Molecular Genetics and Genomics

, Volume 283, Issue 4, pp 305–315 | Cite as

Gain of deleterious function causes an autoimmune response and Bateson–Dobzhansky–Muller incompatibility in rice

  • Eiji Yamamoto
  • Tomonori Takashi
  • Yoichi Morinaka
  • Shaoyang Lin
  • Jianzhong Wu
  • Takashi Matsumoto
  • Hidemi Kitano
  • Makoto Matsuoka
  • Motoyuki Ashikari
Original Paper

Abstract

Reproductive isolation plays an important role in speciation as it restricts gene flow and accelerates genetic divergence between formerly interbreeding population. In rice, hybrid breakdown is a common reproductive isolation observed in both intra and inter-specific crosses. It is a type of post-zygotic reproductive isolation in which sterility and weakness are manifested in the F2 and later generations. In this study, the physiological and molecular basis of hybrid breakdown caused by two recessive genes, hbd2 and hbd3, in a cross between japonica variety, Koshihikari, and indica variety, Habataki, were investigated. Fine mapping of hbd2 resulted in the identification of the causal gene as casein kinase I (CKI1). Further analysis revealed that hbd2-CKI1 allele gains its deleterious function that causes the weakness phenotype by a change of one amino acid. As for the other gene, hbd3 was mapped to the NBS-LRR gene cluster region. It is the most common class of R-gene that triggers the immune signal in response to pathogen attack. Expression analysis of pathogen response marker genes suggested that weakness phenotype in this hybrid breakdown can be attributed to an autoimmune response. So far, this is the first evidence linking autoimmune response to post-zygotic isolation in rice. This finding provides a new insight in understanding the molecular and evolutionary mechanisms establishing post-zygotic isolation in plants.

Keywords

Rice Reproductive isolation BDM incompatibility Autoimmune response Weakness phenotype 

Notes

Acknowledgments

We thank Mr. Naoya Watanabe and Dr. Yasuhiro Kondoh (Honda Research Institute, Japan) for helpful suggestions regarding the experimental design and Ikuko Aichi and Midori Ito for technical assistance. This study was supported by a Grant-in-Aid from the Ministry of Education, Culture, Sports, Science, and Technology, Japan (19688002 to M.A.) and research fellowships from the Japan Society for the Promotion of Science for Young Scientists (to E.Y.).

Supplementary material

438_2010_514_MOESM1_ESM.xls (32 kb)
Supplementary Table 1 (XLS 32 kb)
438_2010_514_MOESM2_ESM.xls (31 kb)
Supplementary Table 2 (XLS 31 kb)

References

  1. Agrawal GK, Jwa NS, Rakwal R (2000a) A novel rice (Oryza sativa L.) acidic PR1 gene highly responsive to cut, phytohormones, and protein phosphatase inhibitors. Biochem Biophys Res Commun 274(1):157–165CrossRefPubMedGoogle Scholar
  2. Agrawal GK, Rakwal R, Jwa NS (2000b) Rice (Oryza sativa L.) OsPR1b gene is phytohormonally regulated in close interaction with light signals. Biochem Biophys Res Commun 278(2):290–298CrossRefPubMedGoogle Scholar
  3. Agrawal GK, Jwa NS, Han KS, Agrawal VP, Rakwal R (2003) Isolation of a novel rice PR4 type gene whose mRNA expression is modulated by blast pathogen attack and signaling components. Plant Physiol Biochem 41(1):81–90CrossRefGoogle Scholar
  4. Alcázar R, García AV, Parker JE, Reymond M (2009) Incremental steps toward incompatibility revealed by Arabidopsis epistatic interactions modulating salicylic acid pathway activation. Proc Natl Acad Sci USA 106(1):334–339CrossRefPubMedGoogle Scholar
  5. Amemiya A, Akamine H (1963) Biochemical genetic studies on the root growth inhibiting complementary lethal genes on rice plant. Bull Nat Inst Agric Sci Ser D 10:139–226Google Scholar
  6. Axtell MJ, Staskawicz BJ (2003) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112(3):369–377CrossRefPubMedGoogle Scholar
  7. Belkhadir Y, Nimchuk Z, Hubert DA, Mackey D, Dangl JL (2004) Arabidopsis RIN4 negatively regulates disease resistance mediated by RPS2 and RPM1 downstream or independent of the NDR1 signal modulator and is not required for the virulence functions of bacterial type III effectors AvrRpt2 or AvrRpm1. Plant Cell 16(10):2822–2835CrossRefPubMedGoogle Scholar
  8. Bergelson J, Kreitman M, Stahl EA, Tian D (2001) Evolutionary dynamics of plant R-genes. Science 292(5525):2281–2285CrossRefPubMedGoogle Scholar
  9. Bikard D, Patel D, Le Metté C, Giorgi V, Camilleri C, Bennett MJ, Loudet O (2009) Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana. Science 323(5914):623–626CrossRefPubMedGoogle Scholar
  10. Bomblies K, Weigel D (2007) Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat Rev Genet 8(5):382–393CrossRefPubMedGoogle Scholar
  11. Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, Dangl JL, Weigel D (2007) Autoimmune response as a mechanism for a Dobzhansky–Muller-type incompatibility syndrome in plants. PLoS Biol 5(9):e236CrossRefPubMedGoogle Scholar
  12. Chen J, Ding J, Ouyang Y, Du H, Yang J, Cheng K, Zhao J, Qiu S, Zhang X, Yao J, Liu K, Wang L, Xu C, Li X, Xue Y, Xia M, Ji Q, Lu J, Xu M, Zhang Q (2008) A triallelic system of S5 is a major regulator of the reproductive barrier and compatibility of indica-japonica hybrids in rice. Proc Natl Acad Sci USA 105(32):11436–11441CrossRefPubMedGoogle Scholar
  13. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host–microbe interactions: shaping the evolution of the plant immune response. Cell 124(4):803–814CrossRefPubMedGoogle Scholar
  14. Coaker G, Falick A, Staskawicz B (2005) Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin. Science 308(5721):548–550CrossRefPubMedGoogle Scholar
  15. Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, SunderlandGoogle Scholar
  16. DeYoung BJ, Innes RW (2006) Plant NBS-LRR proteins in pathogen sensing and host defense. Nat Immunol 7(12):1243–1249CrossRefPubMedGoogle Scholar
  17. Dobzhansky T (1937) Genetics and the origin of species. Columbia University Press, New YorkGoogle Scholar
  18. Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang CI, Ayliffe MA, Kobe B, Ellis JG (2003) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci USA 103(23):8888–8893CrossRefGoogle Scholar
  19. Fukuoka S, Namai H, Okuno K (1998) RFLP mapping of the genes controlling hybrid breakdown in rice. Theor Appl Genet 97:446–449CrossRefGoogle Scholar
  20. Fukuoka S, Newingham MCV, Ishtaq M, Nagamine T, Kawase M, Okuno K (2005) Identification and mapping of two new loci for hybrid breakdown in cultivated rice. Rice Genet Newsl 22:29Google Scholar
  21. Gross SD, Anderson RA (1998) Casein kinase I: spatial organization and positioning of a multifunctional protein kinase family. Cell Signal 10(10):699–711CrossRefPubMedGoogle Scholar
  22. Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B (2000) Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19(15):4004–4014CrossRefPubMedGoogle Scholar
  23. Jones JD, Dangl JL (2006) The plant immune system. Nature 444(7117):323–329CrossRefPubMedGoogle Scholar
  24. Knippschild U, Gocht A, Wolff S, Huber N, Löhler J, Stöter M (2005) The casein kinase 1 family: participation in multiple cellular processes in eukaryotes. Cell Signal 17(6):675–689CrossRefPubMedGoogle Scholar
  25. 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(4):431–440CrossRefGoogle Scholar
  26. Kubo T, Yoshimura A (2002) Genetic basis of hybrid breakdown in a japonica/indica cross of rice, Oryza sativa L. Theor Appl Genet 105:906–911CrossRefPubMedGoogle Scholar
  27. Liu W, Xu ZH, Luo D, Xue HW (2003) Role of CKI1, a rice casein kinase I, in root development and plant hormone sensitivity. Plant J 36:189–202CrossRefPubMedGoogle Scholar
  28. Lomsadze A, Ter-Hovhannisyan V, Chernoff Y, Borodovsky M (2005) Gene identification in novel eukaryotic genomes by self-training algorithm. Nucleic Acids Res 33(20):6494–6506CrossRefPubMedGoogle Scholar
  29. Long Y, Zhao L, Niu B, Su J, Wu H, Chen Y, Zhang Q, Guo J, Zhuang C, Mei M, Xia J, Wang L, Wu H, Liu YG (2008) Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes. Proc Natl Acad Sci USA 105(48):18871–18876CrossRefPubMedGoogle Scholar
  30. Mackey D, Holt BF 3rd, Wiig A, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108(6):743–754CrossRefPubMedGoogle Scholar
  31. Matsubara K, Ando T, Mizubayashi T, Ito S, Yano M (2007) Identification and linkage mapping of complementary recessive genes causing hybrid breakdown in an intraspecific rice cross. Theor Appl Genet 115(2):179–186CrossRefPubMedGoogle Scholar
  32. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 5(4):809–834CrossRefGoogle Scholar
  33. Midoh N, Iwata M (1996) Cloning and characterization of a probenazole-inducible gene for an intracellular pathogenesis-related protein in rice. Plant Cell Physiol 37(1):9–18PubMedGoogle Scholar
  34. Mitsuhara I, Iwai T, Seo S, Yanagawa Y, Kawahigasi H, Hirose S, Ohkawa Y, Ohashi Y (2008) Characteristic expression of twelve rice PR1 family genes in response to pathogen infection, wounding, and defense-related signal compounds (121/180). Mol Genet Genomics 279(4):415–427CrossRefPubMedGoogle Scholar
  35. Miura K, Yamamoto E, Morinaka Y, Takashi T, Kitano H, Matsuoka M, Ashikari M (2008) The hybrid breakdown 1(t) locus induces interspecific hybrid breakdown between rice Oryza sativa cv. Koshihikari and its wild relative O. nivara. Breed Sci 58(2):99–105CrossRefGoogle Scholar
  36. Mondragon-Palomino M, Meyers BC, Michelmore RW, Gaut BS (2002) Patterns of positive selection in the complete NBS-LRR gene family of Arabidopsis thaliana. Genome Res 12:1305–1315CrossRefPubMedGoogle Scholar
  37. Mucyn TS, Clemente A, Andriotis VM, Balmuth AL, Oldroyd GE, Staskawicz BJ, Rathjen JP (2006) The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity. Plant Cell 18(10):2792–2806CrossRefPubMedGoogle Scholar
  38. Muller HJ (1942) Isolating mechanisms, evolution, and temperature. Biol Symp 6:71–124Google Scholar
  39. Nishimura A, Ashikari M, Lin S, Takashi T, Angeles ER, Yamamoto T, Matsuoka M (2005) Isolation of a rice regeneration quantitative trait loci gene and its application to transformation systems. Proc Natl Acad Sci USA 102(33):11940–11944CrossRefPubMedGoogle Scholar
  40. Rieseberg LH, Willis JH (2007) Plant speciation. Science 317(5840):910–914CrossRefPubMedGoogle Scholar
  41. Rieseberg LH, Wood TE, Baack EJ (2006) The nature of plant species. Nature 440(7083):524–527CrossRefPubMedGoogle Scholar
  42. Sato YI, Morishima H (1988) Distribution of the genes causing F2 chlorosis in rice cultivars of the indica and japonica types. Theor Appl Genet 75:723–724CrossRefGoogle Scholar
  43. Schaffrath U, Zabbai F, Dudler R (2000) Characterization of RCI-1, a chloroplastic rice lipoxygenase whose synthesis is induced by chemical plant resistance activators. Eur J Biochem 267(19):5935–5942CrossRefPubMedGoogle Scholar
  44. Shimono M, Sugano S, Nakayama A, Jiang CJ, Ono K, Toki S, Takatsuji H (2007) Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 19(6):2064–2076CrossRefPubMedGoogle Scholar
  45. Stebbins GL Jr (1950) Isolation and the origin of species. In: Stebbins GL Jr (ed) Variation and evolution in plants. Columbia University Press, New York, pp 189–250Google Scholar
  46. Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423(6935):74–77CrossRefPubMedGoogle Scholar
  47. van Hulten M, Pelser M, van Loon LC, Pieterse CM, Ton J (2006) Costs and benefits of priming for defense in Arabidopsis. Proc Natl Acad Sci USA 103(14):5602–5607CrossRefPubMedGoogle Scholar
  48. Yamamoto E, Takashi T, Morinika Y, Lin S, Kitano H, Matsuoka M, Ashikari M (2007) Interaction of two recessive genes, hbd2 and hbd3, induces hybrid breakdown in rice. Theor Appl Genet 115:187–194CrossRefPubMedGoogle Scholar
  49. Yang S, Feng Z, Zhang X, Jiang K, Jin X, Hang Y, Chen JQ, Tian D (2006) Genome-wide investigation on the genetic variations of rice disease resistance genes. Plant Mol Biol 62(1–2):181–193CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Eiji Yamamoto
    • 1
  • Tomonori Takashi
    • 2
  • Yoichi Morinaka
    • 2
  • Shaoyang Lin
    • 2
  • Jianzhong Wu
    • 3
  • Takashi Matsumoto
    • 3
  • Hidemi Kitano
    • 1
  • Makoto Matsuoka
    • 1
  • Motoyuki Ashikari
    • 1
  1. 1.Bioscience and Biotechnology CenterNagoya UniversityNagoyaJapan
  2. 2.Honda Research Institute JapanKisarazuJapan
  3. 3.National Institute of Agrobiological ResourcesTsukubaJapan

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