Skip to main content
Log in

Introgression of the chromosomal region with the Pi-cd locus from Oryza meridionalis into O. sativa L. during rice domestication

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

The genotype of the Pi-cd locus found in blast-resistant rice variety Kitakurin, which is a cultivated rice from Japan belonging to Oryza sativa japonica, is identical to that of its wild relative O. meridionalis.

Abstract

Crop domestication from wild relatives to cultivated species has encompassed significant phenotypic changes. However, little is known about the genetic changes involved in domestication. Here, we surveyed the origin of the Pi-cd locus across Oryza species with AA genomes by comparison with the genome sequences of Hoshinoyume (HS), which does not carry the Pi-cd blast resistance gene, and Kitakurin (KK), which carries the Pi-cd blast resistance gene. We found that variety-specific transposons were enriched at the Pi-cd locus. The genotype of the Pi-cd locus characterized by transposons in HS and KK was specific to each Oryza species with the AA genome. The Kitaake (KT) genotype at the Pi-cd locus found in KK was identical only to that of O. meridionalis and distributed only in subgroups of japonica in the World Rice Collection and tropical japonica in the Japanese Rice Collection, whereas it was not present in O. rufipogon accessions. The distinct distributions of genotypes of the Pi-cd locus clearly demonstrated that the Pi-cd locus was introgressed from O. meridionalis into O. sativa, specific to tropical japonica.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

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

    Google Scholar 

  • Ali ML, Sanchez LP, Yu S, Lorieux M, Eizenga CG (2010) Chromosome segment substitution lines: a powerful tool for the introgression of valuable genes from Oryza wild species into cultivated rice (O. sativa). Rice 3:218–234

    Article  Google Scholar 

  • Ammiraju JS, Lu F, Sanyal A, Yu Y, Song X, Jiang N, Pontaroli AC, Rambo T, Currie J, Collura K, Talag J, Fan C, Goicoechea JL, Zuccolo A, Chen J, Bennetzen JL, Chen M, Jackson S, Wing RA (2008) Dynamic evolution of Oryza genomes is revealed by comparative genomic analysis of a genus-wide vertical data set. Plant Cell 20:3191–3209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arbelaez JD, Moreno LT, Singh N, Tung CW, Maron LG, Ospina Y, Martinez CP, Grenier C, Lorieux M, McCouch S (2015) Development and GBS-genotyping of introgression lines (ILs) using two wild species of rice, O. meridionalis and O. rufipogon, in a common recurrent parent, O. sativa cv. Curinga. Mol Breed 35:81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Banaticla-Hilario NMC, McNally LK, van den Berg GR, Hamilton NRS (2013) Crossability patterns within and among Oryza series Sativae species from Asia and Australia. Genet Res Crop Evol 60:1573–5109

    Article  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Civáň P, Craig H, Cox CJ, Brown TA (2015) Three geographically separate domestications of Asian rice. Nat Plants 1:15164

    Article  PubMed  PubMed Central  Google Scholar 

  • Deng Y, Zhai K, Xie Z, Yang D, Zhu X, Liu J, Wang X, Qin P, Yang Y, Zhang G, Li Q, Zhang J, Wu S, Milazzo J, Mao B, Wang E, Xie H, Tharreau D, He Z (2017) Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. Science 355:962–965

    Article  CAS  PubMed  Google Scholar 

  • Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127:1309–1321

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Fujino K, Sekiguchi H, Kiguchi T (2005) Identification of an active transposon in intact rice plants. Mol Genet Genomics 273:150–157

    Article  CAS  PubMed  Google Scholar 

  • 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 Genomics 284:137–146

    Article  CAS  PubMed  Google Scholar 

  • Fujino K, Obara M, Ikegaya T, Tamura K (2015) 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Fujino K, Hirayama Y, Obara M, Ikegaya T (2018) Colocalization of QTLs for hull-cracked rice and grain size in elite rice varieties in Japan. Breed Sci 68:449–454

    Article  PubMed  PubMed Central  Google Scholar 

  • Fukuoka S, Okuno K (2001) QTL analysis and mapping of pi21, a recessive gene for field resistance to rice blast in Japanese upland rice. Theor Appl Genet 103:185–190

    Article  CAS  Google Scholar 

  • Fukuoka S, Saka N, Mizukami Y, Koga H, Yamanouchi U, Yoshioka Y, Hayashi N, Ebana K, Mizobuchi R, Yano M (2015) Gene pyramiding enhances durable blast disease resistance in rice. Sci Rep 5:7773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuller DQ (2011) Pathways to Asian civilizations: tracing the origins and spread of rice and rice cultures. Rice 4:78–92

    Article  Google Scholar 

  • Garris AJ, Tai TH, Coburn J, Kresovich S, McCouch S (2005) Genetic structure and diversity in Oryza sativa L. Genetics 169:1631–1638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harlan JR, de Wet JMJ, Price EG (1973) Comparative evolution of cereals. Evolution 27:311–325

    Article  PubMed  Google Scholar 

  • He N, Wu R, Pan X, Peng L, Sun K, Zou T, Zhu H, Zeng R, Liu Z, Liu G, Wang S, Zhang G, Fu X (2017) Development and trait evaluation of chromosome single-segment substitution lines of O. meridionalis in the background of O. sativa. Euphytica 213:281

    Article  CAS  Google Scholar 

  • Hua L, Wang DR, Tan L, Fu Y, Liu F, Xiao L, Zhu Z, Fu Q, Sun X, Gu P, Cai H, McCouch SR, Sun C (2015) LABA1, a domestication gene associated with long, barbed awns in wild rice. Plant Cell 27:1875–1888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacquemin J, Ammiraju JS, Haberer G, Billheimer DD, Yu Y, Liu LC, Rivera LF, Mayer K, Chen M, Wing RA (2014) Fifteen million years of evolution in the Oryza genus shows extensive gene family expansion. Mol Plant 7:642–656

    Article  CAS  PubMed  Google Scholar 

  • Jin J, Hua L, Zhu Z, Tan L, Zhao X, Zhang W, Liu F, Fu Y, Cai H, Sun X, Gu P, Xie D, Sun C (2016) GAD1 encodes a secreted peptide that regulates grain number, grain length, and awn development in rice domestication. Plant Cell 28:2453–2463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Juliano BA, Naredo BME, Lu BR, Jackson TM (2005) Genetic differentiation in Oryza meridionalis Ng based on molecular and crossability analyses. Genet Res Crop Evol 52:1573–5109

    Article  CAS  Google Scholar 

  • Khush GS (1997) Origin, dispersal, cultivation and variation of rice. Plant Mol Biol 35:25–34

    Article  CAS  PubMed  Google Scholar 

  • Koide Y, Ogino A, Yoshikawa T, Kitashima Y, Saito N, Kanaoka Y, Onishi K, Yoshitake Y, Tsukiyama T, Saito H, Teraishi M, Yamagata Y, Uemura A, Takagi H, Hayashi Y, Abe T, Fukuta Y, Okumoto Y, Kanazawa A (2018) Lineage-specific gene acquisition or loss is involved in interspecific hybrid sterility in rice. Proc Natl Acad Sci U S A 115:E1955–E1962

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Konishi S, Ebana K, Izawa T (2008) Inference of the japonica rice domestication process from the distribution of six functional nucleotide polymorphisms of domestication-related genes in various landraces and modern cultivars. Plant Cell Physiol 49:1283–1293

    Article  CAS  PubMed  Google Scholar 

  • Kovach MJ, McCouch SR (2008) Leveraging natural diversity: back through the bottleneck. Curr Opin Plant Biol 11:193–200

    Article  CAS  PubMed  Google Scholar 

  • Krishnan SG, Waters DL, Henry RJ (2014) Australian wild rice reveals pre-domestication origin of polymorphism deserts in rice genome. PLoS ONE 9:e98843

    Article  CAS  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAM tools. Bioinformatics 25:2078–2079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Londo JP, Chiang YC, Hung KH, Chiang TY, Schaal BA (2006) Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa. Proc Natl Acad Sci U S A 103:9578–9583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu JJ, Chang TT (1980) Rice in its temporal and spatial perspective. In: Luh BS (ed) Rice production and utilization. AVI Publishing Co, Westport, pp 1–74

    Google Scholar 

  • Lu L, Chen J, Robb SMC, Okumoto Y, Stajich JE, Wessler SR (2017) Tracking the genome-wide outcomes of a transposable element burst over decades of amplification. Proc Natl Acad Sci U S A 114:E10550–E10559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCouch SR, Sweeney M, Li J, Jiang H, Thomson M, Septiningsih E, Edwards J, Moncada P, Xiao J, Garris A, Tai T, Martinez C, Tohme J, Sugiono M, McClung A, Yuan LP, Ahn SN (2007) Through the genetic bottleneck: O. rufipogon as a source of trait-enhancing alleles for O. sativa. Euphytica 154:317–339

    Article  CAS  Google Scholar 

  • McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyamoto M, Hirasawa H (2003) Relationship between RFLP loci with different alleles on chromosome 4 and the levels of blast field resistance in Japanese upland rice varieties. Breed Sci 53:1–5

    Article  CAS  Google Scholar 

  • Miyamoto M, Yano M, Hirasawa H (2001) Mapping of quantitative trait loci conferring blast field resistance in the Japanese upland rice variety Kahei. Breed Sci 51:257–261

    Article  CAS  Google Scholar 

  • Mizuta Y, Harushima Y, Kurata N (2010) Rice pollen hybrid incompatibility caused by reciprocal gene loss of duplicated genes. Proc Natl Acad Sci U S A 107:20417–20422

    Article  PubMed  PubMed Central  Google Scholar 

  • Moner AM, Furtado A, Chivers I, Fox G, Crayn D, Henry RJ (2018) Diversity and evolution of rice progenitors in Australia. Ecol Evol 8:4360–4366

    Article  PubMed  PubMed Central  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acid Res 8:4321–4325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naredo BME, Juliano BA, Lu BR, Jackson TM (1997) Hybridization of AA genome rice species from Asia and Australia I. Crosses and development of hybrids. Genet Res Crop Evol 44:1573–5109

    Article  Google Scholar 

  • Osés-Ruiz M, Sakulkoo W, Littlejohn GR, Martin-Urdiroz M, Talbot NJ (2017) Two independent S-phase checkpoints regulate appressorium-mediated plant infection by the rice blast fungus Magnaporthe oryzae. Proc Natl Acad Sci U S A 114:E237–E244

    Article  CAS  PubMed  Google Scholar 

  • Purugganan MD, Fuller DQ (2009) The nature of selection during plant domestication. Nature 457:843–848

    Article  CAS  PubMed  Google Scholar 

  • Ross-Ibarra J, Morrell PL, Gaut B (2007) Plant domestication, a unique opportunity to identify the genetic basis of adaptation. Proc Natl Acad Sci U S A 104(Suppl 1):8641–8648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    CAS  PubMed  Google Scholar 

  • Scafaro AP, Haynes PA, Atwell BJ (2010) Physiological and molecular changes in Oryza meridionalis Ng., a heat-tolerant species of wild rice. J Exp Bot 61:191–202

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Shinada H, Yamamoto T, Sato H, Yamamoto E, Hori K, Yonemaru J, Sato T, Fujino K (2015) Quantitative trait loci for rice blast resistance detected in a local rice breeding population by genome-wide association mapping. Breed Sci 65:388–395

    Article  PubMed  PubMed Central  Google Scholar 

  • Stein JC, Yu Y, Copetti D, Zwickl DJ, Zhang L, Zhang C, Chougule K, Gao D, Iwata A, Goicoechea JL, Wei S, Wang J, Liao Y, Wang M, Jacquemin J, Becker C, Kudrna D, Zhang J, Londono CEM, Song X, Lee S, Sanchez P, Zuccolo A, Ammiraju JSS, Talag J, Danowitz A, Rivera LF, Gschwend AR, Noutsos C, Wu CC, Kao SM, Zeng JW, Wei FJ, Zhao Q, Feng Q, El Baidouri M, Carpentier MC, Lasserre E, Cooke R, Rosa Farias DD, da Maia LC, Dos Santos RS, Nyberg KG, McNally KL, Mauleon R, Alexandrov N, Schmutz J, Flowers D, Fan C, Weigel D, Jena KK, Wicker T, Chen M, Han B, Henry R, Hsing YC, Kurata N, de Oliveira AC, Panaud O, Jackson SA, Machado CA, Sanderson MJ, Long M, Ware D, Wing RA (2018) Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza. Nat Genet 50:285–296

    Article  CAS  PubMed  Google Scholar 

  • Valent B, Khang CH (2010) Recent advances in rice blast effector research. Curr Opin Plant Biol 13:434–441

    Article  CAS  PubMed  Google Scholar 

  • Vaughan DA, Morishima H, Kadowaki K (2003) Diversity in the Oryza genus. Curr Opin Plant Biol 6:139–146

    Article  CAS  PubMed  Google Scholar 

  • Wang GL, Valent B (2017) Durable resistance to rice blast. Science 355:906–907

    Article  CAS  PubMed  Google Scholar 

  • Wang GW, He YQ, Xu CG, Zhang Q (2005) Identification and confirmation of three neutral alleles conferring wide compatibility in inter-subspecific hybrids of rice (Oryza sativa L.) using near-isogenic lines. Theor Appl Genet 111:702–710

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Basten CJ, Zeng ZB (2012) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh

  • Wing RA, Ammiraju JS, Luo M, Kim H, Yu Y, Kudrna D, Goicoechea JL, Wang W, Nelson W, Rao K, Brar D, Mackill DJ, Han B, Soderlund C, Stein L, San Miguel P, Jackson S (2005) The oryza map alignment project: the golden path to unlocking the genetic potential of wild rice species. Plant Mol Biol 59:53–62

    Article  CAS  PubMed  Google Scholar 

  • Yang C-C, Kawahara Y, Mizuno H, Wu J, Matsumoto T, Itoh T (2012a) Independent domestication of Asian rice followed by gene flow from japonica to indica. Mol Biol Evol 29:1471–1479

    Article  CAS  PubMed  Google Scholar 

  • 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 (2012b) A killer-protector system regulates both hybrid sterility and segregation distortion in rice. Science 337:1336–1340

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura A, Nagayama H, Kurakazu T, Sanchez PL, Doi K, Yamagata Y, Yasui H (2010) Introgression lines of rice (Oryza sativa L.) carrying a donor genome from the wild species, O. glumaepatula Steud. and O. meridionalis Ng. Breed Sci 60:597–603

    Article  Google Scholar 

  • Zhang QJ, Gao LZ (2017) Rapid and recent evolution of LTR retrotransposons drives rice genome evolution during the speciation of AA-genome Oryza species. G3 (Bethesda) 7:1875–1885

    Article  CAS  Google Scholar 

  • Zhang QJ, Zhu T, Xia EH, Shi C, Liu YL, Zhang Y, Liu Y, Jiang WK, Zhao YJ, Mao SY, Zhang LP, Huang H, Jiao JY, Xu PZ, Yao QY, Zeng FC, Yang LL, Gao J, Tao DY, Wang YJ, Bennetzen JL, Gao LZ (2014) Rapid diversification of five Oryza AA genomes associated with rice adaptation. Proc Natl Acad Sci U S A 111:E4954–E4962

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Yang S, Wang J, Jia Y, Huang J, Tan S, Zhong Y, Wang L, Gu L, Chen JQ, Pan Q, Bergelson J, Tian D (2015) A genome-wide survey reveals abundant rice blast R genes in resistant cultivars. Plant J 84:20–28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu T, Xu PZ, Liu JP, Peng S, Mo XC, Gao LZ (2014) Phylogenetic relationships and genome divergence among the AA- genome species of the genus Oryza as revealed by 53 nuclear genes and 16 intergenic regions. Mol Phylogenet Evol 70:348–361

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The wild rice accessions used in this study were supplied by the National Institute of Genetics supported by the National Bioresource Project (NBRP), AMED, Japan. 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).

Author information

Authors and Affiliations

Authors

Contributions

KF conceived and designed the experiments and wrote the manuscript. KF, YH, MO, TI performed the experiments and analyzed the data. KF, YH, MO, TI approved the final manuscript.

Corresponding author

Correspondence to Kenji Fujino.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Lizhong Xiong.

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.

Supplementary material 1 (PPTX 67 kb)

Supplementary material 2 (XLSX 37 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fujino, K., Hirayama, Y., Obara, M. et al. Introgression of the chromosomal region with the Pi-cd locus from Oryza meridionalis into O. sativa L. during rice domestication. Theor Appl Genet 132, 1981–1990 (2019). https://doi.org/10.1007/s00122-019-03332-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-019-03332-1

Navigation