Dataset Information

The genetic breakdown of sporophytic self-incompatibility in Tolpis coronopifolia (Asteraceae).

ABSTRACT: Angiosperm diversity has been shaped by mating system evolution, with the most common transition from outcrossing to self-fertilizing. To investigate the genetic basis of this transition, we performed crosses between two species endemic to the Canary Islands, the self-compatible (SC) species Tolpis coronopifolia and its self-incompatible (SI) relative Tolpis santosii. We scored self-compatibility as self-seed set of recombinant plants within two F2 populations. To map and genetically characterize the breakdown of SI, we built a draft genome sequence of T. coronopifolia, genotyped F2 plants using multiplexed shotgun genotyping (MSG), and located MSG markers to the genome sequence. We identified a single quantitative trait locus (QTL) that explains nearly all variation in self-seed set in both F2 populations. To identify putative causal genetic variants within the QTL, we performed transcriptome sequencing on mature floral tissue from both SI and SC species, constructed a transcriptome for each species, and then located each predicted transcript to the T. coronopifolia genome sequence. We annotated each predicted gene within the QTL and found two strong candidates for SI breakdown. Each gene has a coding sequence insertion/deletion mutation within the SC species that produces a truncated protein. Homologs of each gene have been implicated in pollen development, pollen germination, and pollen tube growth in other species.

SUBMITTER: Koseva B

PROVIDER: S-EPMC5675808 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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The genetic breakdown of sporophytic self-incompatibility in Tolpis coronopifolia (Asteraceae).

Koseva Boryana B Crawford Daniel J DJ Brown Keely E KE Brown Keely E KE Mort Mark E ME Kelly John K JK

The New phytologist 20170911 4

Angiosperm diversity has been shaped by mating system evolution, with the most common transition from outcrossing to self-fertilizing. To investigate the genetic basis of this transition, we performed crosses between two species endemic to the Canary Islands, the self-compatible (SC) species Tolpis coronopifolia and its self-incompatible (SI) relative Tolpis santosii. We scored self-compatibility as self-seed set of recombinant plants within two F<sub>2</sub> populations. To map and genetically ...[more]

PMID: 28892151

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Project description:The Cichorium genus offers a unique opportunity to study the sporophytic self-incompatibility (SSI) system, being composed of species characterized by highly efficient self-incompatibility (e.g., C. intybus) and complete self-compatibility (e.g., C. endivia). To this end, the chicory genome was used to map seven previously identified SSI locus-associated markers. The region containing the S-locus was therefore restricted to an ~4 M bp window on chromosome 5. Among the genes predicted in this region, MDIS1 INTERACTING RECEPTOR LIKE KINASE 2 (ciMIK2) was particularly promising as a candidate for SSI. Its ortholog in Arabidopsis (atMIK2) is involved in pollen-stigma recognition reactions, and its protein structure is similar to that of S-receptor kinase (SRK), a key component of the SSI system in the Brassica genus. The amplification and sequencing of MIK2 in chicory and endive accessions revealed two contrasting scenarios. In C. endivia, MIK2 was fully conserved even when comparing different botanical varieties (i.e., smooth and curly endive). In C. intybus, 387 polymorphic positions and 3 INDELs were identified when comparing accessions of different biotypes all belonging to the same botanical variety (i.e., radicchio). The polymorphism distribution throughout the gene was uneven, with hypervariable domains preferentially localized in the LRR-rich extracellular region, putatively identified as the receptor domain. The gene was hypothesized to be under positive selection, as the nonsynonymous mutations were more than double the synonymous ones (dN/dS = 2.17). An analogous situation was observed when analyzing the first 500 bp of the MIK2 promoter: no SNPs were observed among the endive samples, whereas 44 SNPs and 6 INDELs were detected among the chicory samples. Further analyses are needed to confirm the role of MIK2 in SSI and to demonstrate whether the 23 species-specific nonsynonymous SNPs in the CDS and/or the species-specific 10 bp-INDEL found in a CCAAT box region of the promoter are responsible for the contrasting sexual behaviors of chicory and endive.

Project description:Background and aimsSporophytic self-incompatibility (SI) prevents inbreeding in many members of the Brassicaceae, and has been well documented in a variety of high-profile species. Arabis alpina is currently being developed as a model system for studying the ecological genetics of arctic-alpine environments, and is the focus of numerous studies on population structure and alpine phylogeography. Although it is highly inbreeding throughout most of its range, populations in central Italy have been identified that show inbreeding coefficients (F(IS)) more typical of self-incompatible relatives. The purpose of this study was to establish whether this variation is due to a functioning SI system.MethodsOutcrossing rate estimates were calculated based on 16 allozyme loci and self-compatibility assessed based on controlled pollinations for six Italian populations that have previously been shown to vary in F(IS) values. Putative SRK alleles (the gene controlling the female component of SI in other Brassicaceae) amplified from A. alpina were compared with those published for other species. Linkage of putative SRK alleles and SI phenotypes was assessed using a diallel cross.Key resultsFunctional avoidance of inbreeding is demonstrated in three populations of A. alpina, corresponding with previous F(IS) values. The presence is described of 15 putative SRK-like alleles, which show high sequence identity to known alleles from Brassica and Arabidopsis and the high levels of synonymous and nonsynonymous variation typical of genes under balancing selection. Also, orthologues of two other members of the S-receptor kinase gene family, Aly8 (ARK3) and Aly9 (AtS1) are identified. Further to this, co-segregation between some of the putative S-alleles and compatibility phenotypes was demonstrated using a full-sibling cross design.ConclusionsThe results strongly suggest that, as with other species in the Brassicaceae, A. alpina has a sporophytic SI system but shows variation in the strength of SI within and between populations.

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

The genetic breakdown of sporophytic self-incompatibility in Tolpis coronopifolia (Asteraceae).

Publications

The genetic breakdown of sporophytic self-incompatibility in Tolpis coronopifolia (Asteraceae).

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