孑遗植物湖北枫杨的环境适应性遗传变异与遗传脆弱性

doi:10.17521/cjpe.2024.0445

植物生态学报 ›› 2025, Vol. 49 ›› Issue (10): 1626-1642.DOI: 10.17521/cjpe.2024.0445

孑遗植物湖北枫杨的环境适应性遗传变异与遗传脆弱性

逯子佳¹^,², 王天瑞¹, 郑斯斯¹, 孟宏虎³^,⁴, 曹建国², Gregor KOZLOWSKI¹^,⁵^,⁶, 宋以刚¹^,^*()

¹上海辰山植物园, 华东野生濒危资源植物保育中心, 上海 201602
²上海师范大学生命科学学院, 上海 200234
³中国科学院西双版纳热带植物园综合保护中心, 昆明 650223
⁴中国科学院东南亚生物多样性研究中心, 缅甸内比都 05282
⁵Department of Biology and Botanic Garden, University of Fribourg, Fribourg 1700, Switzerland
⁶Natural History Museum Fribourg, Fribourg 1700, Switzerland

收稿日期:2024-12-09 接受日期:2025-02-07 出版日期:2025-10-20 发布日期:2025-11-20
通讯作者: *宋以刚(ygsong@cemps.ac.cn)
基金资助:
中国国家留学基金(201608310121);上海市绿化和市容管理局科学技术项目(G212406);Foundation Franklinia(2017-2020)

Environmental adaptive genetic variation and genetic vulnerability of relict plant Pterocarya hupehensis

LU Zi-Jia¹^,², WANG Tian-Rui¹, ZHENG Si-Si¹, MENG Hong-Hu³^,⁴, CAO Jian-Guo², Gregor KOZLOWSKI¹^,⁵^,⁶, SONG Yi-Gang¹^,^*()

¹Eastern China Conservation Centre for Wild Endangered Plant Resources, Shanghai Chenshan Botanical Garden, Shanghai 201602, China
²College of Life Sciences, Shanghai Normal University, Shanghai 200234, China
³Center for Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Kunming 650223, China
⁴Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences, Nay Pyi Taw 05282, Myanmar
⁵Department of Biology and Botanic Garden, University of Fribourg, Fribourg 1700, Switzerland
⁶Natural History Museum Fribourg, Fribourg 1700, Switzerland

Received:2024-12-09 Accepted:2025-02-07 Online:2025-10-20 Published:2025-11-20
Supported by:
The China Scholarship Council(201608310121);The Special Fund for Scientific Research of Shanghai Landscaping & City Appearance Administrative Bureau(G212406);Foundation Franklinia(2017-2020)

摘要/Abstract

摘要：

气候的快速波动正加速改变着物种命运, 导致部分物种的脆弱性加剧, 并造成许多物种的遗传多样性丧失, 甚至面临灭绝风险。孑遗植物历经新生代以来的极端气候波动, 携带着大量与环境适应相关遗传信息。探讨其种群适应环境的遗传基础及其对未来气候的适应潜力, 可为生物多样性保护提供重要参考依据。该研究以环绕中国四川盆地分布的新生代孑遗植物湖北枫杨(Pterocarya hupehensis)为研究对象, 对其分布范围内18个种群的122个个体进行简化基因组测序; 利用景观基因组学分析方法, 对湖北枫杨的生态适应和遗传脆弱性进行研究。特异性位点检测表明, 398个单核苷酸多态性位点(SNPs)与6个气候因子(等温性、最冷月份最低气温、气温年较差、最湿季度平均气温、最湿月份降水量和降水量季节性变化)具有显著关联, 此外检测到177个受到选择的SNPs位点。梯度森林分析和广义相异模型分析表明降水量季节性变化是影响该物种遗传变异的重要气候因子。Mantel检验检测到显著的环境隔离信号, 冗余分析结果表明环境因素对于遗传变异的解释度大于地理因素。最后, 非适应性风险分析预测到湖北枫杨种群在2090年SSP585情景下的种群脆弱性整体高于SSP126情景, 且降水量季节性变化对于湖北枫杨西北部种群适应能力具有重要影响。该研究不仅为易危物种湖北枫杨在未来气候变化下的管理与保护策略提供了理论依据, 还为环四川盆地孑遗植物如何应对未来气候变化提供新范例。

关键词: 孑遗植物, 景观基因组学, 生态适应, 遗传脆弱性, 简化基因组测序

Abstract:

Aims The rapid fluctuations of climate are increasingly altering the fate of species, exacerbating their vulnerability, leading to the loss of genetic diversity in many species, and even pushing some to the brink of extinction. Relict plants, having survived extreme climate changes since the Cenozoic era, carry a wealth of genetic information related to environmental adaptation. Investigating the genetic basis of their population-level environmental adaptation and their potential to cope with future climate change can provide valuable insights for biodiversity conservation.
Methods In this study, restriction site-associated DNA sequencing (RAD-seq) was performed on 122 individuals from 18 populations of Pterocarya hupehensis, which is a Cenozoic relict plant distributed around the Sichuan Basin in China. Then, the ecological adaptation and genetic vulnerability of P. hupehensis were studied by landscape genomics. First, we use a latent factor mixed model (LFMM) and Pcadapt to detect selected sites. Second, a Mantel test based on linear models, redundancy analysis (RDA), gradient forest (GF), and generalized dissimilarity modelling (GDM) were used to investigate the response patterns of genetic variation to environmental gradients. Finally, based on the risk of non-adaptedness analysis (RONA), the vulnerability of the P. hupehensis was predicted for the SSP245 and SSP585 scenarios in 2090.
Important findings A total of 398 single nucleotide polymorphism loci (SNPs) were significantly associated with the six climatic factors (isothermality, minimum temperature of coldest month, temperature annual range, mean temperature of wettest quarter, precipitation of wettest month, and precipitation seasonality). In addition, 177 of them were detected as selected SNPs. We found that precipitation seasonality was an important climatic factor affecting the genetic variation of P. hupehensis. A significant signal of isolation by environment (IBE) was detected, indicating that environmental factors account for more genetic variation than geographical factors. Under the SSP585 scenario in 2090, the genetic vulnerability of P. hupehensis was higher than that under SSP126 scenario. The precipitation seasonality has an important effect on the adaptative ability of the population in the northwest range of P. hupehensis. This study not only provides a theoretical foundation for the management and conservation strategies of vulnerable species in the face of future climate change, but also offers a new case study on how relict plants around Sichuan Basin may respond to future climate change.

Key words: relict plants, landscape genomics, ecological adaptation, genetic vulnerability, restriction site-associated DNA sequencing

逯子佳, 王天瑞, 郑斯斯, 孟宏虎, 曹建国, Gregor KOZLOWSKI, 宋以刚. 孑遗植物湖北枫杨的环境适应性遗传变异与遗传脆弱性. 植物生态学报, 2025, 49(10): 1626-1642. DOI: 10.17521/cjpe.2024.0445

LU Zi-Jia, WANG Tian-Rui, ZHENG Si-Si, MENG Hong-Hu, CAO Jian-Guo, Gregor KOZLOWSKI, SONG Yi-Gang. Environmental adaptive genetic variation and genetic vulnerability of relict plant Pterocarya hupehensis. Chinese Journal of Plant Ecology, 2025, 49(10): 1626-1642. DOI: 10.17521/cjpe.2024.0445

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2024.0445

https://www.plant-ecology.com/CN/Y2025/V49/I10/1626

图/表 9

图1 湖北枫杨的生境(A)、植株形态(B-E)和样品采集点(F)。样品采集点信息见表1。

Fig. 1 Habitat of Pterocarya hupehensis (A), plant morphology (B-E), and collection sites of P. hupehensis (F). The information of collection sites is shown in Table 1.

表1 基于酶切的简化基因组测序数据的18个湖北枫杨种群的样本编码、采样位置以及种群个体数量

Table 1 Sample coding, sampling locations, and individual numbers of 18 Pterocarya hupehensis populations based on restriction-site associated DNA-sequnencing (RAD-seq)

种群编号 Code	采样点 Site	经度 Longitude (° E)	纬度 Latitude (° N)	个体数 n
HH	陕西西安 Xi’an, Shaanxi	107.93	33.87	6
HXC	陕西安康 Ankang, Shaanxi	109.49	32.72	3
FLC	陕西安康 Ankang, Shaanxi	109.40	31.95	5
DSP	陕西宝鸡 Baoji, Shaanxi	107.49	33.84	4
QDZ	河南南阳 Nanyang, Henan	111.97	33.52	6
HKC	河南南阳 Nanyang, Henan	112.02	33.57	6
TSG	河南南阳 Nanyang, Henan	111.72	33.63	6
LJL	河南南阳 Nanyang, Henan	111.70	33.63	4
LYG	甘肃天水 Tianshui, Gansu	106.10	34.23	5
YPC	甘肃陇南 Longnan, Gansu	106.23	33.67	5
HJG	甘肃康县 Kang Xian, Gansu	105.51	33.39	5
MYG	甘肃阳坝镇 Yangba, Gansu	105.74	33.03	6
SNJ	湖北神农架 Shennongjia, Hubei	110.92	31.65	7
XJZ	湖北神农架 Shennongjia, Hubei	110.58	31.59	11
SHJZ	湖北恩施 Enshi, Hubei	109.80	30.16	11
JSZ	重庆金山镇 Jinshan, Chongqing	107.14	29.02	7
DFX	贵州毕节 Bijie, Guizhou	105.88	27.33	12
NYX	贵州毕节 Bijie, Guizhou	105.47	26.70	13

图2 基于“Pcadapt”的湖北枫杨特异性位点检测结果(A)、主成分分析(PCA)聚类结果(B)和基于潜在因素混合模型分析的对于6个气候因子分别进行特异性位点检测结果(C)。红色虚线为p = 0.01阈值线, 红色虚线上方为与该环境因子显著关联的位点。MAF, 次等位基因频率。

Fig. 2 Abnormal single nucleotide polymorphism (SNP) detected in Pterocarya hupehensis based on “Pcadapt” (A), Principal Component Analysis (PCA) (B), and latent factor mixed models analysis based on six environmental factors (C). The red dotted line represents the threshold of p = 0.01, and the sites above the red dotted line are significantly associated with the environmental factor. MAF, minor allele frequency.

表2 湖北枫杨全部种群Mantel和偏Mantel检验结果

Table 2 Mantel and partial Mantel test results for the entire population of Pterocarya hupehensis

Mantel检验 Mantel test	Mantel’s r	p	Mantel检验(每个气候因子) Mantel test (Each climatic factor)	Mantel’s r	p
地理隔离 Isolation by distance	0.23	0.062	等温性 Isothermality	-0.17	0.861
环境隔离 Isolation by environment	0.31	0.002	最冷月份最低气温 Minimum temperature of the coldest month	-0.05	0.668
偏Mantel检验 Partial mantel test			气温年较差 Temperature annual range	-0.07	0.675
地理隔离(控制环境距离) Isolation by distance (Conditioned with environmental distance)	0.08	0.298	最湿季度平均气温 Mean temperature of the wettest quarter	0.09	0.212
环境隔离(控制地理距离) Isolation by environment (Conditioned with geographical distance)	0.23	0.029	最湿月份降水量 Precipitation of the wettest month	0.29	0.003
			降水量季节性变化 Precipitation seasonality	0.34	0.007

图3 对于所有种群进行地理距离和遗传距离、环境距离和遗传距离的Mantel检验结果(A)和对于每个气候因子进行遗传距离与环境距离检测结果(B)。红色斜线代表变量之间显著相关。FST/(1 - FST), 衡量成对种群间遗传分化(遗传距离)。

Fig. 3 Mantel test results showing the relationship between geographic distance and genetic distance, and between environmental distance and genetic distance across all populations (A), as well as the results of the genetic distance versus environmental distance for each individual climate factor (B). Red dashed lines represent significant correlations between variables. FST/(1 - FST), measuring genetic differentiation between paired populations (genetic distance).

图4 湖北枫杨的遗传变异与6种气候因子(A)及地理因素(B)的冗余分析(RDA)和偏冗余分析(pRDA) (C、D)。向量长度表示该环境变量在解释方差中的贡献大小, 箭头之间的角度表示变量之间的相关性。MEM, 莫兰特征向量。bio3, 等温性; bio6, 最冷月份最低气温; bio7, 气温年较差; bio8, 最湿季度平均气温; bio13, 最湿月份降水量; bio15, 降水量季节性变化。

Fig. 4 Redundancy analysis (RDA) of P. hupehensis between genetic variation and six climatic factors (A), and between genetic variation and geographical factors (B). As well as partial redundancy analysis (pRDA) between genetic variation and six climatic factors (C), and between genetic variation and geographical factors (D). The length of the vector represents the contribution of the environment variable to the explained variance, and the angle between the arrows represents the correlation between the variables. MEM, Moran’s eigenvector. bio3, isothermality; bio6, minimum temperature of the coldest month; bio7, temperature annual range; bio8, mean temperature of the wettest quarter; bio13, precipitation of the wettest month; bio15, precipitation seasonality.

表3 湖北枫杨所有种群冗余分析和偏冗余分析结果

Table 3 Redundancy analysis (RDA) and partial RDA analysis results of all populations of Pterocarya hupehensis

环境因子 Environmental factor	冗余分析 RDA			偏冗余分析 Partial RDA
环境因子 Environmental factor	PVE	特征值 Eigenvalue	p	PVE	特征值 Eigenvalue	p
地理 Geography	0.13	3.54	0.001	0.09	2.54	0.001
气候 Climate	0.18	4.06	0.001	0.13	3.17	0.001
等温性 Isothermality	0.03	3.63	0.001	0.03	4.05	0.001
最冷月份最低气温 Minimum temperature of the coldest month	0.03	3.70	0.001	0.02	2.60	0.001
气温年较差 Temperature annual range	0.04	5.62	0.001	0.02	2.92	0.001
最湿季度平均气温 Mean temperature of the wettest quarter	0.02	2.82	0.001	0.03	4.24	0.001
最湿月份降水量 Precipitation of the wettest month	0.05	6.71	0.001	0.01	1.81	0.001
降水量季节性变化 Precipitation seasonality	0.01	1.86	0.003	0.02	3.44	0.001

图5 基于梯度森林(GF, A)和广义相异模型(GDM, C)分析的环境变量对于遗传变异重要性排序图, 遗传组成随环境梯度变化的I样条曲线(GF分析结果) (B), 和为GDM分析的累积重要性曲线(D)。MEM, 莫兰特征向量。bio3, 等温性; bio6, 最冷月份最低气温; bio7, 气温年较差; bio8, 最湿季度平均气温; bio13, 最湿月份降水量; bio15, 降水量季节性变化。

Fig. 5 Environmental variable importance rankings for genetic variation based on Gradient Forest (GF) (A) and Generalized Dissimilarity Model (GDM) (C) analyses, with I-spline curves illustrating genetic composition shifts along environmental gradients (B) and cumulative importance curves (D) in GDM analysis. MEM, Moran’s eigenvector. bio3, isothermality; bio6, minimum temperature of the coldest month; bio7, temperature annual range; bio8, mean temperature of the wettest quarter; bio13, precipitation of the wettest month; bio15, precipitation seasonality.

图6 未来气候情景下的潜在分布区预测(A, B)和非适应性风险分析(RONA) (C, D)结果。3个对于基因组脆弱性影响最大的气候因子展示在图中。MIROC和CMCC两种全球气候模型的数据下载于WorldClim v2.1 (https://www.worldclim.org/data/cmip6/ cmip6_clim2.5m.html)。种群名称缩写的详细信息见表1。

Fig. 6 Potential range projections (A, B) and risk of non-adaptedness analysis (RONA) (C, D) for future climate scenarios. Only the three climate factors that have the greatest impact on genomic vulnerability are shown in the picture. Data of two global climate models (MIROC and CMCC) were downloaded from WorldClim v2.1 (https://www.worldclim.org/data/cmip6/cmip6_clim2.5m. html). Detailed information of abbreviations for each population is shown in Table 1.

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孑遗植物湖北枫杨的环境适应性遗传变异与遗传脆弱性

Environmental adaptive genetic variation and genetic vulnerability of relict plant Pterocarya hupehensis

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