Multi-speed genome diploidization and diversification after an ancient allopolyploidization

Hybridization and genome doubling (allopolyploidy) have led to evolutionary novelties as well as to the origin of new clades and species. Despite the importance of allopolyploidization, the dynamics of post-polyploid diploidization (PPD) at the genome level has been only sparsely studied. The Microlepidieae (MICR) is a crucifer tribe of 17 genera and c. 56 species endemic to Australia and New Zealand. Our phylogenetic and cytogenomic analyses revealed that MICR originated via an inter-tribal hybridization between ancestors of Crucihimalayeae (n = 8; maternal genome) and Smelowskieae (n = 7; paternal genome), both native to the Northern Hemisphere. The reconstructed ancestral allopolyploid genome (n = 15) originated probably in north-eastern Asia or western North America during the Late Miocene (c. 10.6 - 7 million years ago) and reached the Australian mainland via long-distance dispersal. In Australia, the allotetraploid genome diverged into at least three main subclades exhibiting different levels of PPD and diversity: 1.25-fold descending dysploidy (DD) of n = 15 → n = 12 (autopolyploidy → 24) in perennial Arabidella (3 species), 1.5-fold DD of n = 15 → n = 10 in the perennial Pachycladon (11 spp.), and 2.1 to 3.75-fold DD of n = 15 → n = 7 - 4 in the largely annual crown group genera (42 spp. in 15 genera). These results are among the first to demonstrate multi-speed genome evolution in taxa descending from a common allopolyploid ancestor. It is suggested that clade-specific PPD can operate at different rates and efficacies, and can be tentatively linked to life histories and the extent of taxonomic diversity.

杂交与基因组加倍（异源多倍化，allopolyploidy）既可催生进化新奇性状，亦促成了新演化支与物种的起源。尽管异源多倍化具有重要的进化意义，但学界对基因组水平上的多倍体后二倍体化（post-polyploid diploidization, PPD）动态过程的研究仍较为匮乏。微鳞族（Microlepidieae, MICR）是十字花科（crucifer）下的一个族，共计17属、约56种，为澳大利亚与新西兰特有类群。我们的系统发育与细胞基因组学分析显示，微鳞族起源于两个北半球土著类群祖先之间的族间杂交事件：硬毛荠族（Crucihimalayeae，n=8；母本基因组）与冰荠族（Smelowskieae，n=7；父本基因组）。研究重建得到的祖先异源多倍体基因组（n=15）可能形成于中新世晚期（约1060万至700万年前）的东北亚或北美西部，并通过长距离扩散抵达澳大利亚大陆。在澳大利亚境内，该异源四倍体基因组分化出至少三个主演化支，各自呈现出不同程度的多倍体后二倍体化水平与多样性：1. 多年生类群南芥荠属（Arabidella，3种）经历了1.25倍的下行非整倍体化（descending dysploidy, DD），染色体基数由n=15变为n=12（伴随同源多倍化（autopolyploidy）→2n=24）；2. 多年生类群厚柄荠属（Pachycladon，11种）经历了1.5倍的下行非整倍体化，染色体基数由n=15变为n=10；3. 以一年生为主的冠群类群（crown group，共15属42种）则经历了2.1至3.75倍的下行非整倍体化，染色体基数由n=15变为n=7至n=4。本研究结果为首批揭示源自同一异源多倍体祖先的类群存在多速基因组演化现象的成果之一。研究表明，演化支特异性的多倍体后二倍体化可通过不同速率与效率运作，且可初步与生物生活史特征及类群分类多样性程度建立关联。