THE PLANT CELL, Vol 9, Issue 2 237-247, Copyright © 1997 by American Society of Plant Biologists

RESEARCH ARTICLE

The Self-Incompatibility (S) Haplotypes of Brassica Contain Highly Divergent and Rearranged Sequences of Ancient Origin

D. C. Boyes, M. E. Nasrallah, J. Vrebalov and J. B. Nasrallah
Section of Plant Biology, Division of Biological Sciences, Cornell University, Ithaca, New York 14853

In Brassica, the recognition of self-related pollen by the stigma is controlled by the highly polymorphic S locus that encodes several linked and coadapted genes and can span several hundred kilobases. We used pulsed-field gel electrophoresis to analyze the structure of different S haplotypes. We show that the S2 and S13 haplotypes of Brassica oleracea contain extensive sequence divergence and rearrangement relative to each other. In contrast, haplotypic configuration is more conserved between B. oleracea S13 and B. campestris S8, two haplotypes that have been proposed to be derived from a common ancestral haplotype based on sequence comparisons. These results support the view that extensive restructuring of the S locus preceded speciation in Brassica. This structural heteromorphism, together with haplotype-specific sequences, may suppress recombination within the S locus complex, potentially providing a mechanism for maintaining the linkage of coadapted allelic combinations of genes over time.

This article has been cited by other articles:

				S. Takuno, R. Fujimoto, T. Sugimura, K. Sato, S. Okamoto, S.-L. Zhang, and T. Nishio Effects of Recombination on Hitchhiking Diversity in the Brassica Self-incompatibility Locus Complex Genetics, October 1, 2007; 177(2): 949 - 958. [Abstract] [Full Text] [PDF]

				S. Sherman-Broyles, N. Boggs, A. Farkas, P. Liu, J. Vrebalov, M. E. Nasrallah, and J. B. Nasrallah S Locus Genes and the Evolution of Self-Fertility in Arabidopsis thaliana PLANT CELL, January 1, 2007; 19(1): 94 - 106. [Abstract] [Full Text] [PDF]

				J. L. Kermicle A Selfish Gene Governing Pollen-Pistil Compatibility Confers Reproductive Isolation Between Maize Relatives Genetics, January 1, 2006; 172(1): 499 - 506. [Abstract] [Full Text] [PDF]

				N. L. Prigoda, A. Nassuth, and B. K. Mable Phenotypic and Genotypic Expression of Self-incompatibility Haplotypes in Arabidopsis lyrata Suggests Unique Origin of Alleles in Different Dominance Classes Mol. Biol. Evol., July 1, 2005; 22(7): 1609 - 1620. [Abstract] [Full Text] [PDF]

				S. I. Wright and B. S. Gaut Molecular Population Genetics and the Search for Adaptive Evolution in Plants Mol. Biol. Evol., March 1, 2005; 22(3): 506 - 519. [Abstract] [Full Text] [PDF]

				T. Sonneveld, K. R. Tobutt, S. P. Vaughan, and T. P. Robbins Loss of Pollen-S Function in Two Self-Compatible Selections of Prunus avium Is Associated with Deletion/Mutation of an S Haplotype-Specific F-Box Gene PLANT CELL, January 1, 2005; 17(1): 37 - 51. [Abstract] [Full Text] [PDF]

				N. Takebayashi, E. Newbigin, and M. K. Uyenoyama Maximum-Likelihood Estimation of Rates of Recombination Within Mating-Type Regions Genetics, August 1, 2004; 167(4): 2097 - 2109. [Abstract] [Full Text] [PDF]

				Y. Akiyama, J. A. Conner, S. Goel, D. T. Morishige, J. E. Mullet, W. W. Hanna, and P. Ozias-Akins High-Resolution Physical Mapping in Pennisetum squamulatum Reveals Extensive Chromosomal Heteromorphism of the Genomic Region Associated with Apomixis Plant Physiology, April 1, 2004; 134(4): 1733 - 1741. [Abstract] [Full Text] [PDF]

				N. Takebayashi, P. B. Brewer, E. Newbigin, and M. K. Uyenoyama Patterns of Variation Within Self-Incompatibility Loci Mol. Biol. Evol., November 1, 2003; 20(11): 1778 - 1794. [Abstract] [Full Text] [PDF]

				K. Ushijima, H. Sassa, A. M. Dandekar, T. M. Gradziel, R. Tao, and H. Hirano Structural and Transcriptional Analysis of the Self-Incompatibility Locus of Almond: Identification of a Pollen-Expressed F-Box Gene with Haplotype-Specific Polymorphism PLANT CELL, March 1, 2003; 15(3): 771 - 781. [Abstract] [Full Text] [PDF]

				M. J. Wheeler, S. A. Armstrong, V. E. Franklin-Tong, and F. C. H. Franklin Genomic organization of the Papaver rhoeas self-incompatibility S1 locus J. Exp. Bot., January 1, 2003; 54(380): 131 - 139. [Abstract] [Full Text] [PDF]

				K. B. Lengeler, D. S. Fox, J. A. Fraser, A. Allen, K. Forrester, F. S. Dietrich, and J. Heitman Mating-Type Locus of Cryptococcus neoformans: a Step in the Evolution of Sex Chromosomes Eukaryot. Cell, October 1, 2002; 1(5): 704 - 718. [Abstract] [Full Text] [PDF]

				J. B. Nasrallah Recognition and Rejection of Self in Plant Reproduction Science, April 12, 2002; 296(5566): 305 - 308. [Abstract] [Full Text] [PDF]

				S. Glemin, T. Bataillon, J. Ronfort, A. Mignot, and I. Olivieri Inbreeding Depression in Small Populations of Self-Incompatible Plants Genetics, November 1, 2001; 159(3): 1217 - 1229. [Abstract] [Full Text] [PDF]

				C. Miege, V. Ruffio-Chable, M. H. Schierup, D. Cabrillac, C. Dumas, T. Gaude, and J. M. Cock Intrahaplotype Polymorphism at the Brassica S Locus Genetics, October 1, 2001; 159(2): 811 - 822. [Abstract] [Full Text] [PDF]

				U. Grossniklaus, G. A. Nogler, and P. J. van Dijk How to Avoid Sex: The Genetic Control of Gametophytic Apomixis PLANT CELL, July 1, 2001; 13(7): 1491 - 1498. [Full Text] [PDF]

				M. Watanabe, K. Hatakeyama, Y. Takada, and K. Hinata Molecular Aspects of Self-Incompatibility in Brassica Species Plant Cell Physiol., June 1, 2001; 42(6): 560 - 565. [Abstract] [Full Text] [PDF]

				M. K. Uyenoyama, Y. Zhang, and E. Newbigin On the Origin of Self-Incompatibility Haplotypes: Transition Through Self-Compatible Intermediates Genetics, April 1, 2001; 157(4): 1805 - 1817. [Abstract] [Full Text]

				X. Wang, A. L. Hughes, T. Tsukamoto, T. Ando, and T.-H. Kao Evidence That Intragenic Recombination Contributes to Allelic Diversity of the S-RNase Gene at the Self-Incompatibility (S) Locus in Petunia inflata Plant Physiology, February 1, 2001; 125(2): 1012 - 1022. [Abstract] [Full Text]

				R. Dixit and J. B. Nasrallah Recognizing Self in the Self-Incompatibility Response Plant Physiology, January 1, 2001; 125(1): 105 - 108. [Full Text]

				M. K. Uyenoyama Evolutionary Dynamics of Self-Incompatibility Alleles in Brassica Genetics, September 1, 2000; 156(1): 351 - 359. [Abstract] [Full Text]

				R. Dixit, M. E. Nasrallah, and J. B. Nasrallah Post-Transcriptional Maturation of the S Receptor Kinase of Brassica Correlates with Co-Expression of the S-Locus Glycoprotein in the Stigmas of Two Brassica Strains and in Transgenic Tobacco Plants Plant Physiology, September 1, 2000; 124(1): 297 - 312. [Abstract] [Full Text]

				V. E. Franklin-Tong and F. C. H. Franklin Self-Incompatibility in Brassica: The Elusive Pollen S Gene Is Identified! PLANT CELL, March 1, 2000; 12(3): 305 - 308. [Full Text]

				R. M. Harbord, C. A. Napoli, and T. P. Robbins Segregation Distortion of T-DNA Markers Linked to the Self-Incompatibility (S) Locus in Petunia hybrida Genetics, March 1, 2000; 154(3): 1323 - 1333. [Abstract] [Full Text]

				A. L. Casselman, J. Vrebalov, J. A. Conner, A. Singhal, J. Giovannoni, M. E. Nasrallah, and J. B. Nasrallah Determining the Physical Limits of the Brassica S Locus by Recombinational Analysis PLANT CELL, January 1, 2000; 12(1): 23 - 34. [Abstract] [Full Text] [PDF]

				C. R. Schopfer, M. E. Nasrallah, and J. B. Nasrallah The Male Determinant of Self-Incompatibility in Brassica Science, November 26, 1999; 286(5445): 1697 - 1700. [Abstract] [Full Text]

				Y. Cui, N. Brugière, L. Jackman, Y.-M. Bi, and S. J. Rothstein Structural and Transcriptional Comparative Analysis of the S Locus Regions in Two Self-Incompatible Brassica napus Lines PLANT CELL, November 1, 1999; 11(11): 2217 - 2232. [Abstract] [Full Text]

				G. Suzuki, N. Kai, T. Hirose, K. Fukui, T. Nishio, S. Takayama, A. Isogai, M. Watanabe, and K. Hinata Genomic Organization of the S Locus: Identification and Characterization of Genes in SLG/SRK Region of S9 Haplotype of Brassica campestris (syn. rapa) Genetics, September 1, 1999; 153(1): 391 - 400. [Abstract] [Full Text]

				P. Awadalla and D. Charlesworth Recombination and Selection at Brassica Self-Incompatibility Loci Genetics, May 1, 1999; 152(1): 413 - 425. [Abstract] [Full Text]

				D. Cabrillac, V. Delorme, J. Garin, V. Ruffio-Châble, J.-L. Giranton, C. Dumas, T. Gaude, and J. M. Cock The S15 Self-Incompatibility Haplotype in Brassica oleracea Includes Three S Gene Family Members Expressed in Stigmas PLANT CELL, May 1, 1999; 11(5): 971 - 986. [Abstract] [Full Text]

				R. W. Michelmore and B. C. Meyers Clusters of Resistance Genes in Plants Evolve by Divergent Selection and a Birth-and-Death Process Genome Res., November 1, 1998; 8(11): 1113 - 1130. [Abstract] [Full Text]

				J. A. Conner, P. Conner, M. E. Nasrallah, and J. B. Nasrallah Comparative Mapping of the Brassica S Locus Region and Its Homeolog in Arabidopsis: Implications for the Evolution of Mating Systems in the Brassicaceae PLANT CELL, May 1, 1998; 10(5): 801 - 812. [Abstract] [Full Text] [PDF]

				P. Ozias-Akins, D. Roche, and W. W. Hanna Tight clustering and hemizygosity of apomixis-linked molecular markers in Pennisetum squamulatum implies genetic control of apospory by a divergent locus that may have no allelic form in sexual genotypes PNAS, April 28, 1998; 95(9): 5127 - 5132. [Abstract] [Full Text] [PDF]

				J. B. Nasrallah Evolution of the Brassica self-incompatibility locus: A look into S-locus gene polymorphisms PNAS, September 2, 1997; 94(18): 9516 - 9519. [Full Text] [PDF]

				S. Takayama, H. Shiba, M. Iwano, H. Shimosato, F.-S. Che, N. Kai, M. Watanabe, G. Suzuki, K. Hinata, and A. Isogai The pollen determinant of self-incompatibility in Brassica campestris PNAS, February 15, 2000; 97(4): 1920 - 1925. [Abstract] [Full Text] [PDF]

				Y. Cui, Y.-M. Bi, N. Brugiere, M. Arnoldo, and S. J. Rothstein The S locus glycoprotein and the S receptor kinase are sufficient for self-pollen rejection in Brassica PNAS, March 28, 2000; 97(7): 3713 - 3717. [Abstract] [Full Text] [PDF]