全基因组复制事件的绝对定年揭示莲座蕨属植物的迟滞演化

doi:10.17520/biods.2020484

生物多样性 ›› 2021, Vol. 29 ›› Issue (6): 722-734. DOI: 10.17520/biods.2020484

所属专题：物种形成与系统进化

• 研究报告: 植物多样性 • 上一篇下一篇

全基因组复制事件的绝对定年揭示莲座蕨属植物的迟滞演化

王婷¹^,²^,³, 夏增强¹^,²^,⁴, 舒江平¹^,²^,⁵, 张娇⁴, 王美娜¹^,², 陈建兵¹^,², 王慷林⁶, 向建英⁷^,^*(), 严岳鸿¹^,²^,^*()

1.深圳市兰科植物保护研究中心, 广东深圳 518114
2.兰科植物保护与利用国家林业和草原局重点实验室, 广东深圳 518114
3.西南林业大学生物多样性保护学院, 昆明 650224
4.中国科学院分子植物科学卓越创新中心/上海植物生理生态研究所, 上海 200032
5.中国科学院华南植物园, 广州 510650
6.西南林业大学绿色发展研究院, 昆明 650224
7.西南林业大学云南生物多样性研究院, 昆明 650224

收稿日期:2020-12-29 接受日期:2021-04-14 出版日期:2021-06-20 发布日期:2021-04-22
通讯作者: 向建英,严岳鸿
作者简介:jy_xiang@hotmail.com
* E-mail: yan.yh@126.com;
基金资助:
广东省基础与应用基础研究基金(2021A1515010920);云南省教育厅科学研究基金(2021Y273)

Dating whole-genome duplication reveals the evolutionary retardation of Angiopteris

Ting Wang¹^,²^,³, Zengqiang Xia¹^,²^,⁴, Jiangping Shu¹^,²^,⁵, Jiao Zhang⁴, Meina Wang¹^,², Jianbing Chen¹^,², Kanglin Wang⁶, Jianying Xiang⁷^,^*(), Yuehong Yan¹^,²^,^*()

1 The Orchid Conservation and Research Centre of Shenzhen, Shenzhen, Guangdong 518114
2 Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, Shenzhen, Guangdong 518114
3 College of Biodiversity Conservation, Southwest Forestry University, Kunming 650224
4 CAS Center for Excellence in Molecular Plant Sciences/Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032
5 South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650
6 Green Development Institute, Southwest Forestry University, Kunming 650224
7 Yunnan Academy of Biodiversity, Southwest Forestry University, Kunming 650224

Received:2020-12-29 Accepted:2021-04-14 Online:2021-06-20 Published:2021-04-22
Contact: Jianying Xiang,Yuehong Yan

摘要/Abstract

摘要：

全基因组复制在维管植物的物种形成过程中普遍存在, 被认为是物种适应极端环境的重要机制之一。确定全基因组复制事件的发生时间对理解生物的适应性演化具有重要意义。然而, 在维管植物, 特别是蕨类植物中, 全基因组复制事件的发生时间及其演化意义仍知之甚少。本研究以蕨类植物重要基部类群——福建莲座蕨(Angiopteris fokiensis)为例, 基于不同采样点(广东、广西、上海)的3个转录组学数据, 利用同义替换率(Ks)和绝对定年的方法分析全基因组复制事件的发生时间和物种单位时间内的分子演化速率, 并对事件发生后保留下的基因进行基因功能注释和富集分析。结果表明, 福建莲座蕨在159‒165 Mya发生了一次全基因组复制事件, 该复制事件优先保留的基因主要与营养代谢、信号传导、适应调节和组织结构生长相关。另外, 福建莲座蕨的分子演化速率为1.66 × 10^‒9 (同义替换/位点/年), 是除裸子植物外, 陆生植物中已知演化速率最缓慢的类群。综合以上研究结果, 我们推测福建莲座蕨全基因组复制的发生可能与裸子植物繁盛、核心被子植物集中兴起或托阿尔阶灭绝事件有关。而复制后显著保留基因可能促进了莲座蕨属(Angiopteris)植物的遗传和形态创新, 从而帮助其快速适应环境的剧烈变化。进一步对该类群植物演化速率缓慢的原因进行讨论, 推测莲座蕨属缓慢的演化速率可能与其本身世代周期长、基因组较大及其生长环境稳定有关。本研究通过分析福建莲座蕨的全基因组复制历史和复制基因的保留模式, 推测全基因组复制事件对促进演化速率较慢的植物适应极端环境变化具有重要意义, 可为理解其他陆生植物的适应性演化提供更多启发。

关键词: 多倍化, 适应性演化, 演化速率, 蕨类植物, 转录组学

Abstract

Aim: Whole-genome duplication (WGD) plays a positive role in speciation in vascular plants and is considered to be an important mechanism for species adaptation to the extreme environments. Dating whole-genome duplication events in different species is essential for understanding the adaptive evolution of organisms. However, the role that these mechanisms play in vascular plants, especially ferns, is still poorly understood.

Method: Based on the synonymous substitution rates (Ks) and absolute dating of the WGD event, this study used three different transcriptome sequences of Angiopteris fokiensis to analyze the contribution of polyploidy to the evolution of plants, and the silent substitution rate. Gene annotation and functional enrichment were carried out to elucidate the biological processes, molecular function, and cellular component for the genes retained after the WGD.

Results: We found that there was at least one WGD event in A. fokiensis at 159-165 Mya, and most duplicated genes were often related to nutrient metabolism, signal transduction, adaptive regulation and anatomical structure development. The silent substitution rate of A. fokiensis is 1.66 × 10^‒9 synonymous substitutions per site per year. Based on the above results, we speculate that the WGD event was associated with gymnosperms flourishing and the emergence of core angiosperms, or the Toarcian extinction event. The retention of particular genes after the WGD may have promoted genetic and morphological innovation in Angiopteris, thus helping it adapt to the drastic changes in environmental conditions. At present, A. fokiensisis the slowest evolving group of land plants except gymnosperms, which may relate to the long generation time, large genome and stable living habitat.

Conclusion: In this study, we analyzed the whole-genome duplication history and the patterns of retention of duplicated genes in A. fokiensis, suggesting that WGD events are of great influence in promoting the adaptation to extreme environmental changes of plants with slower evolutionary rates. These results provide more inspiration for understanding the adaptive evolution of other land plants.

Key words: polyploidization, adaptive evolution, evolution rate, ferns, transcriptome

王婷, 夏增强, 舒江平, 张娇, 王美娜, 陈建兵, 王慷林, 向建英, 严岳鸿 (2021) 全基因组复制事件的绝对定年揭示莲座蕨属植物的迟滞演化. 生物多样性, 29, 722-734. DOI: 10.17520/biods.2020484.

Ting Wang, Zengqiang Xia, Jiangping Shu, Jiao Zhang, Meina Wang, Jianbing Chen, Kanglin Wang, Jianying Xiang, Yuehong Yan (2021) Dating whole-genome duplication reveals the evolutionary retardation of Angiopteris. Biodiversity Science, 29, 722-734. DOI: 10.17520/biods.2020484.

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图/表 7

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物种 Species	NCBI登录号 NCBI no.	转录本Transcript	N50 (bp)	鸟嘌呤/胞嘧啶 GC (%)	编码序列数 No. of coding sequence	BUSCO (%)	文献 References
福建莲座蕨 Angiopteris fokiensis	SRR2103714	46,702	1,720	44.95	34,286	89.6	Shen et al, 2018
福建莲座蕨 Angiopteris fokiensis	SRR5499396	62,608	2,021	44.29	39,010	95.1	You et al, 2017
福建莲座蕨 Angiopteris fokiensis	SRR6920615	62,119	2,021	44.29	39,043	95.4	Huang et al, 2020
披散木贼 Equisetum diffusum	SRR2103706	55,430	1,537	44.93	39,399	91.4	Shen et al, 2018
桂皮紫萁 Osmundastrum cinnamomeum	SRR6727971	28,229	1,922	46.43	22,868	84.4	Wolf et al, 2018
紫萁 Osmunda japonica	SRR2103721	42,649	2,005	46.22	31,414	92.8	Huang et al, 2020
细叶双扇蕨 Dipteris lobbiana	SRR6920640	148,711	1,085	46.09	94,834	78.4	Huang et al, 2020
芒萁 Dicranopteris pedata	SRR5490811	62,818	1,954	45.78	40,874	97.5	You et al, 2017
假芒萁 Sticherus truncatus	SRR6920643	74,801	1,557	44.30	50,507	88.2	Huang et al, 2020

物种 Species	NCBI登录号 NCBI no.	转录本Transcript	N50 (bp)	鸟嘌呤/胞嘧啶 GC (%)	编码序列数 No. of coding sequence	BUSCO (%)	文献 References
福建莲座蕨 Angiopteris fokiensis	SRR2103714	46,702	1,720	44.95	34,286	89.6	Shen et al, 2018
福建莲座蕨 Angiopteris fokiensis	SRR5499396	62,608	2,021	44.29	39,010	95.1	You et al, 2017
福建莲座蕨 Angiopteris fokiensis	SRR6920615	62,119	2,021	44.29	39,043	95.4	Huang et al, 2020
披散木贼 Equisetum diffusum	SRR2103706	55,430	1,537	44.93	39,399	91.4	Shen et al, 2018
桂皮紫萁 Osmundastrum cinnamomeum	SRR6727971	28,229	1,922	46.43	22,868	84.4	Wolf et al, 2018
紫萁 Osmunda japonica	SRR2103721	42,649	2,005	46.22	31,414	92.8	Huang et al, 2020
细叶双扇蕨 Dipteris lobbiana	SRR6920640	148,711	1,085	46.09	94,834	78.4	Huang et al, 2020
芒萁 Dicranopteris pedata	SRR5490811	62,818	1,954	45.78	40,874	97.5	You et al, 2017
假芒萁 Sticherus truncatus	SRR6920643	74,801	1,557	44.30	50,507	88.2	Huang et al, 2020

样本 Sample	采集地 Collection sites	加倍数目 No. of duplicates	组件数目 No. of components	贝叶斯信息标准 Bayesian information criterion	中值 Median (Ks)	方差 Variance	比例 Proportion
福建莲座蕨 Angiopteris fokiensis SRR2103714	上海 Shanghai	3,667	6	?6,824.9400	0.1310	0.0005	0.0763
		3,667	6	?6,824.9400	0.2147	0.0029	0.0577
		3,667	6	?6,824.9400	0.5814	0.0200	0.2697
		3,667	6	?6,824.9400	0.9172	0.0312	0.2529
		3,667	6	?6,824.9400	1.3513	0.1683	0.2040
		3,667	6	?6,824.9400	3.0112	0.8830	0.1393
福建莲座蕨 Angiopteris fokiensis SRR5499396	广东 Guangdong	4,238	7	?7,662.1730	0.1241	0.0003	0.0680
		4,238	7	?7,662.1730	0.2002	0.0023	0.0921
		4,238	7	?7,662.1730	0.5856	0.0191	0.2940
		4,238	7	?7,662.1730	0.9331	0.0198	0.1781
		4,238	7	?7,662.1730	1.1911	0.1116	0.1935
		4,238	7	?7,662.1730	2.3596	0.4994	0.1330
		4,238	7	?7,662.1730	4.1443	0.2343	0.0412
福建莲座蕨 Angiopteris fokiensis SRR6920615	广西 Guangxi	4,235	6	?7,662.1730	0.1259	0.0003	0.0753
		4,235	6	?7,662.1730	0.1996	0.0022	0.0834
		4,235	6	?7,662.1730	0.5489	0.0148	0.2082
		4,235	6	?7,662.1730	0.8841	0.0452	0.3284
		4,235	6	?7,662.1730	1.3642	0.1874	0.1606
		4,235	6	?7,662.1730	2.9677	0.9873	0.1441

样本 Sample	采集地 Collection sites	加倍数目 No. of duplicates	组件数目 No. of components	贝叶斯信息标准 Bayesian information criterion	中值 Median (Ks)	方差 Variance	比例 Proportion
福建莲座蕨 Angiopteris fokiensis SRR2103714	上海 Shanghai	3,667	6	?6,824.9400	0.1310	0.0005	0.0763
		3,667	6	?6,824.9400	0.2147	0.0029	0.0577
		3,667	6	?6,824.9400	0.5814	0.0200	0.2697
		3,667	6	?6,824.9400	0.9172	0.0312	0.2529
		3,667	6	?6,824.9400	1.3513	0.1683	0.2040
		3,667	6	?6,824.9400	3.0112	0.8830	0.1393
福建莲座蕨 Angiopteris fokiensis SRR5499396	广东 Guangdong	4,238	7	?7,662.1730	0.1241	0.0003	0.0680
		4,238	7	?7,662.1730	0.2002	0.0023	0.0921
		4,238	7	?7,662.1730	0.5856	0.0191	0.2940
		4,238	7	?7,662.1730	0.9331	0.0198	0.1781
		4,238	7	?7,662.1730	1.1911	0.1116	0.1935
		4,238	7	?7,662.1730	2.3596	0.4994	0.1330
		4,238	7	?7,662.1730	4.1443	0.2343	0.0412
福建莲座蕨 Angiopteris fokiensis SRR6920615	广西 Guangxi	4,235	6	?7,662.1730	0.1259	0.0003	0.0753
		4,235	6	?7,662.1730	0.1996	0.0022	0.0834
		4,235	6	?7,662.1730	0.5489	0.0148	0.2082
		4,235	6	?7,662.1730	0.8841	0.0452	0.3284
		4,235	6	?7,662.1730	1.3642	0.1874	0.1606
		4,235	6	?7,662.1730	2.9677	0.9873	0.1441

全基因组复制事件的绝对定年揭示莲座蕨属植物的迟滞演化

Dating whole-genome duplication reveals the evolutionary retardation of Angiopteris

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