Genetics, Vol 139, 975-992, Copyright © 1995


INVESTIGATIONS

A Generalized Least-Squares Estimate for the Origin of Sporophytic Self-Incompatibility

M. K. Uyenoyama
Department of Zoology, Duke University, Durham, North Carolina 27708-0325

Analysis of nucleotide sequences that regulate the expression of self-incompatibility in flowering plants affords a direct means of examining classical hypotheses for the origin and evolution of this major feature of mating systems. Departing from the classical view of monophyly of all forms of self-incompatibility, the current paradigm for the origin of self-incompatibility postulates multiple episodes of recruitment and modification of preexisting genes. In Brassica, the S locus, which regulates sporophytic self-incompatibility, shows homology to a multigene family present both in self-compatible congeners and in groups for which this form of self-incompatibility is atypical. A phylogenetic analysis of S-allele sequences together with homologous sequences that do not cosegregate with self-incompatibility permits dating the change of function that marked the origin of self-incompatibility. A generalized least-squares method is introduced that provides closed-form expressions for estimates and standard errors for function-specific divergence rates and times of divergence among sequences. This analysis suggests that the age of the sporophytic self-incompatibility system expressed in Brassica exceeds species divergence within the genus by four- to fivefold. The extraordinarily high levels of sequence diversity exhibited by S alleles appears to reflect their ancient derivation, with the alternative hypothesis of hypermutability rejected by the analysis.


This article has been cited by other articles:


Home page
GeneticsHome page
J. W. Busch, J. Sharma, and D. J. Schoen
Molecular Characterization of Lal2, an SRK-Like Gene Linked to the S-Locus in the Wild Mustard Leavenworthia alabamica
Genetics, April 1, 2008; 178(4): 2055 - 2067.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
M. Hasselmann, X. Vekemans, J. Pflugfelder, N. Koeniger, G. Koeniger, S. Tingek, and M. Beye
Evidence for Convergent Nucleotide Evolution and High Allelic Turnover Rates at the complementary sex determiner Gene of Western and Asian Honeybees
Mol. Biol. Evol., April 1, 2008; 25(4): 696 - 708.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
G. J. Houliston and M. S. Olson
Nonneutral Evolution of Organelle Genes in Silene vulgaris
Genetics, December 1, 2006; 174(4): 1983 - 1994.
[Abstract] [Full Text] [PDF]


Home page
ANN BOT (LOND)Home page
I. MATEU-ANDRES and L. DE PACO
Genetic Diversity and the Reproductive System in Related Species of Antirrhinum
Ann. Bot., November 1, 2006; 98(5): 1053 - 1060.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
L. Timms, R. Jimenez, M. Chase, D. Lavelle, L. McHale, A. Kozik, Z. Lai, A. Heesacker, S. Knapp, L. Rieseberg, et al.
Analyses of Synteny Between Arabidopsis thaliana and Species in the Asteraceae Reveal a Complex Network of Small Syntenic Segments and Major Chromosomal Rearrangements
Genetics, August 1, 2006; 173(4): 2227 - 2235.
[Abstract] [Full Text] [PDF]


Home page
Genome ResHome page
M. A. Lysak, M. A. Koch, A. Pecinka, and I. Schubert
Chromosome triplication found across the tribe Brassiceae
Genome Res., April 1, 2005; 15(4): 516 - 525.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Bot.Home page
M. J. Sanderson, J. L. Thorne, N. Wikstrom, and K. Bremer
Molecular evidence on plant divergence times
Am. J. Botany, October 1, 2004; 91(10): 1656 - 1665.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
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]


Home page
Proc. Natl. Acad. Sci. USAHome page
T. Chookajorn, A. Kachroo, D. R. Ripoll, A. G. Clark, and J. B. Nasrallah
Inaugural Article: Specificity determinants and diversification of the Brassica self-incompatibility pollen ligand
PNAS, January 27, 2004; 101(4): 911 - 917.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
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]


Home page
Mol Biol EvolHome page
Y. Lu and M. D. Rausher
Evolutionary Rate Variation in Anthocyanin Pathway Genes
Mol. Biol. Evol., November 1, 2003; 20(11): 1844 - 1853.
[Abstract] [Full Text] [PDF]


Home page
J Exp BotHome page
B. P. Kemp and J. Doughty
Just how complex is the BrassicaS-receptor complex?
J. Exp. Bot., January 1, 2003; 54(380): 157 - 168.
[Abstract] [Full Text] [PDF]


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


Home page
Mol Biol EvolHome page
M. J. Sanderson
Estimating Absolute Rates of Molecular Evolution and Divergence Times: A Penalized Likelihood Approach
Mol. Biol. Evol., January 1, 2002; 19(1): 101 - 109.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
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]


Home page
GeneticsHome page
M. H. Schierup, B. K. Mable, P. Awadalla, and D. Charlesworth
Identification and Characterization of a Polymorphic Receptor Kinase Gene Linked to the Self-Incompatibility Locus of Arabidopsis lyrata
Genetics, May 1, 2001; 158(1): 387 - 399.
[Abstract] [Full Text]


Home page
GeneticsHome page
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]


Home page
Plant CellHome page
M. Kusaba, K. Dwyer, J. Hendershot, J. Vrebalov, J. B. Nasrallah, and M. E. Nasrallah
Self-Incompatibility in the Genus Arabidopsis: Characterization of the S Locus in the Outcrossing A. lyrata and Its Autogamous Relative A. thaliana
PLANT CELL, March 1, 2001; 13(3): 627 - 643.
[Abstract] [Full Text]


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


Home page
Proc. Natl. Acad. Sci. USAHome page
G. May, F. Shaw, H. Badrane, and X. Vekemans
The signature of balancing selection: Fungal mating compatibility gene evolution
PNAS, August 3, 1999; 96(16): 9172 - 9177.
[Abstract] [Full Text] [PDF]


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


Home page
GeneticsHome page
M. H. Schierup, X. Vekemans, and F. B. Christiansen
Allelic Genealogies in Sporophytic Self-Incompatibility Systems in Plants
Genetics, November 1, 1998; 150(3): 1187 - 1198.
[Abstract] [Full Text]


Home page
GeneticsHome page
K. Hatakeyama, T. Takasaki, M. Watanabe, and K. Hinata
Molecular Characterization of S Locus Genes, SLG and SRK, in a Pollen-Recessive Self-Incompatibility Haplotype of Brassica rapa L
Genetics, July 1, 1998; 149(3): 1587 - 1597.
[Abstract] [Full Text] [PDF]


Home page
Plant CellHome page
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]


Home page
Proc. Natl. Acad. Sci. USAHome page
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]


Home page
Proc. Natl. Acad. Sci. USAHome page
M. Kusaba, T. Nishio, Y. Satta, K. Hinata, and D. Ockendon
Striking sequence similarity in inter- and intra-specific comparisons of class I SLG alleles from Brassica oleracea and Brassica campestris: Implications for the evolution and recognition mechanism
PNAS, July 8, 1997; 94(14): 7673 - 7678.
[Abstract] [Full Text] [PDF]


Home page
Plant CellHome page
H. Shiba, M. Iwano, T. Entani, K. Ishimoto, H. Shimosato, F.-S. Che, Y. Satta, A. Ito, Y. Takada, M. Watanabe, et al.
The Dominance of Alleles Controlling Self-Incompatibility in Brassica Pollen Is Regulated at the RNA Level
PLANT CELL, February 1, 2002; 14(2): 491 - 504.
[Abstract] [Full Text] [PDF]