A novel allele of ASY3 promotes meiotic stability in autotetraploid Arabidopsis lyrata
A novel allele of ASY3 promotes meiotic stability in autotetraploid Arabidopsis lyrata
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DOI：
10.1101/2019.12.25.888388
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发表时间：
2019-12
期刊：
影响因子：
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通讯作者：
P. Seear;Martin G France;Catherine L. Gregory;D. Heavens;R. Schmickl;Levi Yant;J. Higgins
中科院分区：
文献类型：
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作者：
P. Seear;Martin G France;Catherine L. Gregory;D. Heavens;R. Schmickl;Levi Yant;J. Higgins
本研究对10个同源四倍体拟南芥和拟南芥/拟南芥的减数分裂稳定性进行了基因型-表型关联分析。收集自瓦豪地区和东奥地利山地的沙蚤杂交种。目的是确定八个减数分裂基因在极端选择下对全基因组复制适应的影响。通过对与突触复合体形成有关的8个减数分裂基因（ASY1、ASY3、PDS5b、PRD3、REC8、SMC3、ZYP1a/b）的高通量测序，对单株植物进行了基因分型，并通过评估减数分裂中期I染色体构型进行了表型分型。我们的研究结果表明，四倍体植物间减数分裂稳定性差异很大（20-100%），这与来自a. lyrata的与出芽酵母RED1染色体轴蛋白同源的新等位基因Asynapsis3 （ASY3）的分离有关。自适应ASY3蛋白在DNA微同源位点的螺旋结构域上游具有一个假定的富含丝氨酸的框内串联重复（TD）。纯合的ASY3 TD单倍型植物的多价体频率显著低于TD/ND（非重复）ASY3单倍型植物的杂合频率。与不稳定植物相比，稳定植物的交叉分布发生了显著变化，从近端和间隙向远端转移。与ASY3 ND/TD杂合子相比，ASY3 TD纯合子植物减数分裂核中标记I类杂交的厚粒上的he10焦点数量显著减少，表明ASY3 TD等位基因的适应性结果。从10个群体中鉴定出这8个减数分裂基因的58个等位基因，显示出这些位点的动态群体变异，但表现出强硬选择扫描的特征。源自A. lyrata/A.的等位基因之间的广泛嵌合。砂状体和二倍体/四倍体表明，这组快速进化的基因对四倍体的减数分裂重组提供了精确的适应性控制，而减数分裂重组正是产生它们的过程。全基因组复制可以促进适应性，但它是一种剧烈的突变，通常会导致减数分裂突变和基因组不稳定。本文研究了10个同源四倍体拟南芥和拟南芥/拟南芥减数分裂重组协调稳定的案例。来自瓦豪地区和东奥地利山地的沙蚤杂交种群。我们将群体基因组数据与基因型-表型关联研究相结合，重点研究了极端选择下四倍体中涉及突触复合体形成的8个减数分裂基因（ASY1, ASY3, PDS5b, PRD3, REC8, SMC3, ZYP1a/b）的影响。我们的分析表明，减数分裂染色体轴蛋白Asynapsis3的一个新的等位基因包含一个富含丝氨酸区域的帧内重复，是男性减数分裂稳定性的主要决定因素。这种适应性再稳定似乎是通过减数分裂交叉数量的减少以及它们向染色体末端定位的转移来实现的。在8个基因中，鉴定出58个等位基因，表明这些位点在极端选择下存在动态群体变异。此外，还发现了广泛存在的等位基因嵌合现象。砂状体和二倍体/四倍体表明，这组快速进化的基因对四倍体的减数分裂重组提供了精确的适应性控制，而减数分裂重组正是产生它们的过程。
In this study we performed a genotype-phenotype association analysis of meiotic stability in ten autotetraploid Arabidopsis lyrata and A. lyrata/A. arenosa hybrid populations collected from the Wachau region and East Austrian Forealps. The aim was to determine the effect of eight meiosis genes under extreme selection upon adaptation to whole genome duplication. Individual plants were genotyped by high-throughput sequencing of the eight meiosis genes (ASY1, ASY3, PDS5b, PRD3, REC8, SMC3, ZYP1a/b) implicated in synaptonemal complex formation and phenotyped by assessing meiotic metaphase I chromosome configurations. Our results reveal that meiotic stability varied greatly (20-100%) between individual tetraploid plants and was associated with segregation of a novel allele orthologous to the budding yeast RED1 chromosome axis protein, Asynapsis3 (ASY3), derived from A. lyrata. The adaptive ASY3 protein possesses a putative in-frame tandem duplication (TD) of a serine-rich region upstream of the coiled-coil domain that has arisen at sites of DNA microhomology. The frequency of multivalents observed in plants homozygous for the ASY3 TD haplotype was significantly lower than plants heterozygous for TD/ND (non-duplicated) ASY3 haplotypes. Chiasma distribution was significantly altered in the stable plants compared to the unstable plants with a shift from proximal and interstitial to predominantly distal locations. The number of HEI10 foci at pachtyene that mark class I crossovers was significantly reduced in meiotic nuclei from ASY3 TD homozygous plants compared to ASY3 ND/TD heterozygotes, indicating an adaptive consequence of the ASY3 TD allele. From the ten populations, fifty-eight alleles of these 8 meiosis genes were identified, demonstrating dynamic population variability at these loci which nevertheless exhibit signatures of strong hard selective sweeps. Widespread chimerism between alleles originating from A. lyrata/A. arenosa and diploid/tetraploids indicates that this group of rapidly evolving genes provide precise adaptive control over meiotic recombination in the tetraploids, the very process that gave rise to them. Author summary Whole genome duplication can promote adaptability, but is a dramatic mutation usually resulting in meiotic catastrophe and genome instability. Here we focus on a case of coordinated stabilization of meiotic recombination in ten autotetraploid Arabidopsis lyrata and A. lyrata/A. arenosa hybrid populations from the Wachau region and East Austrian Forealps. We fuse population genomic data with a genotype-phenotype association study, concentrating on the effects of eight meiosis genes (ASY1, ASY3, PDS5b, PRD3, REC8, SMC3, ZYP1a/b) implicated in synaptonemal complex formation in the tetraploids under extreme selection. Our analysis demonstrates that a novel allele of the meiotic chromosome axis protein Asynapsis3 that contains an in-frame duplication of a serine-rich region is the major determinant of male meiotic stability. This adaptive restabilisation appears to be achieved by a reduction in the number of meiotic crossovers as well as a shift in their positioning towards the chromosome ends. Of the eight genes, fifty-eight alleles were identified, indicating dynamic population variability at these loci under extreme selection. In addition, widespread allelic chimerism between alleles originating from A. lyrata/A. arenosa and diploid/tetraploids indicates that this group of rapidly evolving genes provide precise adaptive control over meiotic recombination in the tetraploids, the very process that gave rise to them.