Standing genetic variation in a tissue-specific enhancer underlies selfing-syndrome evolution in Capsella
Standing genetic variation in a tissue-specific enhancer underlies selfing-syndrome evolution in Capsella
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DOI：
10.1073/pnas.1613394113
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发表时间：
2016-11
期刊：
影响因子：
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通讯作者：
A. Sicard;C. Kappel;Y. Lee;N. Woźniak;Cindy Marona;J. Stinchcombe;S. Wright;Michael Lenhard
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文献类型：
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作者：
A. Sicard;C. Kappel;Y. Lee;N. Woźniak;Cindy Marona;J. Stinchcombe;S. Wright;Michael Lenhard
花的大小在进化过程中变化迅速；特别是，从动物介导的异交到自花授粉的频繁过渡通常与花大小的急剧、快速和特定的减少有关。在这里，我们证明了自花红荠菜（风疹荠菜）的小花瓣是由于花瓣中一般生长因子活性的特定减少。这种生长基因的不同强度版本已经存在于祖先的外种繁殖种群中，从这个群体中捕获一个弱版本可以解释风疹C.花瓣大小的快速缩小。低多效性的小效突变分离的加性效应允许花瓣大小的特定调节，以适应新的繁殖模式。交配系统的变化经常导致器官尺寸的特定变化。交配系统从外交到自交的转变是开花植物中最常见的进化转变之一，通常与器官特异性的花大小缩小有关。然而，人们对多基因特征（如体型）的进化路径知之甚少。特别是，尽管大多数已知的生长调节剂具有多效性，但尚不清楚自然选择如何特异性地调节一个器官的大小。在这里，我们证明了一般生长调节剂内含子的等位基因变异有助于在油菜属向自交过渡后花瓣大小的特定减小。该内含子内的变异影响一个器官特异性增强子，该增强子调节发育中的花瓣中无菌无瓣花序（SAP）蛋白的水平。SAP活性降低导致细胞增殖周期缩短，花瓣细胞数量减少。在自交物种的因果区域中没有私人多态性，这表明小花瓣等位基因是从祖先异交群体的长期遗传变异中捕获的。当前异交群体中花瓣大小的变化表明，一些小效应突变有助于花瓣大小的减小。这些数据证明了多效基因中的组织特异性调控元件如何促进器官特异性进化。此外，它们还提供了一种基于分离等位基因加性效应的花型在外缘繁殖到自交过渡后快速进化的合理进化解释。
Significance Flower size can change rapidly in evolution; in particular, the frequent transition from animal-mediated out-crossing to self-pollination is often associated with a dramatic, yet rapid and specific, reduction in flower size. Here we demonstrate that the small petals of the selfing red Shepherd’s Purse (Capsella rubella) are because of a specific reduction in the activity of a general growth factor in petals. Different-strength versions of this growth gene were already present in the ancestral out-breeding population, and capture of a weak version from this pool can explain the rapid reduction of petal size in C. rubella. The additive effects of segregating small-effect mutations with low pleiotropy allowed specific modulation of petal size to enable adaptation to a new mode of reproduction. Mating system shifts recurrently drive specific changes in organ dimensions. The shift in mating system from out-breeding to selfing is one of the most frequent evolutionary transitions in flowering plants and is often associated with an organ-specific reduction in flower size. However, the evolutionary paths along which polygenic traits, such as size, evolve are poorly understood. In particular, it is unclear how natural selection can specifically modulate the size of one organ despite the pleiotropic action of most known growth regulators. Here, we demonstrate that allelic variation in the intron of a general growth regulator contributed to the specific reduction of petal size after the transition to selfing in the genus Capsella. Variation within this intron affects an organ-specific enhancer that regulates the level of STERILE APETALA (SAP) protein in the developing petals. The resulting decrease in SAP activity leads to a shortening of the cell proliferation period and reduced number of petal cells. The absence of private polymorphisms at the causal region in the selfing species suggests that the small-petal allele was captured from standing genetic variation in the ancestral out-crossing population. Petal-size variation in the current out-crossing population indicates that several small-effect mutations have contributed to reduce petal-size. These data demonstrate how tissue-specific regulatory elements in pleiotropic genes contribute to organ-specific evolution. In addition, they provide a plausible evolutionary explanation for the rapid evolution of flower size after the out-breeding-to-selfing transition based on additive effects of segregating alleles.