct distribution of the loss-of-function Hd5 revealed that this mutation event of the 19-bp deletion occurred in a local landrace Bouzu and that this mutation may have been selected as an early-heading variety in rice breeding programs in Hokkaido in the early 1900s. The loss-of-function Hd5 was then introduced into the rice variety Fanny from France and contributed to its extremely early heading under the presence of functional Ghd7. These results demonstrated that Hd5 plays roles not only in generating early heading in variations of heading date among a local population in Hokkaido, but also in extremely early heading for adaptation to northern limits of rice cultivation.
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References
Alonso-Blanco C, Aarts MG, Bentsink L, Keurentjes JJ, Reymond M et al (2009) What has natural variation taught us about plant development, physiology, and adaptation? Plant Cell 21:1877–1896
Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T et al (2004) Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev 18:926–936
Ebana K, Kojima Y, Fukuoka S, Nagamine T, Kawase M (2008) Development of mini core collection of Japanese rice landrace. Breed Sci 58:281–291
Ebana K, Shibaya T, Wu J, Matsubara K, Kanamori H et al (2011) Uncovering of major genetic factors generating naturally occurring variation in heading date among Asian rice cultivars. Theor Appl Genet 122:1199–1210
Endo-Higashi N, Izawa T (2011) Flowering time genes Heading date 1 and Early heading date 1 together control panicle development in rice. Plant Cell Physiol 52:1083–1094
Fujino K (2003) Photoperiod sensitivity gene controlling heading date in rice cultivars in the northernmost region of Japan. Euphytica 131:97–103
Fujino K, Iwata N (2011) Identification of QTLs controlling heading date on the short arm of chromosome 3 in rice (Oryza sativa L.). Breed Sci 61:294–300
Fujino K, Sekiguchi H (2005a) Identification of QTLs conferring genetic variation for heading date among rice varieties at the northern-limit of rice cultivation. Breed Sci 55:141–146
Fujino K, Sekiguchi H (2005b) Mapping of QTLs conferring extremely early heading in rice (Oryza sativa L.). Theor Appl Genet 111:393–398
Fujino K, Sekiguchi H (2008) Mapping of quantitative trait loci controlling heading date among rice cultivars in the northernmost region of Japan. Breed Sci 58:367–373
Fujino K, Sekiguchi H, Sato T, Kiuchi H, Nonoue Y et al (2004) Mapping of quantitative trait loci controlling low-temperature germinability in rice (Oryza sativa L.). Theor Appl Genet 108:794–799
Fuse T, Sasaki T, Yano M (2001) Ti-plasmid vectors useful for functional analysis of rice genes. Plant Biotechnol 18:219–222
Gu XY, Foley ME (2007) Epistatic interactions of three loci regulate flowering time under short and long daylengths in a backcross population of rice. Theor Appl Genet 114:745–754
Izawa T (2007a) Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice. J Exp Bot 58:3091–3097
Izawa T (2007b) Daylength measurements by rice plants in photoperiodic short-day flowering. Int Rev Cytol 256:191–222
Kojima Y, Ebana K, Fukuoka S, Nagamine T, Kawase M (2005) Development of an RFLP-based rice diversity research set of germplasm. Breed Sci 55:431–440
Lin SY, Sasaki T, Yano M (1998) Mapping quantitative trait loci controlling seed dormancy and heading date in rice, Oryza sativa L., using backcross inbred lines. Theor Appl Genet 96:997–1003
Lin HX, Ashikari M, Yamanouchi U, Sasaki T, Yano M (2002) Identification and characterization of a quantitative trait locus, Hd9, controlling heading date in rice. Breed Sci 52:35–41
Lin HX, Liang Z-W, Sasaki T, Yano M (2003) Fine mapping and characterization of quantitative trait loci Hd4 and Hd5 controlling heading date in rice. Breed Sci 53:51–59
Miura K, Ashikari M, Matsuoka M (2011) The role of QTLs in the breeding of high-yielding rice. Trends Plant Sci 16:319–326
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucl Acid Res 8:4321–4325
Nagasaki H, Ebana K, Shibaya T, Yonemaru J, Yano M (2010) Core single-nucleotide polymorphisms—a tool for genetic analysis of the Japanese rice population. Breed Sci 60:648–655
Nonoue Y, Fujino K, Hirayama Y, Yamanouchi U, Lin S, Yano M (2008) Detection of quantitative trait loci controlling extremely early heading in rice. Theor Appl Genet 116:715–722
Okumoto Y, Ichitani K, Inoue H, Tanisaka T (1996) Photoperiod insensitivity gene essential to the varieties grown in the northern limit region of paddy rice (Oryza sativa L.) cultivation. Euphytica 92:63–66
Shibaya T, Nonoue Y, Ono N, Yamanouchi U, Hori K, Yano M (2011) Genetic interactions involved in the inhibition of heading by heading date QTL, Hd2 in rice under long-day conditions. Theor Appl Genet 123:1133–1143
Tanisaka T, Inoue H, Uozu S, Yamagata H (1992) Basic vegetative growth and photoperiod sensitivity of heading-time mutants induced in rice. Jpn J Breed 42:657–668
Toki S, Hara N, Ono K, Onodera H, Tagiri A, Oka S et al (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J 47:969–976
Tsuji H, Taoka K, Shimamoto K (2011) Regulation of flowering in rice: two florigen genes, a complex gene network, and natural variation. Curr Opin Plant Biol 14:45–52
Uga Y, Nonoue Y, Liang ZW, Lin HX, Yamamoto S, Yamanouchi U, Yano M (2007) Accumulation of additive effects generates a strong photoperiod sensitivity in the extremely late-heading rice cultivar ‘Nona Bokra’. Theor Appl Genet 114:1457–1466
Wei X, Xu J, Guo H, Jiang L, Chen S et al (2010) DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol 153:1747–1758
Xue WY, Xing YZ, Weng XY, Zhao Y, Tang WJ et al (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40:761–767
Yamamoto T, Lin HX, Sasaki T, Yano M (2000) Identification of heading date quantitative trait locus Hd6 and characterization of its epistatic interactions with Hd2 in rice. Genetics 154:885–891
Yamamoto T, Yonemaru J, Yano M (2009) Towards the understanding of complex traits in rice: substantially or superficially? DNA Res 16:141–154
Yan WH, Wang P, Chen HX, Zhou HJ, Li QP et al (2011) A Major QTL, Ghd8, plays pleiotropic roles in regulating grain productivity, plant height, and heading date in rice. Mol Plant 4:319–330
Yano M (2001) Genetic and Molecular dissection of naturally occurring variation. Curr Opin Plant Biol 4:130–135
Yano M, Harushima Y, Nagamura Y, Kurata N, Minobe Y, Sasaki T (1997) Identification of quantitative trait loci controlling heading date in rice using a high-density linkage map. Theor Appl Genet 95:1025–1032
Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L et al (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12:2473–2483
Yonemaru J, Yamamoto T, Ebana K, Yamamoto E, Nagasaki H et al (2012) Genome-wide haplotype changes produced by artificial selection during modern rice breeding in Japan. PLoS ONE 7:e32982
Acknowledgments
We are grateful to Kazuo Ise (Japan International Research Center for Agricultural Sciences, Japan) and Professor Dai Luyuan (Yunnan Academy of Agricultural Sciences, China) for information on the pedigree of rice varieties from China.
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Communicated by L. Xiong.
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Fujino, K., Yamanouchi, U. & Yano, M. Roles of the Hd5 gene controlling heading date for adaptation to the northern limits of rice cultivation. Theor Appl Genet 126, 611–618 (2013). https://doi.org/10.1007/s00122-012-2005-5
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DOI: https://doi.org/10.1007/s00122-012-2005-5