Benítez-Benítez Carmen, Mohan Ashwini V, Sánchez-Villegas Rogelio, Gómez-Ramos Inés, Valdés-Florido Ana, Lucek Kay, Slovák Marek, Kolář Filip, Leitch Ilia J, Luceño Modesto, Larridon Isabel, Carta Angelino, Cuscó-Borràs Joan, Maguilla Enrique, Montero-Ramírez Alegría, Meirmans Patrick G, Scott Alison Dawn, Martín-Bravo Santiago, Escudero Marcial
Botany Area, Department of Plant Biology and Ecology, Faculty of Biology, University of Seville, Seville, Spain.
Biodiversity Genomics Laboratory, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland.
Front Plant Sci. 2025 Aug 22;16:1606450. doi: 10.3389/fpls.2025.1606450. eCollection 2025.
Understanding the relationship between macro- and microevolutionary processes and their delimitation remains a challenge. This review focuses on the role of chromosomal rearrangements in plant population differentiation and lineage diversification resulting in speciation, helping bridge the gap between macro- and microevolution through chromosomal evolution. We focus on angiosperms, a group that comprises the majority of extant plant species diversity and exhibits the largest chromosomal and genomic variations. Here, we address the following questions: Are macroevolutionary patterns of chromosome evolution the result of accumulated microevolutionary changes, or do chromosomal dynamics drive larger shifts along the speciation continuum? At the macroevolutionary level, we investigated the association between karyotype diversity and diversification rates using evidence from comparative genomics, chromosomal evolution modelling across phylogenies, and the association with several traits across different angiosperm lineages. At the microevolutionary level, we explore if different karyotypes are linked to morphological changes and population genetic differentiation in the same lineages. Polyploidy (autopolyploidy and allopolyploidy) and dysploidy are known drivers of speciation, with karyotypic differences often leading to reproductive barriers. We found that dysploidy, involving gains and losses of single chromosomes with no significant change in overall content of the genome, appears to be relatively more frequent and persistent across macroevolutionary histories than polyploidy. Additionally, chromosomal rearrangements that do not entail change in chromosome number, such as insertions, deletions, inversions, and duplications of chromosome fragments, as well as translocations between chromosomes, are increasingly recognized for their role in local adaptation and speciation. We argue that there is more evidence linking chromosomal rearrangements with genetic and morphological trait differentiation at microevolutionary scales than at macroevolutionary ones. Our findings highlight the importance of selection across evolutionary scales, where certain chromosomal dynamics become fixed over macroevolutionary time. Consequently, at microevolutionary scales, chromosome rearrangements are frequent and diverse, serving as key drivers of plant diversification and adaptation by providing a pool of variation from which beneficial chromosomal changes can be selected and fixed by evolutionary forces.
理解宏观和微观进化过程之间的关系及其界定仍然是一项挑战。本综述聚焦于染色体重排在植物种群分化和谱系多样化（导致物种形成）中的作用，通过染色体进化帮助弥合宏观和微观进化之间的差距。我们关注被子植物，这一群体包含了现存植物物种多样性的大部分，并且展现出最大的染色体和基因组变异。在此，我们探讨以下问题：染色体进化的宏观进化模式是微观进化变化积累的结果，还是染色体动态变化推动了沿着物种形成连续统的更大转变？在宏观进化层面，我们利用比较基因组学的证据、跨系统发育的染色体进化建模以及与不同被子植物谱系中若干性状的关联，研究了核型多样性与多样化速率之间的关联。在微观进化层面，我们探究同一谱系中不同核型是否与形态变化和种群遗传分化相关联。多倍体（同源多倍体和异源多倍体）和非整倍体是已知的物种形成驱动因素，核型差异常常导致生殖隔离。我们发现，涉及单条染色体增减而基因组总体含量无显著变化的非整倍体，在宏观进化历史中似乎比多倍体更为频繁和持久。此外，不涉及染色体数目变化的染色体重排，如染色体片段的插入、缺失、倒位和重复，以及染色体之间的易位，因其在局部适应和物种形成中的作用而越来越受到认可。我们认为，在微观进化尺度上，将染色体重排与遗传和形态性状分化联系起来的证据比在宏观进化尺度上更多。我们的研究结果凸显了跨进化尺度选择的重要性，在宏观进化时间里某些染色体动态变化得以固定。因此，在微观进化尺度上，染色体重排频繁且多样，通过提供一个变异库，从中有益的染色体变化可被进化力量选择和固定，从而成为植物多样化和适应的关键驱动因素。
