Evolution of the self-incompatibility system in the Brassicaceae: identification of S-locus receptor kinase (SRK) in self-incompatible Capsella grandiflora

Paetsch, Melanie; Mayland-Quellhorst, Sara; Neuffer, Barbara

doi:10.1038/sj.hdy.6800854

Cited by 60 publications

(57 citation statements)

References 34 publications

(43 reference statements)

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“…The C. grandiflora SRK7 and SCR7 genes (hereafter designated CgSRK7 and CgSCR7), which represent the first SRK-SCR gene pair identified in the Capsella species, contain all sequence motifs characteristic of SRK and SCR genes (Figure 3). The CgSRK7 sequence represents a new allele distinct from the partial C. grandiflora SRK sequences that have been reported recently (Paetsch et al 2006). BLAST searches show CgSRK7 and CgSCR7 to be most similar to the SRKa and SCRa genes of A. lyrata (Kusaba et al 2001).…”

Section: Resultsmentioning

confidence: 99%

Epigenetic Mechanisms for Breakdown of Self-Incompatibility in Interspecific Hybrids

et al. 2007

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As a major agent of rapid speciation, interspecific hybridization has played an important role in plant evolution. When hybridization involves species that exhibit self-incompatibility (SI), this prezygotic barrier to self-fertilization must be overcome or lost to allow selfing. How SI, a normally dominant trait, is lost in nascent hybrids is not known, however. Here we demonstrate that hybrid self-fertility can result from epigenetic changes in expression of the S-locus genes that determine specificity in the SI response. We analyzed loss of SI in synthetic hybrids produced by crossing self-fertile and self-incompatible species in each of two crucifer genera. We show that SI is lost in the stigmas of A. thaliana-lyrata hybrids and their neo-allotetraploid derivatives and in the pollen of C. rubella-grandiflora hybrids and their homoploid progenies. Aberrant processing of S-locus receptor kinase gene transcripts as detected in Arabidopsis hybrids and suppression of the S-locus cysteine-rich protein gene as observed in Capsella hybrids are two reversible mechanisms by which SI might break down upon interspecific hybridization to generate selffertile hybrids in nature.

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Section: Resultsmentioning

confidence: 99%

Epigenetic Mechanisms for Breakdown of Self-Incompatibility in Interspecific Hybrids

et al. 2007

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“…After binding, SRK activates a signaling pathway in the stigmatic papilla that rapidly rejects pollen by blocking pollen hydration or pollen tube penetration into the stigmatic surface (reviewed in Chapman and Goring, 2010;Ivanov et al, 2010). The SCR/SP11 and SRK genes are highly polymorphic, and alleles have been identified in other species, including A. lyrata (Kusaba et al, 2001;Schierup et al, 2001Schierup et al, , 2006Prigoda et al, 2005;Mable and Adam, 2007) and C. grandiflora (Paetsch et al, 2006;Boggs et al, 2009b;Guo et al, 2009). Downstream of SRK in the self-incompatibility pathway, there are two positive regulators that have been shown to interact with SRK, M locus Protein Kinase (MLPK) and the E3 ubiquitin ligase, ARM-Repeat Containing1 (ARC1) (Gu et al, 1998;Kakita et al, 2007aKakita et al, , 2007b.…”

Section: Introductionmentioning

confidence: 99%

The ARC1 E3 Ligase Promotes Two Different Self-Pollen Avoidance Traits inArabidopsis

2014

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Flowering plants have evolved various strategies for avoiding self-pollen to drive genetic diversity. These strategies include spatially separated sexual organs (herkogamy), timing differences between male pollen release and female pistil receptivity (dichogamy), and self-pollen rejection. Within the Brassicaceae, these outcrossing systems are the evolutionary default state, and many species display these traits, including Arabidopsis lyrata. In contrast to A. lyrata, closely related Arabidopsis thaliana has lost these self-pollen traits and thus represents an excellent system to test genes for reconstructing these evolutionary traits. We previously demonstrated that the ARC1 E3 ligase is required for self-incompatibility in two diverse Brassicaceae species, Brassica napus and A. lyrata, and is frequently deleted in self-compatible species, including A. thaliana. In this study, we examined ARC1's requirement for reconstituting self-incompatibility in A. thaliana and uncovered an important role for ARC1 in promoting a strong and stable pollen rejection response when expressed with two other A. lyrata self-incompatibility factors. Furthermore, we discovered that ARC1 promoted an approach herkogamous phenotype in A. thaliana flowers. Thus, ARC1's expression resulted in two different A. lyrata traits for self-pollen avoidance and highlights the key role that ARC1 plays in the evolution and retention of outcrossing systems.

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“…1). The breakdown of self-incompatibility is also associated with an expansion of geographic range; C. grandiflora is restricted to Western Greece and Albania and locally in Northern Italy, whereas C. rubella has expanded into much of southern Europe extending to Middle Europe, Northern Africa, and into Australia and North and South America (11,12). Interspecific crossing experiments suggest that, in addition to mating system evolution, there is considerable postpollination reproductive isolation between the species, with only a small proportion of crosses producing viable seed (refs.…”

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Recent speciation associated with the evolution of selfing inCapsella

Foxe

Slotte²,

Stahl³

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

247

325

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The evolution from outcrossing to predominant self-fertilization represents one of the most common transitions in flowering plant evolution. This shift in mating system is almost universally associated with the ''selfing syndrome,'' characterized by marked reduction in flower size and a breakdown of the morphological and genetic mechanisms that prevent self-fertilization. In general, the timescale in which these transitions occur, and the evolutionary dynamics associated with the evolution of the selfing syndrome are poorly known. We investigated the origin and evolution of selfing in the annual plant Capsella rubella from its self-incompatible, outcrossing progenitor Capsella grandiflora by characterizing multilocus patterns of DNA sequence variation at nuclear genes. We estimate that the transition to selfing and subsequent geographic expansion have taken place during the past 20,000 years. This transition was probably associated with a shift from stable equilibrium toward a nearcomplete population bottleneck causing a major reduction in effective population size. The timing and severe founder event support the hypothesis that selfing was favored during colonization as new habitats emerged after the last glaciation and the expansion of agriculture. These results suggest that natural selection for reproductive assurance can lead to major morphological evolution and speciation on relatively short evolutionary timescales.divergence population genetics ͉ reproductive assurance ͉ bottleneck ͉ selfing syndrome ͉ mating system evolution S elfing plants benefit from 2 distinct advantages over their outcrossing competitors (1-3). First, because selfers are 100% related to their progeny and can also act as outcross pollen donors for seed produced by other individuals, they have an inherent transmission advantage over outcrossers (4). A second major advantage conferred by selfing, first discussed by Darwin (5), is the ability to reproduce when pollinators or potential mates are limited (reproductive assurance). One important aspect of reproductive assurance is the ability of selfing lineages to colonize new habitats from a very small founding population. Evolutionary theory predicts that selfing will evolve when these advantages outweigh the costs associated with inbreeding depression, reduced fitness caused by increased homozygosity of deleterious recessive alleles (6).In most cases the timescale over which the selfing syndrome has evolved remains difficult to ascertain. In the model genus Arabidopsis, for example, the selfing Arabidopsis thaliana diverged from its closest outcrossing relatives Ϸ5 million years ago (7), and patterns of diversity have suggested a possibly complicated picture of the breakdown of outcrossing over a period of more than a million years (7,8). Thus, it remains unclear how rapidly the selfing syndrome can arise, and what historical conditions have favored mating system evolution. Capturing and characterizing a recent transition is important for inferring this timescale, and the relative import...

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Evolution of the self-incompatibility system in the Brassicaceae: identification of S-locus receptor kinase (SRK) in self-incompatible Capsella grandiflora

Cited by 60 publications

References 34 publications

Epigenetic Mechanisms for Breakdown of Self-Incompatibility in Interspecific Hybrids

Epigenetic Mechanisms for Breakdown of Self-Incompatibility in Interspecific Hybrids

The ARC1 E3 Ligase Promotes Two Different Self-Pollen Avoidance Traits inArabidopsis

Recent speciation associated with the evolution of selfing inCapsella

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