Florez-Rueda Ana M, Paris Margot, Schmidt Anja, Widmer Alex, Grossniklaus Ueli, Städler Thomas
Plant Ecological Genetics, Institute of Integrative Biology & Zurich-Basel Plant Science Center, ETH Zurich, Zurich, Switzerland.
Plant Developmental Genetics, Department of Plant and Microbial Biology & Zurich-Basel Plant Science Center, University of Zurich, Zurich, Switzerland.
Mol Biol Evol. 2016 Nov;33(11):2935-2946. doi: 10.1093/molbev/msw175. Epub 2016 Sep 6.
Hybrid seed failure represents an important postzygotic barrier to interbreeding among species of wild tomatoes (Solanum section Lycopersicon) and other flowering plants. We studied genome-wide changes associated with hybrid seed abortion in the closely related Solanum peruvianum and S. chilense where hybrid crosses yield high proportions of inviable seeds due to endosperm failure and arrested embryo development. Based on differences of seed size in reciprocal hybrid crosses and developmental evidence implicating endosperm failure, we hypothesized that perturbed genomic imprinting is involved in this strong postzygotic barrier. Consequently, we surveyed the transcriptomes of developing endosperms from intra- and inter-specific crosses using tissues isolated by laser-assisted microdissection. We implemented a novel approach to estimate parent-of-origin-specific expression using both homozygous and heterozygous nucleotide differences between parental individuals and identified candidate imprinted genes. Importantly, we uncovered systematic shifts of "normal" (intraspecific) maternal:paternal transcript proportions in hybrid endosperms; the average maternal proportion of gene expression increased in both crossing directions but was stronger with S. peruvianum in the maternal role. These genome-wide shifts almost entirely eliminated paternally expressed imprinted genes in S. peruvianum hybrid endosperm but also affected maternally expressed imprinted genes and all other assessed genes. These profound, systematic changes in parental expression proportions suggest that core processes of transcriptional regulation are functionally compromised in hybrid endosperm and contribute to hybrid seed failure.
杂种种子败育是野生番茄（番茄属）和其他开花植物物种间杂交的一个重要合子后障碍。我们研究了与秘鲁番茄和智利番茄这两个近缘种杂种种子败育相关的全基因组变化，在这两个物种的杂交中，由于胚乳败育和胚胎发育停滞，杂种后代产生大量 inviable 种子。基于正反交杂种种子大小的差异以及暗示胚乳败育的发育证据，我们推测基因组印记紊乱参与了这种强烈的合子后障碍。因此，我们使用激光辅助显微切割分离的组织，对种内和种间杂交发育中的胚乳转录组进行了调查。我们采用了一种新方法，利用亲本个体间纯合和杂合核苷酸差异来估计亲本来源特异性表达，并鉴定了候选印记基因。重要的是，我们发现杂种胚乳中“正常”（种内）母本：父本转录比例发生了系统性变化；在两个杂交方向上，基因表达的平均母本比例都增加了，但当秘鲁番茄作为母本时变化更明显。这些全基因组变化几乎完全消除了秘鲁番茄杂种胚乳中父本表达的印记基因，但也影响了母本表达的印记基因和所有其他评估基因。亲本表达比例的这些深刻、系统性变化表明，转录调控的核心过程在杂种胚乳中功能受损，导致杂种种子败育。
