Population-Specific Selection on Standing Variation Generated by Lateral Gene Transfers in a Grass

First author: Jill K. Olofsson; Affiliations: University of Sheffield (谢菲尔德大学): Sheffield, UK

Corresponding author: Pascal-Antoine Christin

Evidence of eukaryote-to-eukaryote lateral gene transfer (LGT) has accumulated in recent years, but the selective pressures governing the evolutionary fate of these genes within recipient species remain largely unexplored. Among non-parasitic plants, successful LGT has been reported between different grass species. Here, we use the grass Alloteropsis semialata, a species that possesses multigene LGT fragments that were acquired recently from distantly related grass species, to test the hypothesis that the successful LGT conferred an advantage and were thus rapidly swept into the recipient species. Combining whole-genome and population-level RAD sequencing, we show that the multigene LGT fragments were rapidly integrated in the recipient genome, likely due to positive selection for genes encoding proteins that added novel functions. These fragments also contained physically linked hitchhiking protein-coding genes, and subsequent genomic erosion has generated gene presence-absence polymorphisms that persist in multiple geographic locations, becoming part of the standing genetic variation. Importantly, one of the hitchhiking genes underwent a secondary rapid spread in some populations. This shows that eukaryotic LGT can have a delayed impact, contributing to local adaptation and intraspecific ecological diversification. Therefore, while short-term LGT integration is mediated by positive selection on some of the transferred genes, physically linked hitchhikers can remain functional and augment the standing genetic variation with delayed adaptive consequences.

近年来，不断有证据显示真核生物-真核生物的侧向基因转移LGT，但是控制这些基因在受体物种内演化命运的选择压仍然还不是很清楚。在非寄生植物中，已经有研究报道了不同草种之间的LGT。本文中，作者通过利用一种基因组上近期从远缘物种获取的多个基因的LGT片段的草种毛颖草（Alloteropsis semialata），测试了成功的LGT能够使得受体物种具有优势，并因此迅速席卷受体的假说。通过结合全基因组和群体水平的RAD测序，作者的研究显示多个基因的LGT片段迅速整合到了受体基因组中，这可能是由于对那些编码新功能蛋白的基因进行了正选择。这些片段还包含物理连锁的"搭便车"蛋白编码基因，随后的基因组侵蚀产生了基因存在/缺失多态性，该多态性持续存在于基因组上多个位置，成为遗传变异的一部分。重要的是，其中一个“搭便车”基因在某些群体中经历了二次快速传播。这表明真核LGT可能具有延迟效应，作用于局部适应和种内生态多样化。因此，尽管短期LGT整合是通过对某些转移基因的正选择来介导的，但物理连锁的“搭便车”基因仍可以保持功能、并增加了具有延迟性适应的遗传变异。

搭便车效应（hitchhiking）：Genetic hitchhiking, also called genetic draft or the hitchhiking effect, is when an allele changes frequency not because it itself is under natural selection, but because it is near another gene that is undergoing a selective sweep and that is on the same DNA chain. -- Wikipedia

遗传侵蚀（Genetic erosion）：Genetic erosion, also known as genetic depletion, is a process where the limited gene pool of an endangered species diminishes even more when reproductive individuals die off before reproducing with others in their endangered low population. -- Wikipedia

通讯：Pascal-Antoine Christin (https://www.sheffield.ac.uk/aps/staff-and-students/acadstaff/christinhttps://www.sheffield.ac.uk/aps/staff-and-students/acadstaff/christin)

个人简介：2005年，瑞士洛桑大学，硕士；2008年，瑞士洛桑大学；博士。

研究方向：植物如何在演化过程中获得复杂的性状；环境变化如何驱动植物演化出新的性状。

doi: https://doi.org/10.1016/j.cub.2019.09.023

Journal: Current Biology

Published date: October 31, 2019