Hybrid Incompatibility in Arabidopsis Is Determined by a Multiple-Locus Genetic Network1[W][OA]

The cross between Arabidopsis thaliana and the closely related species Arabidopsis arenosa results in postzygotic hybrid incompatibility, manifested as seed death. Ecotypes of A. thaliana were tested for their ability to produce live seed when crossed to A. arenosa. The identified genetic variation was used to map quantitative trait loci (QTLs) encoded by the A. thaliana genome that affect the frequency of postzygotic lethality and the phenotypes of surviving seeds. Seven QTLs affecting the A. thaliana component of this hybrid incompatibility were identified by crossing a Columbia × C24 recombinant inbred line population to diploid A. arenosa pollen donors. Additional epistatic loci were identified based on their pairwise interaction with one or several of these QTLs. Epistatic interactions were detected for all seven QTLs. The two largest additive QTLs were subjected to fine-mapping, indicating the action of at least two genes in each. The topology of this network reveals a large set of minor-effect loci from the maternal genome controlling hybrid growth and viability at different developmental stages. Our study establishes a framework that will enable the identification and characterization of genes and pathways in A. thaliana responsible for hybrid lethality in the A. thaliana × A. arenosa interspecific cross.

[1]  J. Willis,et al.  EVIDENCE FOR DOBZHANSKY‐MULLER INCOMPATIBILITES CONTRIBUTING TO THE STERILITY OF HYBRIDS BETWEEN MIMULUS GUTTATUS AND M. NASUTUS , 2001, Evolution; international journal of organic evolution.

[2]  Mattias Jakobsson,et al.  A unique recent origin of the allotetraploid species Arabidopsis suecica: Evidence from nuclear DNA markers. , 2006, Molecular biology and evolution.

[3]  R. Meyer,et al.  Construction and analysis of 2 reciprocal Arabidopsis introgression line populations. , 2008, The Journal of heredity.

[4]  O. Loudet,et al.  Divergent Evolution of Duplicate Genes Leads to Genetic Incompatibilities Within A. thaliana , 2009, Science.

[5]  N. Warthmann,et al.  Autoimmune Response as a Mechanism for a Dobzhansky-Muller-Type Incompatibility Syndrome in Plants , 2007, PLoS biology.

[6]  M. Yano,et al.  A genome-wide survey of reproductive barriers in an intraspecific hybrid. , 2001, Genetics.

[7]  R. Meyer,et al.  Segregation distortion in Arabidopsis C24/Col-0 and Col-0/C24 recombinant inbred line populations is due to reduced fertility caused by epistatic interaction of two loci , 2006, Theoretical and Applied Genetics.

[8]  J. Palmer,et al.  1 Systematic Relationships of Arabidopsis: A Molecular and Morphological Perspective , 1994 .

[9]  L. Rieseberg,et al.  Speciation genes in plants. , 2010, Annals of botany.

[10]  F. Berger,et al.  Maternal Control of Integument Cell Elongation and Zygotic Control of Endosperm Growth Are Coordinated to Determine Seed Size in Arabidopsis , 2005, The Plant Cell Online.

[11]  D G Brown,et al.  Selective mapping: a strategy for optimizing the construction of high-density linkage maps. , 2000, Genetics.

[12]  D. Weigel,et al.  Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species , 2007, Nature Reviews Genetics.

[13]  H. A. Orr,et al.  THE EVOLUTION OF POSTZYGOTIC ISOLATION: ACCUMULATING DOBZHANSKY‐MULLER INCOMPATIBILITIES , 2001, Evolution; international journal of organic evolution.

[14]  L. K. Crowe,et al.  Unilateral interspecific incompatibility in flowering plants , 1958, Heredity.

[15]  Katy C. Kao,et al.  A Genome-Wide Analysis Reveals No Nuclear Dobzhansky-Muller Pairs of Determinants of Speciation between S. cerevisiae and S. paradoxus, but Suggests More Complex Incompatibilities , 2010, PLoS genetics.

[16]  Caroline Josefsson,et al.  Parent-Dependent Loss of Gene Silencing during Interspecies Hybridization , 2006, Current Biology.

[17]  T. Dobzhansky,et al.  Studies on hybrid sterility , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[18]  J. Coyne,et al.  A Test of the Snowball Theory for the Rate of Evolution of Hybrid Incompatibilities , 2010, Science.

[19]  J. Draper,et al.  The isolation and characterisation of the tapetum-specific Arabidopsis thaliana A9 gene , 1992, Plant Molecular Biology.

[20]  Jonathan D. G. Jones,et al.  Cladosporium Avr2 Inhibits Tomato Rcr3 Protease Required for Cf-2-Dependent Disease Resistance , 2005, Science.

[21]  François Curtin,et al.  Multiple correlations and bonferroni’s correction , 1998, Biological Psychiatry.

[22]  B. Dilkes,et al.  A Differential Dosage Hypothesis for Parental Effects in Seed Development , 2004, The Plant Cell Online.

[23]  L. Moyle,et al.  Hybrid Incompatibility “Snowballs” Between Solanum Species , 2010, Science.

[24]  B. Dilkes,et al.  Aneuploidy and Genetic Variation in the Arabidopsis thaliana Triploid Response , 2005, Genetics.

[25]  M. Marinus.  DNA methylation in Escherichia coli. , 1987, Annual review of genetics.

[26]  T. Dobzhansky.  Studies on Hybrid Sterility. II. Localization of Sterility Factors in Drosophila Pseudoobscura Hybrids. , 1936, Genetics.

[27]  K. Bomblies.  Doomed lovers: mechanisms of isolation and incompatibility in plants. , 2010, Annual review of plant biology.

[28]  R. Doerge,et al.  Empirical threshold values for quantitative trait mapping. , 1994, Genetics.

[29]  J. Willis,et al.  NATURAL VARIATION FOR A HYBRID INCOMPATIBILITY BETWEEN TWO SPECIES OF MIMULUS , 2007, Evolution; international journal of organic evolution.

[30]  D. Presgraves,et al.  The molecular evolutionary basis of species formation , 2010, Nature Reviews Genetics.

[31]  H. Walia,et al.  Dosage-Dependent Deregulation of an AGAMOUS-LIKE Gene Cluster Contributes to Interspecific Incompatibility , 2009, Current Biology.

[32]  Steven J. M. Jones,et al.  Circos: an information aesthetic for comparative genomics. , 2009, Genome research.

[33]  J. Willis,et al.  A Simple Genetic Incompatibility Causes Hybrid Male Sterility in Mimulus , 2006, Genetics.

[34]  R. Scott,et al.  The Basis of Natural and Artificial Postzygotic Hybridization Barriers in Arabidopsis Species Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010496. , 2003, The Plant Cell Online.

[35]  Jonathan D. G. Jones,et al.  The Tomato Cf-2 Disease Resistance Locus Comprises Two Functional Genes Encoding Leucine-Rich Repeat Proteins , 1996, Cell.

[36]  Renate A Weizbauer,et al.  The Maternally Expressed WRKY Transcription Factor TTG2 Controls Lethality in Interploidy Crosses of Arabidopsis , 2008, PLoS biology.

[37]  K. Manly,et al.  Map Manager QTX, cross-platform software for genetic mapping , 2001, Mammalian Genome.

[38]  Jonathan D. G. Jones,et al.  A Tomato Cysteine Protease Required for Cf-2-Dependent Disease Resistance and Suppression of Autonecrosis , 2002, Science.

[39]  R. Sederoff,et al.  Genetics of Postzygotic Isolation in Eucalyptus: Whole-Genome Analysis of Barriers to Introgression in a Wide Interspecific Cross of Eucalyptus grandis and E. globulus , 2004, Genetics.

[40]  H. A. Orr,et al.  The population genetics of speciation: the evolution of hybrid incompatibilities. , 1995, Genetics.

[41]  L. Moyle,et al.  Genetics of Hybrid Incompatibility Between Lycopersicon esculentum and L. hirsutum , 2005, Genetics.

[42]  M. Matsuoka,et al.  Gain of deleterious function causes an autoimmune response and Bateson–Dobzhansky–Muller incompatibility in rice , 2010, Molecular Genetics and Genomics.

[43]  P. Laplace.  A Philosophical Essay On Probabilities , 1902 .

[44]  R. Visser,et al.  Rin4 Causes Hybrid Necrosis and Race-Specific Resistance in an Interspecific Lettuce Hybrid[W] , 2009, The Plant Cell Online.

[45]  U. Grossniklaus,et al.  Different Polycomb group complexes regulate common target genes in Arabidopsis , 2006, EMBO reports.