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      Molecular insights into self-incompatibility systems: From evolution to breeding

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          Abstract

          Plants have evolved diverse self-incompatibility (SI) systems for outcrossing. Since Darwin’s time, considerable progress has been made toward elucidating this unrivaled reproductive innovation. Recent advances in interdisciplinary studies and applications of biotechnology have given rise to major breakthroughs in understanding the molecular pathways that lead to SI, particularly the strikingly different SI mechanisms that operate in Solanaceae, Papaveraceae, Brassicaceae, and Primulaceae. These best-understood SI systems, together with discoveries in other “nonmodel” SI taxa such as Poaceae, suggest a complex evolutionary trajectory of SI, with multiple independent origins and frequent and irreversible losses. Extensive exploration of self-/nonself-discrimination signaling cascades has revealed a comprehensive catalog of male and female identity genes and modifier factors that control SI. These findings also enable the characterization, validation, and manipulation of SI-related factors for crop improvement, helping to address the challenges associated with development of inbred lines. Here, we review current knowledge about the evolution of SI systems, summarize key achievements in the molecular basis of pollen‒pistil interactions, discuss potential prospects for breeding of SI crops, and raise several unresolved questions that require further investigation.

          Abstract

          Self-incompatibility (SI) is an intraspecific reproductive barrier that promotes outbreeding. Molecular interactions between male and female S determinants trigger multiple signaling cascades and cellular events that lead to rejection of self-pollen and prevention of self-fertilization. Characterization of identity genes and modifier factors that control the SI response is crucial to understanding the complex evolutionary trajectories and breakdown of SI and provides guidance for SI crop breeding using biotechnology.

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          Most cited references265

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          An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV

          (2016)
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            Comparative analysis of the receptor-like kinase family in Arabidopsis and rice.

            Receptor-like kinases (RLKs) belong to the large RLK/Pelle gene family, and it is known that the Arabidopsis thaliana genome contains >600 such members, which play important roles in plant growth, development, and defense responses. Surprisingly, we found that rice (Oryza sativa) has nearly twice as many RLK/Pelle members as Arabidopsis does, and it is not simply a consequence of a larger predicted gene number in rice. From the inferred phylogeny of all Arabidopsis and rice RLK/Pelle members, we estimated that the common ancestor of Arabidopsis and rice had >440 RLK/Pelles and that large-scale expansions of certain RLK/Pelle members and fusions of novel domains have occurred in both the Arabidopsis and rice lineages since their divergence. In addition, the extracellular domains have higher nonsynonymous substitution rates than the intracellular domains, consistent with the role of extracellular domains in sensing diverse signals. The lineage-specific expansions in Arabidopsis can be attributed to both tandem and large-scale duplications, whereas tandem duplication seems to be the major mechanism for recent expansions in rice. Interestingly, although the RLKs that are involved in development seem to have rarely been duplicated after the Arabidopsis-rice split, those that are involved in defense/disease resistance apparently have undergone many duplication events. These findings led us to hypothesize that most of the recent expansions of the RLK/Pelle family have involved defense/resistance-related genes.
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              The evolution of plant sexual diversity.

              Charles Darwin recognized that flowering plants have an unrivalled diversity of sexual systems. Determining the ecological and genetic factors that govern sexual diversification in plants is today a central problem in evolutionary biology. The integration of phylogenetic, ecological and population-genetic studies have provided new insights into the selective mechanisms that are responsible for major evolutionary transitions between reproductive modes.
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                Author and article information

                Contributors
                Journal
                Plant Commun
                Plant Commun
                Plant Communications
                Elsevier
                2590-3462
                16 September 2023
                12 February 2024
                16 September 2023
                : 5
                : 2
                : 100719
                Affiliations
                [1 ]Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, Fujian Agriculture and Forestry University, Fuzhou 350002, China
                [2 ]College of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002, China
                [3 ]College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, China
                Author notes
                []Corresponding author lkzx@ 123456fafu.edu.cn
                [∗∗ ]Corresponding author yinwl@ 123456bjfu.edu.cn
                [∗∗∗ ]Corresponding author zjliu@ 123456fafu.edu.cn
                Article
                S2590-3462(23)00265-1 100719
                10.1016/j.xplc.2023.100719
                10873884
                37718509
                89f7acdd-521a-4352-a21a-72283011431b
                © 2023 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 29 March 2023
                : 18 August 2023
                : 13 September 2023
                Categories
                Review Article

                self-incompatibility,s-rnase,evolution,genome editing,crop improvement

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