Interspecific reproductive barriers between sympatric populations of wild tomato species (<i>Solanum</i> section <i>Lycopersicon</i>)

Baek, You Soon; Royer, Suzanne M.; Broz, Amanda K.; Covey, Paul A.; López-Casado, Gloria; Nuñez, Reynaldo; Kear, Philip; Bonierbale, Merideth; Orillo, Matilde; Knaap, Esther van der; Stack, Stephên M.; McClure, Bruce; Chetelat, Roger T.; Bedinger, Patricia A.

doi:10.3732/ajb.1600356

Cited by 32 publications

(47 citation statements)

References 133 publications

(108 reference statements)

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“…This UI mechanism may also have ecological significance by preventing hybridization between related species. Populations of S. pennellii overlap with several other Solanum species, including S. pimpinellifolium , the pollen of which is also rejected by UI (Baek et al ., ). Tomatoes and other Solanum species provide rich sources of natural variation in reproductive traits to address these questions, to decipher the mechanisms of SI‐independent pollen rejection and to manipulate pollen compatibility for crop improvement.…”

Section: Discussionmentioning

confidence: 97%

A farnesyl pyrophosphate synthase gene expressed in pollen functions in S‐RNase‐independent unilateral incompatibility

Qin

Liu

et al. 2018

The Plant Journal

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SUMMARYMultiple independent and overlapping pollen rejection pathways contribute to unilateral interspecific incompatibility (UI). In crosses between tomato species, pollen rejection usually occurs when the female parent is self-incompatible (SI) and the male parent self-compatible (SC) (the 'SI 3 SC rule'). Additional, as yet unknown, UI mechanisms are independent of self-incompatibility and contribute to UI between SC species or populations. We identified a major quantitative trait locus on chromosome 10 (ui10.1) which affects pollen-side UI responses in crosses between cultivated tomato, Solanum lycopersicum, and Solanum pennellii LA0716, both of which are SC and lack S-RNase, the pistil determinant of S-specificity in Solanaceae. Here we show that ui10.1 is a farnesyl pyrophosphate synthase gene (FPS2) expressed in pollen. Expression is about 18-fold higher in pollen of S. pennellii than in S. lycopersicum. Pollen with the hypomorphic S. lycopersicum allele is selectively eliminated on pistils of the F 1 hybrid, leading to transmission ratio distortion in the F 2 progeny. CRISPR/Cas9-generated knockout mutants (fps2) in S. pennellii LA0716 are self-sterile due to pollen rejection, but mutant pollen is fully functional on pistils of S. lycopersicum. F 2 progeny of S. lycopersicum 3 S. pennellii (fps2) show reversed transmission ratio distortion due to selective elimination of pollen bearing the knockout allele. Overexpression of FPS2 in S. lycopersicum pollen rescues the pollen elimination phenotype. FPS2-based pollen selectivity does not involve S-RNase and has not been previously linked to UI. Our results point to an entirely new mechanism of interspecific pollen rejection in plants.

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Section: Discussionmentioning

confidence: 97%

A farnesyl pyrophosphate synthase gene expressed in pollen functions in S‐RNase‐independent unilateral incompatibility

Qin

Liu

et al. 2018

The Plant Journal

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“…Co‐variation between self and interspecific incompatibility has been observed across many closely related species of plants giving rise to the SI × SC rule (Lewis & Crowe, ). In some systems, SI and II are known to result from overlapping developmental and genetic mechanisms (Covey et al ., ; Bedinger et al ., ; Baek et al ., ). For example, loci contributing to unilateral incompatibility in Solanum co‐localize with the S‐locus (Chetelat & DeVerna, ; Bernacchi & Tanksley, ) and other loci known to mediate self‐incompatibility (Covey et al ., ).…”

Section: Discussionmentioning

confidence: 97%

“…Therefore, these systems may be good models for understanding the molecular basis of the SI × SC rule, but they cannot necessarily tell us if and how the shared molecular basis of self and interspecific incompatibility affect the evolution of these traits. By examining patterns of genetic variation in SI within a species, whether it is quantitative variation as in P. drummondii or qualitative as in most Solanum species (Baek et al ., , ), we can gain a better understanding of the factors influencing the evolution of incompatibilities.…”

Section: Discussionmentioning

confidence: 99%

Correlated evolution of self and interspecific incompatibility across the range of a Texas wildflower

Roda

Hopkins

2018

New Phytologist

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Selection to prevent interspecific mating can cause an increase or a decrease in self-pollination in sympatric populations. Characterizing the geographical variation in self and interspecific incompatibilities within a species can reveal if and how the evolution of self and interspecific mate choice are linked. We used controlled pollinations to characterize the variation in self and interspecific incompatibility across 29 populations of Phlox drummondii. We evaluated seed set from these pollinations and described the developmental timing of variation in pollen-pistil compatibility. There is extensive quantitative variation in self-incompatibility and interspecific-incompatibility with its close congener P. cuspidata. Phlox drummondii populations that co-occur and hybridize with P. cuspidata have significantly higher interspecific incompatibility and self-incompatibility than geographically isolated P. drummondii populations. The strength of self and interspecific incompatibility is significantly correlated among individuals and the strength of both incompatibilities is explained by the success of pollen adhesion to the stigma. The correlated strength of self and interspecific incompatibility across the range of P. drummondii and the concurrent developmental timing of the pollen-pistil interaction, suggests these incompatibilities have an overlapping molecular mechanism. The geographical distribution of variation in incompatibilities indicates that this mechanistic link between incompatibilities may affect the evolution of mate choice in plants.

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“…Wild tomatoes (Solanum section Lycopersicon) provide an excellent model system to study the incidence, evolution and consequences of imprinting in the endosperm; they diverged fairly recently (~2.5 Mya; Pease et al ., ), harbor a diversity of mating systems and exhibit various degrees of post‐zygotic isolation mediated by endosperm‐based hybrid seed failure (Baek et al ., ; Roth et al ., ). Unlike all other taxa that have been the focus of studies on endosperm genomic imprinting, Solanum is characterized by a cellular‐ rather than a nuclear‐type endosperm during early development.…”

Section: Introductionmentioning

confidence: 97%

Wild tomato endosperm transcriptomes reveal common roles of genomic imprinting in both nuclear and cellular endosperm

et al. 2018

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Genomic imprinting is a conspicuous feature of the endosperm, a triploid tissue nurturing the embryo and synchronizing angiosperm seed development. An unknown subset of imprinted genes (IGs) is critical for successful seed development and should have highly conserved functions. Recent genome-wide studies have found limited conservation of IGs among distantly related species, but there is a paucity of data from closely related lineages. Moreover, most studies focused on model plants with nuclear endosperm development, and comparisons with properties of IGs in cellular-type endosperm development are lacking. Using laser-assisted microdissection, we characterized parent-specific expression in the cellular endosperm of three wild tomato lineages (Solanum section Lycopersicon). We identified 1025 candidate IGs and 167 with putative homologs previously identified as imprinted in distantly related taxa with nuclear-type endosperm. Forty-two maternally expressed genes (MEGs) and 17 paternally expressed genes (PEGs) exhibited conserved imprinting status across all three lineages, but differences in power to assess imprinted expression imply that the actual degree of conservation might be higher than that directly estimated (20.7% for PEGs and 10.4% for MEGs). Regardless, the level of shared imprinting status was higher for PEGs than for MEGs, indicating dissimilar evolutionary trajectories. Expression-level data suggest distinct epigenetic modulation of MEGs and PEGs, and gene ontology analyses revealed MEGs and PEGs to be enriched for different functions. Importantly, our data provide evidence that MEGs and PEGs interact in modulating both gene expression and the endosperm cell cycle, and uncovered conserved cellular functions of IGs uniting taxa with cellular- and nuclear-type endosperm.

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Interspecific reproductive barriers between sympatric populations of wild tomato species (Solanum section Lycopersicon)

Abstract: We have identified diverse prezygotic and postzygotic IRBs that would prevent hybridization between sympatric wild tomato species, but interspecific hybridization is possible in a few cases.

Cited by 32 publications

References 133 publications

A farnesyl pyrophosphate synthase gene expressed in pollen functions in S‐RNase‐independent unilateral incompatibility

A farnesyl pyrophosphate synthase gene expressed in pollen functions in S‐RNase‐independent unilateral incompatibility

Correlated evolution of self and interspecific incompatibility across the range of a Texas wildflower

Wild tomato endosperm transcriptomes reveal common roles of genomic imprinting in both nuclear and cellular endosperm

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