Skip to main content
Log in

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

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

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.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 5

Similar content being viewed by others

References

  • 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):157–165

    Article  CAS  PubMed  Google Scholar 

  • 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):290–298

    Article  CAS  PubMed  Google Scholar 

  • 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):81–90

    Article  CAS  Google Scholar 

  • 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):334–339

    Article  PubMed  Google Scholar 

  • 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 10:139–226

    Google Scholar 

  • 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):369–377

    Article  CAS  PubMed  Google Scholar 

  • 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):2822–2835

    Article  CAS  PubMed  Google Scholar 

  • Bergelson J, Kreitman M, Stahl EA, Tian D (2001) Evolutionary dynamics of plant R-genes. Science 292(5525):2281–2285

    Article  CAS  PubMed  Google Scholar 

  • 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):623–626

    Article  CAS  PubMed  Google Scholar 

  • Bomblies K, Weigel D (2007) Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat Rev Genet 8(5):382–393

    Article  CAS  PubMed  Google Scholar 

  • 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):e236

    Article  PubMed  Google Scholar 

  • 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):11436–11441

    Article  CAS  PubMed  Google Scholar 

  • Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host–microbe interactions: shaping the evolution of the plant immune response. Cell 124(4):803–814

    Article  CAS  PubMed  Google Scholar 

  • Coaker G, Falick A, Staskawicz B (2005) Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin. Science 308(5721):548–550

    Article  CAS  PubMed  Google Scholar 

  • Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland

  • DeYoung BJ, Innes RW (2006) Plant NBS-LRR proteins in pathogen sensing and host defense. Nat Immunol 7(12):1243–1249

    Article  CAS  PubMed  Google Scholar 

  • Dobzhansky T (1937) Genetics and the origin of species. Columbia University Press, New York

    Google Scholar 

  • 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):8888–8893

    Article  Google Scholar 

  • Fukuoka S, Namai H, Okuno K (1998) RFLP mapping of the genes controlling hybrid breakdown in rice. Theor Appl Genet 97:446–449

    Article  CAS  Google Scholar 

  • 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 22:29

    Google Scholar 

  • Gross SD, Anderson RA (1998) Casein kinase I: spatial organization and positioning of a multifunctional protein kinase family. Cell Signal 10(10):699–711

    Article  CAS  PubMed  Google Scholar 

  • 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):4004–4014

    Article  CAS  PubMed  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444(7117):323–329

    Article  CAS  PubMed  Google Scholar 

  • 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):675–689

    Article  CAS  PubMed  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(4):431–440

    Article  CAS  Google Scholar 

  • Kubo T, Yoshimura A (2002) Genetic basis of hybrid breakdown in a japonica/indica cross of rice, Oryza sativa L. Theor Appl Genet 105:906–911

    Article  CAS  PubMed  Google Scholar 

  • 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 36:189–202

    Article  CAS  PubMed  Google Scholar 

  • 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):6494–6506

    Article  CAS  PubMed  Google Scholar 

  • 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):18871–18876

    Article  CAS  PubMed  Google Scholar 

  • 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):743–754

    Article  CAS  PubMed  Google Scholar 

  • 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):179–186

    Article  CAS  PubMed  Google Scholar 

  • 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):809–834

    Article  Google Scholar 

  • 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):9–18

    CAS  PubMed  Google Scholar 

  • 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):415–427

    Article  CAS  PubMed  Google Scholar 

  • 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):99–105

    Article  CAS  Google Scholar 

  • 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 12:1305–1315

    Article  CAS  PubMed  Google Scholar 

  • 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):2792–2806

    Article  CAS  PubMed  Google Scholar 

  • Muller HJ (1942) Isolating mechanisms, evolution, and temperature. Biol Symp 6:71–124

    Google Scholar 

  • 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):11940–11944

    Article  CAS  PubMed  Google Scholar 

  • Rieseberg LH, Willis JH (2007) Plant speciation. Science 317(5840):910–914

    Article  CAS  PubMed  Google Scholar 

  • Rieseberg LH, Wood TE, Baack EJ (2006) The nature of plant species. Nature 440(7083):524–527

    Article  CAS  PubMed  Google Scholar 

  • Sato YI, Morishima H (1988) Distribution of the genes causing F2 chlorosis in rice cultivars of the indica and japonica types. Theor Appl Genet 75:723–724

    Article  Google Scholar 

  • 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):5935–5942

    Article  CAS  PubMed  Google Scholar 

  • 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):2064–2076

    Article  CAS  PubMed  Google Scholar 

  • 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 189–250

    Google Scholar 

  • Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423(6935):74–77

    Article  CAS  PubMed  Google Scholar 

  • 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):5602–5607

    Article  PubMed  Google Scholar 

  • 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 115:187–194

    Article  CAS  PubMed  Google Scholar 

  • 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):181–193

    Article  CAS  PubMed  Google Scholar 

Download references

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.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Motoyuki Ashikari.

Additional information

Communicated by K. Shirasu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Table 1 (XLS 32 kb)

Supplementary Table 2 (XLS 31 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yamamoto, E., Takashi, T., Morinaka, Y. et al. Gain of deleterious function causes an autoimmune response and Bateson–Dobzhansky–Muller incompatibility in rice. Mol Genet Genomics 283, 305–315 (2010). https://doi.org/10.1007/s00438-010-0514-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-010-0514-y

Keywords

Navigation