Ren Chen, Wang Long, Nie Ze-Long, Tang Ming, Johnson Gabriel, Tan Hui-Tong, Xia Nian-He, Wen Jun, Yang Qin-Er
State Key Laboratory of Plant Diversity and Specialty Crops, South China Botanical Garden, Chinese Academy of Sciences, 723 Xingke Road, Tianhe District, Guangzhou, Guangdong 510650, China.
South China National Botanical Garden, 723 Xingke Road, Tianhe District, Guangzhou, Guangdong 510650, China.
Syst Biol. 2024 Nov 29;73(6):941-963. doi: 10.1093/sysbio/syae046.
Polyploidy is a significant mechanism in eukaryotic evolution and is particularly prevalent in the plant kingdom. However, our knowledge about this phenomenon and its effects on evolution remains limited. A major obstacle to the study of polyploidy is the great difficulty in untangling the origins of allopolyploids. Due to the drastic genome changes and the erosion of allopolyploidy signals caused by the combined effects of hybridization and complex postpolyploid diploidization processes, resolving the origins of allopolyploids has long been a challenging task. Here we revisit this issue with the interesting case of subtribe Tussilagininae (Asteraceae: Senecioneae) and by developing HomeoSorter, a new pipeline for network inferences by phasing homeologs to parental subgenomes. The pipeline is based on the basic idea of a previous study but with major changes to address the scaling problem and implement some new functions. With simulated data, we demonstrate that HomeoSorter works efficiently on genome-scale data and has high accuracy in identifying polyploid patterns and assigning homeologs. Using HomeoSorter, the maximum pseudo-likelihood model of Phylonet, and genome-scale data, we further address the complex origin of Tussilagininae, a speciose group (ca. 45 genera and 710 species) characterized by having high base chromosome numbers (mainly x = 30, 40). In particular, the inferred patterns are strongly supported by the chromosomal evidence. Tussilagininae is revealed to comprise 2 large groups with successive allopolyploid origins: Tussilagininae s.s. (mainly x = 30) and the Gynoxyoid group (x = 40). Two allopolyploidy events first give rise to Tussilagininae s.s., with the first event occurring between the ancestor of subtribe Senecioninae (x = 10) and a lineage (highly probably with x = 10) related to the Brachyglottis alliance, and the resulting hybrid lineage crossing with the ancestor of Chersodoma (x = 10) and leading to Tussilagininae s.s. Then, after early diversification, the Central American group (mainly x = 30) of Tussilagininae s.s., is involved in a third allopolyploidy event with, again, the Chersodoma lineage and produces the Gynoxyoid group. Our study highlights the value of HomeoSorter and the homeolog-sorting approach in polyploid phylogenetics. With rich species diversity and clear evolutionary patterns, Tussilagininae s.s. and the Gynoxyoid group are also excellent models for future investigations of polyploidy.
多倍体是真核生物进化中的一个重要机制，在植物界尤为普遍。然而，我们对这一现象及其对进化的影响的了解仍然有限。研究多倍体的一个主要障碍是解开异源多倍体起源的巨大困难。由于杂交和复杂的多倍体后二倍体化过程的综合作用导致基因组发生剧烈变化以及异源多倍体信号的侵蚀，解析异源多倍体的起源长期以来一直是一项具有挑战性的任务。在这里，我们以款冬亚族（菊科：千里光族）这一有趣的案例，并通过开发HomeoSorter（一种通过将同源基因定相到亲本亚基因组进行网络推断的新流程）来重新审视这个问题。该流程基于先前一项研究的基本思想，但有重大改变以解决规模问题并实现一些新功能。通过模拟数据，我们证明HomeoSorter在基因组规模数据上能高效运行，在识别多倍体模式和分配同源基因方面具有很高的准确性。使用HomeoSorter、Phylonet的最大伪似然模型和基因组规模数据，我们进一步解析了款冬亚族复杂的起源，款冬亚族是一个物种丰富的类群（约45属710种），其特征是具有高基数染色体数（主要x = 30、40）。特别是，推断出的模式得到了染色体证据的有力支持。款冬亚族被揭示由两个具有连续异源多倍体起源的大组组成：狭义款冬亚族（主要x = 30）和裸果千里光类群（x = 40）。两次异源多倍体事件首先产生了狭义款冬亚族，第一次事件发生在千里光亚族（x = 10）的祖先与一个与短舌菊联盟相关的谱系（极有可能x = 且10）之间，产生的杂交谱系与雪果属（x = 10）的祖先杂交，从而形成狭义款冬亚族。然后，在早期分化之后，狭义款冬亚族的中美洲类群（主要x = 30）与雪果属谱系再次发生第三次异源多倍体事件，产生了裸果千里光类群。我们的研究突出了HomeoSorter和同源基因分类方法在多倍体系统发育学中的价值。狭义款冬亚族和裸果千里光类群具有丰富的物种多样性和清晰的进化模式，也是未来多倍体研究的优秀模型。
