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      Incidence and developmental timing of endosperm failure in post-zygotic isolation between wild tomato lineages

      , , , ,
      Annals of Botany
      Oxford University Press (OUP)

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          Abstract

          <div class="section"> <a class="named-anchor" id="s1"> <!-- named anchor --> </a> <h5 class="section-title" id="d1018981e148">Background and Aims</h5> <p id="d1018981e150">Defective hybrid seed development in angiosperms might mediate the rapid establishment of intrinsic post-zygotic isolation between closely related species. Extensive crosses within and among three lineages of wild tomatoes ( <i>Solanum</i> section <i>Lycopersicon</i>) were performed to address the incidence, developmental timing and histological manifestations of hybrid seed failure. These lineages encompass different, yet fairly recent, divergence times and both allopatric and partially sympatric pairs. </p> </div><div class="section"> <a class="named-anchor" id="s2"> <!-- named anchor --> </a> <h5 class="section-title" id="d1018981e159">Methods</h5> <p id="d1018981e161">Mature seeds were scored visually 2 months after hand pollinations, and viable-looking seeds were assessed for germination success. Using histological sections from early-developing seeds from a sub-set of crosses, the growth of three major seed compartments (endosperm, embryo and seed coat) was measured at critical developmental stages up to 21 d after pollination, with a focus on the timing and histological manifestations of endosperm misdevelopment in abortive hybrid seeds. </p> </div><div class="section"> <a class="named-anchor" id="s3"> <!-- named anchor --> </a> <h5 class="section-title" id="d1018981e164">Key Results</h5> <p id="d1018981e166">For two of three interspecific combinations including the most closely related pair that was also studied histologically, almost all mature seeds appeared ‘flat’ and proved inviable; histological analyses revealed impaired endosperm proliferation at early globular embryo stages, concomitant with embryo arrest and seed abortion in both cross directions. The third interspecific combination yielded a mixture of flat, inviable and plump, viable seeds; many of the latter germinated and exhibited near-normal juvenile phenotypes or, in some instances, hybrid necrosis and impaired growth. </p> </div><div class="section"> <a class="named-anchor" id="s4"> <!-- named anchor --> </a> <h5 class="section-title" id="d1018981e169">Conclusions</h5> <p id="d1018981e171">The overall results suggest that near-complete hybrid seed failure can evolve fairly rapidly and without apparent divergence in reproductive phenology/biology. While the evidence accrued here is largely circumstantial, early-acting disruptions of normal endosperm development are most probably the common cause of seed failure regardless of the type of endosperm (nuclear or cellular). </p> </div>

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          Phylogenomics Reveals Three Sources of Adaptive Variation during a Rapid Radiation

          Speciation events often occur in rapid bursts of diversification, but the ecological and genetic factors that promote these radiations are still much debated. Using whole transcriptomes from all 13 species in the ecologically and reproductively diverse wild tomato clade (Solanum sect. Lycopersicon), we infer the species phylogeny and patterns of genetic diversity in this group. Despite widespread phylogenetic discordance due to the sorting of ancestral variation, we date the origin of this radiation to approximately 2.5 million years ago and find evidence for at least three sources of adaptive genetic variation that fuel diversification. First, we detect introgression both historically between early-branching lineages and recently between individual populations, at specific loci whose functions indicate likely adaptive benefits. Second, we find evidence of lineage-specific de novo evolution for many genes, including loci involved in the production of red fruit color. Finally, using a “PhyloGWAS” approach, we detect environment-specific sorting of ancestral variation among populations that come from different species but share common environmental conditions. Estimated across the whole clade, small but substantial and approximately equal fractions of the euchromatic portion of the genome are inferred to contribute to each of these three sources of adaptive genetic variation. These results indicate that multiple genetic sources can promote rapid diversification and speciation in response to new ecological opportunity, in agreement with our emerging phylogenomic understanding of the complexity of both ancient and recent species radiations.
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            Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species.

            Ecological factors, hybrid sterility and differences in ploidy levels are well known for contributing to gene-flow barriers in plants. Another common postzygotic incompatibility, hybrid necrosis, has received comparatively little attention in the evolutionary genetics literature. Hybrid necrosis is associated with a suite of phenotypic characteristics that are similar to those elicited in response to various environmental stresses, including pathogen attack. The genetic architecture is generally simple, and complies with the Bateson-Dobzhansky-Muller model for hybrid incompatibility between species. We survey the extensive literature on this topic and present the hypothesis that hybrid necrosis can result from autoimmunity, perhaps as a pleiotropic effect of evolution of genes that are involved in pathogen response.
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              The origins of reproductive isolation in plants.

              Reproductive isolation in plants occurs through multiple barriers that restrict gene flow between populations, but their origins remain uncertain. Work in the past decade has shown that postpollination barriers, such as the failure to form hybrid seeds or sterility of hybrid offspring, are often less strong than prepollination barriers. Evidence implicates multiple evolutionary forces in the origins of reproductive barriers, including mutation, stochastic processes and natural selection. Although adaptation to different environments is a common element of reproductive isolation, genomic conflicts also play a role, including female meiotic drive. The genetic basis of some reproductive barriers, particularly flower colour influencing pollinator behaviour, is well understood in some species, but the genetic changes underlying many other barriers, especially pollen-stylar interactions, are largely unknown. Postpollination barriers appear to accumulate at a faster rate in annuals compared with perennials, due in part to chromosomal rearrangements. Chromosomal changes can be important isolating barriers in themselves but may also reduce the recombination of genes contributing to isolation. Important questions for the next decade include identifying the evolutionary forces responsible for chromosomal rearrangements, determining how often prezygotic barriers arise due to selection against hybrids, and establishing the relative importance of genomic conflicts in speciation.
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                Author and article information

                Journal
                Annals of Botany
                Oxford University Press (OUP)
                0305-7364
                1095-8290
                January 2018
                January 25 2018
                December 21 2017
                January 2018
                January 25 2018
                December 21 2017
                : 121
                : 1
                : 107-118
                Article
                10.1093/aob/mcx133
                5786209
                29280998
                6684cce1-c7c4-4864-8560-de5b389f608f
                © 2017
                History

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