Paternally expressed imprinted genes associate with hybridization barriers in Capsella

First author: Clément Lafon-Placette; Affiliations: Swedish University of Agricultural Sciences (瑞典农业科学大学): Uppsala, Sweden

Corresponding author: Claudia Köhler

Hybrid seed lethality (致死性) is a widespread type of reproductive barrier (生殖障碍) among angiosperm taxa that contributes to species divergence by preventing gene flow (基因流) between natural populations. Besides its ecological importance, it is an important obstacle (障碍) to plant breeding strategies. Hybrid seed lethality is mostly due to a failure of the nourishing endosperm tissue (胚乳组织), resulting in embryo arrest (停止). The cause of this failure is a parental dosage imbalance (剂量失衡) in the endosperm that can be a consequence of either differences in parental ploidy levels or differences in the 'effective ploidy', also known as the endosperm balance number (EBN; 胚乳平衡数). Hybrid seed defects exhibit a parent-of-origin pattern, suggesting that differences in number or expression strength of parent-of-origin-specific imprinted genes underpin, as the primary or the secondary cause, the molecular basis of the EBN. Here, we have tested this concept in the genus Capsella (荠属) and show that the effective ploidy of three Capsella species correlates with the number and expression level of paternally expressed genes (PEGs). Importantly, the number of PEGs and the effective ploidy decrease with the selfing history of a species: the obligate outbreeder (专性异交) Capsella grandiflora had the highest effective ploidy, followed by the recent selfer Capsella rubella and the ancient selfer Capsella orientalis. PEGs were associated with the presence of transposable elements and their silencing mark, DNA methylation in CHH context (where H denotes any base except C). This suggests that transposable elements have driven the imprintome divergence between Capsella species. Together, we propose that variation in transposable element insertions, the resulting differences in PEG number and divergence in their expression level form one component of the effective ploidy variation between species of different breeding system histories, and, as a consequence, allow the establishment of endosperm-based hybridization barriers.

杂交种子致死是被子植物物种广泛存在的生殖障碍类型，可以防止自然群体之间的基因流，从而促进物种分化。除了生态学上的重要作用，杂交种子致死还是植物育种策略中的重要障碍。杂交种子致死大多是由于供给营养的胚乳组织发育缺陷，导致了胚的发育停止。这种缺陷是亲本在胚乳中的计量失衡，可能是由亲本倍性的差异或是有效倍性，即胚乳平衡数的差异所导致的。杂交种子缺陷存在亲本起源的模式，表明来源于亲本特异的印记基因的数量或表达强度作为主要原因或者次要原因，作用于胚乳平衡数差异的分子机制。本文研究了荠属植物中这一问题，结果显示三个荠属植物的有效倍性与亲本表达基因PEG的数量和表达水平相关。重要的是，PEG的数量和有效倍性随着物种自交历史的时间降低，专性异交的Capsella grandiflora具有最高的有效倍性，随后就是最近开始自交的Capsella rubella和很早以前就开始自交的Capsella orientalis。PEG与转座元件的出现及其沉默标记，即位于CHH上的甲基化相关，说明转座元件驱动了荠属植物之间印迹组的分化。综上，作者提出转座元件插入的变异，及其导致的具有不同育种系统历史的物种之间有效倍性变异的组分之一PEG数量和表达水平的分化，二者共同建立起了基于胚乳的杂交障碍。

通讯：Claudia Köhler (http://kohlerlab.se/people/claudia-kohler/)

个人简介：1999年，德国弗莱堡大学，植物细胞生物学博士；1999-2000年，德国弗莱堡大学，植物细胞生物学博士后；2000-2003年，瑞士苏黎世大学，植物发育遗传学博士后；2003-2005年，瑞士苏黎世大学，植物发育遗传学助理教授；2005-2010年，瑞士苏黎世联邦理工学院，植物发育遗传学助理教授；2010-至今，瑞典农业科学大学，植物分子细胞生物学教授。

研究方向：植物种子发育和物种形成的遗传及表观遗传机制。

doi: 10.1038/s41477-018-0161-6

Journal: Nature Plants

First Published: 28 May, 2018

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