Abstract
The domestication of cultivated crops from their wild relatives narrowed down their genetic diversity in a bottleneck effect. Subsequently, the cultivation areas of crops have expanded all over the world into various environmental conditions from the original area along with human migration after domestication. Here, we demonstrated the genetic changes in the adaptation of rice to Hokkaido (41°2–45°3N latitude), Japan, from the tropics of their origin in Asian cultivated rice, Oryza sativa L. Although cultivated rice originated from the tropics, Hokkaido is one of the northern-limits of rice cultivation worldwide. Population genomics focusing on the local populations showed the varieties had genetically distinct classes with limited genetic diversity. In addition, some varieties in the class carried unique genotypes for flowering time, exhibiting extremely early flowering time. Certain mutations in unique genotypes can split off the varieties that are able to grow in Hokkaido. Furthermore, the changes in the genotype for flowering time during rice cultivation in Hokkaido demonstrated novel combinations of genes for flowering time owing to the intensive artificial selection on natural variation and rice breeding programs to achieve stable rice production in Hokkaido.
Similar content being viewed by others
References
Agrama H, Yan W, Jia M, Fjellstrom R, McClung A (2010) Genetic structure associated with diversity and geographic distribution in the USDA rice world collection. Nat Sci 2:247–291
Ando T, Yamamoto T, Shimizu T, Ma XF, Shomura A, Takeuchi Y, Lin SY, Yano M (2008) Genetic dissection and pyramiding of quantitative traits for panicle architecture by using chromosomal segment substitution lines in rice. Theor Appl Genet 116:881–890
Beales J, Turner A, Griffiths S, Snape J, Laurie D (2007) A pseudo-response regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.). Theor Appl Genet 115:721–733
Choi JY, Platts AE, Fuller DQ, Hsing YI, Wing RA, Purugganan MD (2017) The rice paradox: multiple origins but single domestication in Asian rice. Mol Biol Evol 34:969–979
Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127:1309–1321
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
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Faure S, Turner AS, Gruszka D, Christodoulou V, Davis SJ, von Korff M, Laurie DA (2012) Mutation at the circadian clock gene EARLY MATURITY 8 adapts domesticated barley (Hordeum vulgare) to short growing seasons. Proc Natl Acad Sci USA 109:8328–8333
Felsenstein J (1989) PHYlIP-phylogeny inference package (version 3.2). Cladistics 5:164–166
Fujino K, Sekiguchi H (2005a) Mapping of QTLs conferring extremely early heading in rice (Oryza sativa L.). Theor Appl Genet 111:393–398
Fujino K, Sekiguchi H (2005b) 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, Sato T, Kiuchi H, Nonoue Y, Takeuchi Y, Ando T, Lin SY, Yano M (2004) Mapping of quantitative trait loci controlling low-temperature germinability in rice (Oryza sativa L.). Theor Appl Genet 108:794–799
Fujino K, Sekiguchi H, Kiguchi T (2005) Identification of an active transposon in intact rice plants. Mol Gen Genet 273:150–157
Fujino K, Wu J, Sekiguchi H, Ito T, Izawa T, Matsumoto T (2010) Multiple introgression events surrounding the Hd1 flowering-time gene in cultivated rice, Oryza sativa L. Mol Genet Genom 284:137–146
Fujino K, Yamanouchi U, Yano M (2013) Roles of the Hd5 gene controlling heading date for adaptation to the northern limits of rice cultivation. Theor Appl Genet 126:611–618
Fujino K, Obara M, Shimizu T, Koyanagi KO, Ikegaya T (2015a) Genome-wide association mapping focusing on a rice population derived from rice breeding programs in a region. Breed Sci 65:403–410
Fujino K, Obara M, Ikegaya T, Tamura K (2015b) Genetic shift in local rice populations during rice breeding programs in the northern limit of rice cultivation in the world. Theor Appl Genet 128:1739–1746
Fujino K, Nishimura T, Kiuchi H, Hirayama Y, Sato T (2017) Phenotypic changes during 100-year rice breeding programs in Hokkaido. Breed Sci 67:528–534
Fujino K, Yamanouchi U, Nonoue Y, Obara M, Yano M (2019) Switching genetic effects of the flowering time gene Hd1 under LD conditions by Ghd7 and OsPRR37 in rice. Breed Sci. https://doi.org/10.1270/jsbbs.18060
Fuller DQ (2011) Pathways to Asian civilizations: tracing the origins and spread of rice and rice cultures. Rice 4:78–92
Gao H, Jin M, Zheng XM, Chen J, Yuan D, Xin Y, Wang M, Huang D, Zhang Z, Zhou K et al (2014) Days to heading 7, a major quantitative locus determining photoperiod sensitivity and regional adaptation in rice. Proc Natl Acad Sci USA 111:16337–16342
Haudry A, Cenci A, Ravel C, Bataillon T, Brunel D, Poncet C, Hochu I, Poirier S, Santoni S, Glemin S, David J (2007) Grinding up wheat: a massive loss of nucleotide diversity since domestication. Mol Biol Evol 24:1506–1517
Hori K, Nonoue Y, Ono N, Shibaya T, Ebana K, Matsubara K, Ogiso-Tanaka E, Tanabata T, Sugimoto K, Taguchi-Shiobara F et al (2015) Genetic architecture of variation in heading date among Asian rice accessions. BMC Plant Biol 15:115
Hori K, Matsubara K, Yano M (2016) Genetic control of flowering time in rice: integration of Mendelian genetics and genomics. Theor Appl Genet 129:2241–2252
Huang X, Kurata N, Wei X, Wang ZX, Wang A, Zhao Q, Zhao Y, Liu K, Lu H, Li W, Guo Y, Lu Y, Zhou C, Fan D, Weng Q, Zhu C, Huang T, Zhang L, Wang Y, Feng L, Furuumi H, Kubo T, Miyabayashi T, Yuan X, Xu Q, Dong G, Zhan Q, Li C, Fujiyama A, Toyoda A, Lu T, Feng Q, Qian Q, Li J, Han B (2012) A map of rice genome variation reveals the origin of cultivated rice. Nature 490:497–501
Huang C, Sun H, Xu D, Chen Q, Liang Y, Wang X, Xu G, Tian J, Wang C, Li D, Wu L, Yang X, Jin W, Doebley JF, Tian F (2018) ZmCCT9 enhances maize adaptation to higher latitudes. Proc Natl Acad Sci USA 115:E334–E341
Hung HY, Shannon LM, Tian F, Bradbury PJ, Chen C, Flint-Garcia SA, McMullen MD, Ware D, Buckler ES, Doebley JF, Holland JB (2012) ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize. Proc Natl Acad Sci USA109:E1913–E1921
Hyten DL, Song Q, Zhu Y, Choi IY, Nelson RL, Costa JM, Specht JE, Shoemaker RC, Cregan PB (2006) Impacts of genetic bottlenecks on soybean genome diversity. Proc Natl Acad Sci USA 103:16666–16671
Khush GS (1997) Origin, dispersal, cultivation and variation of rice. Plant Mol Biol 35:25–34
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
Koo BH, Yoo SC, Park JW, Kwon CT, Lee BD, An G, Zhang Z, Li J, Li Z, Paek NC (2013) Natural variation in OsPRR37 regulates heading date and contributes to rice cultivation at a wide range of latitudes. Mol Plant 6:1877–1888
Li X, Qian Q, Fu Z, Wang Y, Xiong G, Zeng D, Wang X, Liu X, Teng S, Hiroshi F, Yuan M, Luo D, Han B, Li J (2003) Control of tillering in rice. Nature 422:618–621
Liang WH, Shang F, Lin QT, Lou C, Zhang J (2014) Tillering and panicle branching genes in rice. Gene 537:1–5
Lu JJ, Chang TT (1980) Rice in its temporal and spatial perspectives. In: Luh BS (ed) Rice: production and utilization. AVI Publishing Co., Inc., Westport, pp 1–74
Murakami M, Tago Y, Yamashino T, Mizuno T (2007) Comparative overviews of clock-associated genes of Arabidopsis thaliana and Oryza sativa. Plant Cell Physiol 48:110–121
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acid Res 8:4321–4325
Nakamichi N, Kita M, Ito S, Yamashino T, Mizuno T (2005) PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana. Plant Cell Physiol 46:686–698
Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323
Nonoue Y, Fujino K, Hirayama Y, Yamanouchi U, Lin SY, 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
Pitchard JK, Stephens M, Donnely P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Purugganan MD, Fuller DQ (2009) The nature of selection during plant domestication. Nature 457:843–848
Ross-Ibarra J, Morrell PL, Gaut BS (2007) Plant domestication, a unique opportunity to identify the genetic basis of adaptation. Proc Natl Acad Sci USA 104(Suppl 1):8641–8648
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
Shinada H, Yamamoto T, Yamamoto E, Hori K, Yonemaru J, Matsuba S, Fujino K (2014) Historical changes in population structure during rice breeding programs in the northern limits of rice cultivation. Theor Appl Genet 127:995–1004
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
Tenaillon MI, U’Ren J, Tenaillon O, Gaut BS (2004) Selection versus demography: a multilocus investigation of the domestication process in maize. Mol Biol Evol 21:1214–1225
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
Tsuji H, Tachibana C, Tamaki S, Taoka K, Kyozuka J, Shimamoto K (2015) Hd3a promotes lateral branching in rice. Plant J 82:256–266
Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–1034
Wang Y, Li J (2008) Molecular basis of plant architecture. Ann Rev Plant Biol 59:253–279
Wang L, Lu Q, Wen X, Lu C (2015a) Enhanced sucrose loading improves rice yield by increasing grain size. Plant Physiol 169:2848–2862
Wang L, Sun S, Jin J, Fu D, Yang X, Weng X, Xu C, Li X, Xiao J, Zhang Q (2015b) Coordinated regulation of vegetative and reproductive branching in rice. Proc Natl Acad Sci USA 112:15504–15509
Wei X, Xu J, Guo H, Jiang L, Chen S, Yu C, Zhou Z, Hu P, Zhai H, Wan J (2010) DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol 153:1747–1758
Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X, Zhang Q (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40:761–767
Yang J, Zhao X, Cheng K, Du H, Ouyang Y, Chen J, Qiu S, Huang J, Jiang Y, Jiang L, Ding J, Wang J, Xu C, Li X, Zhang Q (2012) A killer-protector system regulates both hybrid sterility and segregation distortion in rice. Science 337:1336–1340
Yang S, Murphy RL, Morishige DT, Klein PE, Rooney WL, Mullet JE (2014) Sorghum phytochrome B inhibits flowering in long days by activating expression of SbPRR37 and SbGHD, repressors of SbEHD1, SbCN8 and SbCN12. PLoS One 9:e105352
Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, Sasaki T (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12:2473–2484
Yokoo M, Kikuchi F (1977) Multiple allelism of the locus controlling heading time of rice, detecting using close linkage with blast-resistance. Jpn J Breed 21:123–130
Yokoo M, Kikuchi F, Nakane A, Fujimaki H (1980) Genetical analysis of heading time by aid of close linkage with blast, Pyricularia oryzae, resistance in rice. Bull Natl Inst Agric Sci Ser D 31:95–126
Zakhrabekova S, Gough SP, Braumann I, Muller AH, Lundqvist J, Ahmann K, Dockter C, Matyszczak I, Kurowska M, Druka A, Waugh R, Graner A, Stein N, Steuernagel B, Lundqvist U, Hansson M (2012) Induced mutations in circadian clock regulator Mat-a facilitated short-season adaptation and range extension in cultivated barley. Proc Natl Acad Sci USA 109:4326–4331
Acknowledgements
This work was supported in part by a grant from the Ministry of Agriculture, Forestry and Fisheries of Japan (Science and Technology Research Promotion Program for Agriculture, Forestry, Fisheries and Food Industry) (to KF) and JSPS KAKENHI Grant number 25450015 (to KF).
Funding
This work was supported in part by a grant from the Ministry of Agriculture, Forestry and Fisheries of Japan (Science and Technology Research Promotion Program for Agriculture, Forestry, Fisheries and Food Industry) (to KF) and JSPS KAKENHI Grant number 25450015 (to KF).
Author information
Authors and Affiliations
Contributions
Conceived and designed the experiments and wrote the manuscript: KF. Performed the experiments, analyzed the data, and approved the final manuscript: TI, MO, KF.
Corresponding author
Ethics declarations
Conflict of interest
All author declares that he/she has no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Communicated by Bing Yang.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Fujino, K., Obara, M. & Ikegaya, T. Establishment of adaptability to the northern-limit of rice production. Mol Genet Genomics 294, 729–737 (2019). https://doi.org/10.1007/s00438-019-01542-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-019-01542-2