Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Genetic analysis of interspecific incompatibility in Brassica rapa

  • 579 Accesses

  • 13 Citations

Abstract

In interspecific pollination of Brassica rapa stigmas with Brassica oleracea pollen grains, pollen tubes cannot penetrate stigma tissues. This trait, called interspecific incompatibility, is similar to self-incompatibility in pollen tube behaviors of rejected pollen grains. Since some B. rapa lines have no interspecific incompatibility, genetic analysis of interspecific incompatibility was performed using two F2 populations. Analysis with an F2 population between an interspecific-incompatible line and a self-compatible cultivar ‘Yellow sarson’ having non-functional alleles of S-locus genes and MLPK, the stigmas of which are compatible with B. oleracea pollen grains, revealed no involvement of the S locus and MLPK in the difference of their interspecific incompatibility phenotypes. In QTL analysis of the strength of interspecific incompatibility, three peaks of LOD scores were found, but their LOD scores were as high as the threshold value, and the variance explained by each QTL was small. QTL analysis using another F2 population derived from selected parents having the highest and lowest levels of interspecific incompatibility revealed five QTLs with high LOD scores, which did not correspond to those found in the former population. The QTL having the highest LOD score was found in linkage group A02. The effect of this QTL on interspecific incompatibility was confirmed by analyzing backcrossed progeny. Based on synteny of this QTL region with Arabidopsis thaliana chromosome 5, a possible candidate gene, which might be involved in interspecific incompatibility, is discussed.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Bernacchi D, Tanksley SD (1997) An interspecific backcross of Lycopersicon esculentum X L. hirsutum: linkage analysis and a QTL study of sexual compatibility factors and floral traits. Genetics 147:861–877

  2. Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

  3. Escobar-Restrepo J-M, Huck, Kessler NS, Gagliardini V, Gheyselinck J, Yang W-C, Grossniklaus U (2007) The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317:656–660

  4. Fujimoto R, Sugimura T, Fukai E, Nishio T (2006) Suppression of gene expression of a recessive SP11/SCR allele by an untranscribed SP11/SCR allele in Brassica self-incompatibility. Plant Mol Biol 61:577–587

  5. Gu T, Mazzurco M, Sulaman W, Matias DD, Goring DR (1998) Binding of an arm repeat protein to the kinase domain of the S-locus receptor kinase. Proc Natl Acad Sci USA 95:382–387

  6. Guo H, Li L, Ye H, Yu X, Algreen A, Yin Y (2009) Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc Natl Acad Sci USA 106:7648–7653

  7. Hinata K, Okazaki K, Nishio T (1983) Gene analysis of self-compatibility in Brassica campestris var. yellow sarson (a case of recessive epistatic modifier) In: Proc 6th Int Rapeseed Conf 1:354–359

  8. Hiscock SJ, Dickinson HG (1993) Unilateral incompatibility within the Brassicaceae: further evidence for the involvement of the self-incompatibility (S)-locus. Theor Appl Genet 86:744–753

  9. Iniguez-Luy FL, Voort AV, Osborn TC (2008) Development of a set of public SSR markers derived from genomic sequence of a rapid cycling Brassica oleracea L. genotype. Theor Appl Genet 117:977–985

  10. Inoue H, Nishio T (2004) Efficiency of PCR-RF-SSCP marker production in Brassica oleracea using Brassica EST sequences. Euphytica 137:233–242

  11. Iwata H, Ninomiya S (2006) AntMap: constructing genetic linkage maps using an ant colony optimization algorithm. Breed Sci 56:371–378

  12. Kim JS, Chung TY, King GJ, Jin M, Yang T-J, Jin Y-M, Kim H-I, Park B-S (2006) A sequence-tagged linkage map of Brassica rapa. Genetics 174:29–39

  13. Kitashiba H, Nishio T (2009) Self-incompatibility. In: Gupta (ed) Biology and Breeding of Crucifers. CRC Press, New York, pp 99–112

  14. Lewis D, Crowe LK (1958) Unilateral incompatibility in flowering plants. Heredity 12:233–256

  15. Li F, Kitashiba H, Inaba K, Nishio T (2009) A Brassica rapa linkage map of EST-based SNP markers for identification of candidate genes controlling flowering time and leaf morphological traits. DNA Res (in press)

  16. Murase K, Shiba H, Iwano M, Che F-S, Watanabe M, Isogai A, Takayama S (2004) A membrane-anchored protein kinase involved in Brassica self-incompatibility signaling. Science 303:1516–1519

  17. Murfett J, Strabala TJ, Zurek DM, Mou B, Beecher B, McClure B (1996) S RNase and interspecific pollen rejection in the genus Nicotiana: multiple pollen-rejection pathways contribute to unilateral incompatibility between self-incompatible and self-compatible species. Plant Cell 8:943–958

  18. Nettancourt DD (2001) Incompatibility and incongruity in wild and cultivated plants, 2nd edn. Springer, Berlin, p 322

  19. Nishio T, Kusaba M, Watanabe M, Hinata K (1996) Registration of S alleles in Brassica campestris L. by the restriction fragment sizes of SLGs. Theor Appl Genet 92:388–394

  20. Sato Y, Fujimoto R, Toriyama K, Nishio T (2003) Commonality of self-recognition specificity of S haplotypes between Brassica oleracea and Brassica rapa. Plant Mol Biol 52:617–626

  21. Schopfer CR, Nasrallah ME, Nasrallah JB (1999) The male determinant of self-incompatibility in Brassica. Science 286:1697–1700

  22. Shirasawa K, Shiokai S, Yamaguchi M, Kishitani S, Nishio T (2006) Dot-blot-SNP analysis for practical plant breeding and cultivar identification in rice. Theor Appl Genet 113:147–155

  23. Shiu SH, Bleecker AB (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132:530–543

  24. Stein JC, Howlett B, Boyes DC, Nasrallah ME, Nasrallah JB (1991) Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc Natl Acad Sci USA 88:8816–8820

  25. Stone SL, Arnoldo M, Goring DR (1999) A breakdown of Brassica self-incompatibility in ARC1 antisense transgenic plants. Science 286:1729–1731

  26. Suwabe K, Tsukazaki H, Iketani H, Hatakeyama K, Kondo M, Fujimura M, Nunome T, Fukuoka H, Hirai M, Matsumoto S (2006) Simple sequence repeat-based comparative genomics between Brassica rapa and Arabidopsis thaliana: the genetic origin of clubroot resistance. Genetics 173:309–319

  27. Suzuki G, Kai N, Hirose T, Fukui K, Nishio T, Takayama S, Isogai A, Watanabe M, Hinata K (1999) Genomic organization of the S locus: identification and characterization of genes in SLG/SRK region of S9 haplotype of Brassica campestris (syn. rapa). Genetics 153:391–400

  28. Takuno S, Oikawa E, Kitashiba H, Nishio T (2010) Assessment of genetic diversity of accessions in Brassicaceae genetic resources by frequency distribution analysis of S haplotypes. Theor Appl Genet (in press)

  29. Tamura K, Nishioka M, Hayashi M, Zhang Z, Lian Z, Hougetsu T, Harada K (2005) Development of microsatellite markers by ISSR-suppression-PCR method in Brassica rapa. Breed Sci 55:247–252

  30. Tung CW, Dwyer GK, Nasrallah ME, Nasrallah JB (2005) Genome-wide identification of genes expressed in Arabidopsis pistils specifically along the path of pollen tube growth. Plant Physiol 138:977–989

Download references

Acknowledgments

We are grateful to Dr. Kuginuki of Asahi Noen Seed Co. Ltd. for providing seeds of ‘Osome P11’ and ‘Harusakari P04’. This work was supported in part by a Grant-in-Aid for Scientific Research (A) (no. 19208001) from the Japan Society for the Promotion of Science (JSPS) and the Program for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry (BRAIN).

Author information

Correspondence to T. Nishio.

Additional information

Communicated by R. Visser.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Udagawa, H., Ishimaru, Y., Li, F. et al. Genetic analysis of interspecific incompatibility in Brassica rapa . Theor Appl Genet 121, 689–696 (2010). https://doi.org/10.1007/s00122-010-1340-7

Download citation

Keywords

  • Linkage Group
  • Pollen Tube
  • Doubled Haploid Line
  • Interspecific Pollination
  • Unilateral Incompatibility