Key message

Reproduction in triploid plants is important for understanding polyploid population dynamics. We show that genetically identical reciprocal F1 hybrid triploids can display transgenerational epigenetic effects on viable F2 seed development.

Abstract

The success or failure of reproductive outcomes from intra-species crosses between plants of different ploidy levels is an important factor in flowering plant evolution and crop breeding. However, the effects of inter-ploidy cross directions on F1 hybrid offspring fitness are poorly understood. In Arabidopsis thaliana, hybridization between diploid and tetraploid plants can produce viable F1 triploid plants. When selfed, such F1 triploid plants act as aneuploid gamete production “machines” where the vast majority of gametes generated are aneuploid which, following sexual reproduction, can generate aneuploid swarms of F2 progeny (Henry et al. 2009). There is potential for some aneuploids to cause gametophyte abortion and/or F2 seed abortion (Henry et al. 2009). In this study, we analyse the reproductive success of 178 self-fertilized inter-accession F1 hybrid triploids and demonstrate that the proportions of aborted or normally developed F2 seeds from the selfed F1 triploids depend upon a combination of natural variation and cross direction, with strong interaction between these factors. Single-seed ploidy analysis indicates that the embryonic DNA content of phenotypically normal F2 seeds is highly variable and that these DNA content distributions are also affected by genotype and cross direction. Notably, genetically identical reciprocal F1 hybrid triploids display grandparent-of-origin effects on F2 seed set, and hence on the ability to tolerate aneuploidy in F2 seed. There are differences between reciprocal F1 hybrid triploids regarding the proportions of normal and aborted F2 seeds generated, and also for the DNA content averages and distributions of the F2 seeds. To identify genetic variation for tolerance of aneuploidy in F2 seeds, we carried out a GWAS which identified two SNPs, termed MOT and POT, which represent candidate loci for genetic control of the proportion of normal F2 seeds obtained from selfed F1 triploids. Parental and grandparental effects on F2 seeds obtained from selfed F1 triploids can have transgenerational consequences for asymmetric gene flow, emergence of novel genotypes in polyploid populations, and for control of F2 seed set in triploid crops.

中文翻译：

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倍性间交叉方向对拟南芥F1杂种三倍体繁殖和F2种子发育的跨代影响。

 关键信息

三倍体植物的繁殖对于了解多倍体种群动态非常重要。我们证明，遗传相同的互惠 F1 杂种三倍体可以对可行的 F2 种子发育表现出跨代表观遗传效应。

 抽象的

不同倍性水平植物之间的种内杂交繁殖结果的成功或失败是开花植物进化和作物育种的重要因素。然而，倍性间交叉方向对 F1 杂种后代适应性的影响知之甚少。在拟南芥中，二倍体和四倍体植物之间的杂交可以产生可存活的F1三倍体植物。当自交时，此类 F1 三倍体植物充当非整倍体配子生产“机器”，其中生成的绝大多数配子都是非整倍体，在有性繁殖后，可以产生非整倍体 F2 后代群（Henry 等，2009）。某些非整倍体有可能导致配子体败育和/或 F2 种子败育（Henry et al. 2009）。在本研究中，我们分析了 178 个自交种间 F1 杂种三倍体的繁殖成功率，并证明自交 F1 三倍体中败育或正常发育的 F2 种子的比例取决于自然变异和交叉方向的组合，具有很强的这些因素之间的相互作用。单种子倍性分析表明，表型正常的 F2 种子的胚胎 DNA 含量变化很大，并且这些 DNA 含量分布也受到基因型和交叉方向的影响。值得注意的是，遗传相同的互惠 F1 杂种三倍体对 F2 种子表现出祖父母起源效应，因此对 F2 种子耐受非整倍性的能力也有影响。倒数 F1 杂种三倍体之间在产生的正常和败育的 F2 种子的比例以及 F2 种子的 DNA 含量平均值和分布方面存在差异。 为了鉴定F2种子中非整倍体耐受性的遗传变异，我们进行了GWAS，鉴定了两个SNP，称为MOT和POT ，它们代表从自交F1三倍体获得的正常F2种子比例的遗传控制的候选位点。亲本和祖父母对自交 F1 三倍体获得的 F2 种子的影响可能会对不对称基因流、多倍体群体中新基因型的出现以及三倍体作物中 F2 种子的控制产生跨代后果。