Costa Lucas, Castro Natália, Buddenhagen Christopher E, Marques André, Pedrosa-Harand Andrea, Souza Gustavo
Laboratory of Plant Cytogenetics and Evolution, Department of Botany, Federal University of Pernambuco, Recife-PE, Brazil.
AgResearch, Ruakura Research Centre, Hamilton, New Zealand.
Ann Bot. 2025 May 9;135(5):909-924. doi: 10.1093/aob/mcae220.
Genomic changes triggered by polyploidy, chromosomal rearrangements and/ or environmental stress are among factors that affect the activity of mobile elements, particularly long terminal repeat retrotransposons (LTR-RTs) and DNA transposons. Because these elements can proliferate and move throughout host genomes, altering the genetic, epigenetic and nucleotypic landscape, they have been recognized as a relevant evolutionary force. Beaksedges (Rhynchospora) stand out for their wide cosmopolitan distribution, high diversity (~400 species) and holocentric chromosomes related to high karyotypic diversity and a centromere-specific satDNA, Tyba. This makes the genus an interesting model to investigate the interactions between repetitive elements, phylogenetic relationships and ecological variables.
Here we used comparative phylogenetic methods to investigate the forces driving the evolution of the entire set of mobile elements (mobilome) in the holocentric genus Rhynchospora. We statistically tested the impact of phylogenetic relationships, abundance of holocentromeric satDNA Tyba, diversity of repeatome composition, ecological variables and chromosome number in mobile element diversification.
Tyba abundance was found to be inversely correlated with LTR-RT content. Decrease of LTR abundance and diversity was also related to increase in chromosome number (likely due to fission events) and colonization of dry environments in the northern hemisphere. In contrast, we found constant LTR insertions throughout time in species with lower chromosome numbers in rainier environments in South America. A multivariate model showed that different traits drive LTR abundance, especially repeat diversity and Tyba abundance. Other mobile elements, such as non-LTR RTs and DNA transposons, had insufficient abundance to be included in our models.
Our findings suggest that LTR evolution is strongly impacted by the holocentric characteristics of Rhynchospora chromosomes, correlating with species diversification and biome shifts, and supporting a holokinetic drive model of evolution and a competitive scenario with Tyba. Altogether, our results present evidence of multi-trait influence on LTR-RT dynamics and provide a broader understanding of transposable element evolution in a macroevolutionary context.
多倍体、染色体重排和/或环境胁迫引发的基因组变化是影响移动元件活性的因素之一，尤其是长末端重复逆转座子（LTR-RTs）和DNA转座子。由于这些元件能够在宿主基因组中增殖和移动，改变遗传、表观遗传和核型格局，它们已被视为一种重要的进化力量。喙莎草属（Rhynchospora）以其广泛的全球分布、高多样性（约400种）以及与高核型多样性和着丝粒特异性卫星DNA（Tyba）相关的全着丝粒染色体而闻名。这使得该属成为研究重复元件、系统发育关系和生态变量之间相互作用的有趣模型。
在此，我们使用比较系统发育方法来研究驱动全着丝粒属喙莎草移动元件全集（移动基因组）进化的力量。我们对系统发育关系、全着丝粒卫星DNA Tyba的丰度、重复基因组组成的多样性、生态变量和染色体数目对移动元件多样化的影响进行了统计检验。
发现Tyba丰度与LTR-RT含量呈负相关。LTR丰度和多样性的降低也与染色体数目的增加（可能由于裂变事件）以及北半球干旱环境的定殖有关。相比之下，我们发现在南美洲降雨较多环境中染色体数目较少的物种中，LTR插入在整个时间内保持恒定。一个多变量模型表明，不同特征驱动LTR丰度，尤其是重复多样性和Tyba丰度。其他移动元件，如非LTR逆转座子和DNA转座子，丰度不足，无法纳入我们的模型。
我们的研究结果表明，LTR进化受到喙莎草染色体全着丝粒特征的强烈影响，与物种多样化和生物群落转变相关，并支持进化的全动粒驱动模型以及与Tyba的竞争场景。总之，我们的结果提供了多性状对LTR-RT动态影响的证据，并在宏观进化背景下对转座元件进化提供了更广泛的理解。
