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Interspecific crossing and genetic mapping reveal intrinsic genomic incompatibility between two Senecio species that form a hybrid zone on Mount Etna, Sicily.

ABSTRACT: Studies of hybridizing species can reveal much about the genetic basis and maintenance of species divergence in the face of gene flow. Here we report a genetic segregation and linkage analysis conducted on F2 progeny of a reciprocal cross between Senecio aethnensis and S. chrysanthemifolius that form a hybrid zone on Mount Etna, Sicily, aimed at determining the genetic basis of intrinsic hybrid barriers between them. Significant transmission ratio distortion (TRD) was detected at 34 (?27%) of 127 marker loci located in nine distinct clusters across seven of the ten linkage groups detected, indicating genomic incompatibility between the species. TRD at these loci could not be attributed entirely to post-zygotic selective loss of F2 individuals that failed to germinate or flower (16.7%). At four loci tests indicated that pre-zygotic events, such as meiotic drive in F1 parents or gametophytic selection, contributed to TRD. Additional tests revealed that cytonuclear incompatibility contributed to TRD at five loci, Bateson-Dobzhansky-Muller (BDM) incompatibilities involving epistatic interactions between loci contributed to TRD at four loci, and underdominance (heterozygote disadvantage) was a possible cause of TRD at one locus. Major chromosomal rearrangements were probably not a cause of interspecific incompatibility at the scale that could be examined with current map marker density. Intrinsic genomic incompatibility between S. aethnensis and S. chrysanthemifolius revealed by TRD across multiple genomic regions in early-generation hybrids is likely to impact the genetic structure of the natural hybrid zone on Mount Etna by limiting introgression and promoting divergence across the genome.

SUBMITTER: Brennan AC

PROVIDER: S-EPMC4815642 | biostudies-literature | 2014 Sep

REPOSITORIES: biostudies-literature

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Interspecific crossing and genetic mapping reveal intrinsic genomic incompatibility between two Senecio species that form a hybrid zone on Mount Etna, Sicily.

Brennan A C AC Hiscock S J SJ Abbott R J RJ

Heredity 20140305 3

Studies of hybridizing species can reveal much about the genetic basis and maintenance of species divergence in the face of gene flow. Here we report a genetic segregation and linkage analysis conducted on F2 progeny of a reciprocal cross between Senecio aethnensis and S. chrysanthemifolius that form a hybrid zone on Mount Etna, Sicily, aimed at determining the genetic basis of intrinsic hybrid barriers between them. Significant transmission ratio distortion (TRD) was detected at 34 (∼27%) of 12 ...[more]

PMID: 24595365

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Project description:Changes in growth forms frequently accompany plant adaptive radiations, including páramo-a high-elevation treeless habitat type of the northern Andes. We tested whether diverse group of Senecio inhabiting montane forests and páramo represented such growth form changes. We also investigated the role of Andean geography and environment in structuring genetic variation of this group. We sampled 108 populations and 28 species of Senecio (focusing on species from former genera Lasiocephalus and Culcitium) and analyzed their genetic relationships and patterns of intraspecific variation using DNA fingerprinting (AFLPs) and nuclear DNA sequences (ITS). We partitioned genetic variation into environmental and geographical components. ITS-based phylogeny supported monophyly of a Lasiocephalus-Culcitium clade. A grade of herbaceous alpine Senecio species subtended the Lasiocephalus-Culcitium clade suggesting a change from the herbaceous to the woody growth form. Both ITS sequences and the AFLPs separated a group composed of the majority of páramo subshrubs from other group(s) comprising both forest and páramo species of various growth forms. These morphologically variable group(s) further split into clades encompassing both the páramo subshrubs and forest lianas, indicating independent switches among the growth forms and habitats. The finest AFLP genetic structure corresponded to morphologically delimited species except in two independent cases in which patterns of genetic variation instead reflected geography. Several morphologically variable species were genetically admixed, which suggests possible hybrid origins. Latitude and longitude accounted for 5%-8% of genetic variation in each of three AFLP groups, while the proportion of variation attributed to environment varied between 8% and 31% among them. A change from the herbaceous to the woody growth form is suggested for species of high-elevation Andean Senecio. Independent switches between habitats and growth forms likely occurred within the group. Hybridization likely played an important role in species diversification.

Project description:BackgroundPollen-pistil interactions are an essential prelude to fertilization in angiosperms and determine compatibility/incompatibility. Pollen-pistil interactions have been studied at a molecular and cellular level in relatively few families. Self-incompatibility (SI) is the best understood pollen-pistil interaction at a molecular level where three different molecular mechanisms have been identified in just five families. Here we review studies of pollen-pistil interactions and SI in the Asteraceae, an important family that has been relatively understudied in these areas of reproductive biology.ScopeWe begin by describing the historical literature which first identified sporophytic SI (SSI) in species of Asteraceae, the SI system later identified and characterized at a molecular level in the Brassicaceae. Early structural and cytological studies in these two families suggested that pollen-pistil interactions and SSI were similar, if not the same. Recent cellular and molecular studies in Senecio squalidus (Oxford ragwort) have challenged this belief by revealing that despite sharing the same genetic system of SSI, the Brassicaceae and Asteraceae molecular mechanisms are different. Key cellular differences have also been highlighted in pollen-stigma interactions, which may arise as a consequence of the Asteraceae possessing a 'semi-dry' stigma, rather than the 'dry' stigma typical of the Brassicaceae. The review concludes with a summary of recent transcriptomic analyses aimed at identifying proteins regulating pollen-pistil interactions and SI in S. squalidus, and by implication the Asteraceae. The Senecio pistil transcriptome contains many novel pistil-specific genes, but also pistil-specific genes previously shown to play a role in pollen-pistil interactions in other species.ConclusionsStudies in S. squalidus have shown that stigma structure and the molecular mechanism of SSI in the Asteraceae and Brassicaceae are different. The availability of a pool of pistil-specific genes for S. squalidus offers an opportunity to elucidate the molecular mechanisms of pollen-pistil interactions and SI in the Asteraceae.

Dataset Information

Interspecific crossing and genetic mapping reveal intrinsic genomic incompatibility between two Senecio species that form a hybrid zone on Mount Etna, Sicily.

Publications

Interspecific crossing and genetic mapping reveal intrinsic genomic incompatibility between two Senecio species that form a hybrid zone on Mount Etna, Sicily.

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