新疆野苹果种群遗传结构及其环境适应性

doi:10.17521/cjpe.2022.0024

植物生态学报 ›› 2022, Vol. 46 ›› Issue (9): 1098-1108.DOI: 10.17521/cjpe.2022.0024

新疆野苹果种群遗传结构及其环境适应性

张宏祥¹^,²^,^*(), 闻志彬¹^,², 王茜¹

¹中国科学院新疆生态与地理研究所荒漠与绿洲生态国家重点实验室, 乌鲁木齐 830011
²中国-塔吉克斯坦生物资源保育与利用联合实验室, 新疆抗逆植物基因资源保育与利用重点实验室, 中国科学院新疆生态与地理研究所标本馆, 乌鲁木齐 830011

收稿日期:2022-01-13 接受日期:2022-03-09 出版日期:2022-09-20 发布日期:2022-10-19
通讯作者: 张宏祥
基金资助:
国家自然科学基金(32170391);国家自然科学基金(31870323);中国科学院青年创新促进会项目(2019428)

Population genetic structure of Malus sieversii and environmental adaptations

ZHANG Hong-Xiang¹^,²^,^*(), WEN Zhi-Bin¹^,², WANG Qian¹

¹State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Ürümqi 830011, China
²Sino-Tajikistan Joint Laboratory for Conservation and Utilization of Biological Resources, Xinjiang Key Lab of Conservation and Utilization of Gene Resources, Specimen Museum of Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Ürümqi 830011, China

Received:2022-01-13 Accepted:2022-03-09 Online:2022-09-20 Published:2022-10-19
Contact: ZHANG Hong-Xiang
About author:* E-mail: zhanghx561@ms.xjb.ac.cn
Supported by:
National Natural Science Foundation of China(32170391);National Natural Science Foundation of China(31870323);Project of Youth Innovation Promotion Association of Chinese Academy of Sciences(2019428)

摘要/Abstract

摘要：

新疆野苹果(Malus sieversii)属国家二级保护植物, 是栽培苹果的主要祖先之一。它呈片段化残遗分布于亚洲中部干旱区山地。为了探究影响该物种种群遗传变异的主要环境因子及其适应机制, 该研究选取中国新疆伊犁地区、哈萨克斯坦、吉尔吉斯斯坦分布的10个种群为研究对象, 通过SLAF-seq简化基因组测序获取单核苷酸多态性(SNP)数据。利用ADMIXTURE软件和主成分分析对种群遗传结构进行分型; 利用梯度森林分析和冗余分析评估影响种群遗传变异的主要环境因子; 运用潜在因素混合模型来检测新疆野苹果种群适应局部环境的基因组位点。结果显示: 10个种群可以区分出2个遗传谱系; 谱系A主导东部种群, 谱系B主导西部种群, 而中部种群则出现了两个谱系的交汇; 种群空间遗传结构呈现出沿经度方向上的地理替代格局。气温年较差(bio 07)和气温季节性变化(bio 04)是影响新疆野苹果种群等位基因频率变化的两个最重要环境因子。经注释发现15个环境关联基因位点与植物响应干旱、高盐、冷热等非生物胁迫的很多生理过程相关。综上所述, 新疆野苹果对环境适应的主要压力来自气温条件的变化, 生理适应可能是其响应环境胁迫的主要机制。

关键词: 新疆野苹果, 遗传结构, 环境适应性, 地理替代, 生理适应

Abstract:

Aims Malus sieversii, being listed as a national second-class protected plant in China, is recognized as one of the wild ancestors for domesticated apple. It is fragmentally distributed in arid mountains of the Central Asian. Here, we aimed to investigate the main environment variables shaping population genetic variations and the genetic adaptation in response to these environment variables for this species.

Methods We collected ten M. sieversii populations from Yili Prefecture of China, Kazakhstan and Kyrgyzstan. Single nucleotide polymorphism (SNP) dataset was generated by SLAF-seq. Population genetic structure was inferred using the ADMIXTURE software and principal component analysis. Main environment variables shaping population genetic variations were assessed by gradient forest analysis and redundancy analysis. Tests of associated outlier loci with environmental variations were carried out by latent factor mixed models, which was used to access genetic signatures of local adaptation.

Important findings Ten populations were clustered into two lineages. Lineage A dominated eastern populations, while Lineage B mainly distributed in western populations. Two lineages were mixed in central populations, and an obvious pattern of geographical substitute along the longitude direction was found. The most important environment variables that influence the change of allele frequency for M. sieversii populations were temperature annual range (bio 07) and temperature seasonality (bio 04). Fifteen loci having a significant association with environmental variables were successfully annotated. Most of them were genes related to abiotic stress responses and stress-induced physiological adaptations, such as drought, salt and cold. In conclusion, temperature variation is the main factor that drives the adaptation of M. sieversii to environments. Physiological adaptations, as indicated by the above candidate loci, were most likely the main mechanism related to abiotic stress response.

Key words: Malus sieversii, genetic structure, environmental adaptation, geographical substitute, physiological adaptation

张宏祥, 闻志彬, 王茜. 新疆野苹果种群遗传结构及其环境适应性. 植物生态学报, 2022, 46(9): 1098-1108. DOI: 10.17521/cjpe.2022.0024

ZHANG Hong-Xiang, WEN Zhi-Bin, WANG Qian. Population genetic structure of Malus sieversii and environmental adaptations. Chinese Journal of Plant Ecology, 2022, 46(9): 1098-1108. DOI: 10.17521/cjpe.2022.0024

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2022.0024

https://www.plant-ecology.com/CN/Y2022/V46/I9/1098

图/表 7

表1 新疆野苹果10个种群的编号、来源地、经纬度信息及其遗传多样性

Table 1 Code, sampling sites, geographical locations and genetic diversity of ten populations of Malus sieversii

编号 Code	来源地 Sampling site	经度 Longitude (° E)	纬度 Latitude (° N)	观察杂合度 Observed heterozygosity	期望杂合度 Expected heterozygosity
C1	中国新疆 Xinjiang, China	83.61	43.38	0.328 4 (0.270 0)	0.271 5 (0.174 3)
C2	中国新疆 Xinjiang, China	82.86	43.26	0.316 5 (0.265 3)	0.264 1 (0.177 1)
C3	中国新疆 Xinjiang, China	81.62	44.12	0.332 0 (0.280 2)	0.268 7 (0.179 3)
C4	中国新疆 Xinjiang, China	80.78	44.43	0.329 0 (0.255 2)	0.276 1 (0.168 5)
C5	哈萨克斯坦东部 Eastern Kazakhstan	77.67	43.37	0.339 4 (0.244 8)	0.288 2 (0.161 4)
C6	哈萨克斯坦东部 Eastern Kazakhstan	77.68	43.36	0.337 6 (0.243 9)	0.289 1 (0.160 1)
C7	吉尔吉斯斯坦 Kyrgyzstan	73.62	41.90	0.346 5 (0.254 8)	0.284 9 (0.165 9)
C8	吉尔吉斯斯坦 Kyrgyzstan	72.96	41.36	0.332 6 (0.245 8)	0.284 3 (0.165 2)
C9	哈萨克斯坦西部 Western Kazakhstan	70.26	42.67	0.332 3 (0.246 2)	0.286 5 (0.163 2)
C10	哈萨克斯坦西部 Western Kazakhstan	69.95	41.94	0.326 7 (0.279 1)	0.269 0 (0.180 4)

图1 10个新疆野苹果种群的地理位置和谱系分布。饼图表示每个种群中由ADMIXTURE划分的两个不同遗传谱系的平均占比; 蓝色代表谱系A, 橙色代表谱系B。图中种群编码信息与表1一致。

Fig. 1 Geographical locations and lineage distributions of ten Malus sieversii populations sampled. Pie charts show mean proportions of lineage memberships for each population from the ADMIXTURE program at K = 2; blue indicates lineage A, while orange indicates lineage B. Population codes are consistent with Table 1.

图2 新疆野苹果10个种群105个个体的谱系分型与分组。A, ADMIXTURE的谱系分型结果。蓝色柱代表源于谱系A的可能性Q值, 橙色柱代表源于谱系B的可能性Q值。B, 主成分分析(PCA)分型结果。源于某一谱系的可能性Q值≥0.65的个体, 则确定为该谱系个体; 而两个谱系的可能性Q值均<0.65的个体, 确定为混合谱系个体。C, 最大似然法(ML)系统进化树结果。节点附近的数值为该节点的支持率(%)。图中种群编码信息与表1一致。

Fig. 2 Genetic clustering of the 105 individuals from ten populations of Malus sieversii. A, Result based on ADMIXTURE at K = 2. Blue columns indicate the Q estimates (possibility values) of lineage A, while orange columns indicate lineage B. B, Result based on principal component analysis (PCA). Individuals of each cluster were divided under the threshold of Q estimates (possibility values) ≥0.65, while individuals with Q estimates < 0.65 were defined as admixed. C, Result based on maximum-likelihood phylogenetic tree. Numbers near the branches showed the ultrafast bootstrap values of the nodes (%). Population codes are consistent with Table 1.

图3 梯度森林分析结果。A, 用于解释遗传变异的环境因子的R2加权重要性。B, 等位基因变异随6个重要环境因子梯度变化的累积重要性。

Fig. 3 Results of gradient forest (GF) analysis. A, R2-weighted importance of environmental variables that explain genetic gradients. B, Cumulative importance of allelic change along the first six environmental gradients.

图4 6个重要环境因子与遗传变异间关系的冗余分析(RDA)。灰色大圆点表示不同的个体, 小黑点表示不同单核苷酸多态性(SNP)位点。bio 02, 平均气温日较差; bio 04, 气温季节性变化; bio 07, 气温年较差; bio 11, 最冷季平均气温; bio 16, 最湿季降水量; bio 19, 最冷季降水量。

Fig. 4 Redundancy analysis (RDA) showing the relationship between environmental variables and genetic variations. Individuals are larger gray points. Small black points are single nucleotide polymorphism (SNP). bio 02, mean diurnal temperature range; bio 04, temperature seasonality; bio 07, temperature annual range; bio 11, mean temperature of the coldest quarter; bio 16, precipitation of the wettest quarter; bio 19, precipitation of the coldest quarter.

表2 6个重要环境因子的冗余分析(RDA)

Table 2 Redundancy analysis (RDA) based on six important environmental variables

环境因子 Environmental variable	约束比例 Constrained proportion	F	p
bio 07	0.019 3	2.031	0.001
bio 04	0.018 6	1.951	0.001
bio 11	0.017 4	1.827	0.001
bio 16	0.017 9	1.883	0.001
bio 02	0.017 7	1.860	0.001
bio 19	0.018 0	1.887	0.001

表3 基于LFMM分析识别并比对到栽培苹果参考基因组上的15个适应性位点

Table 3 List of 15 candidate loci under selection based on LFMM analyses that alignment to the genome of Malus domestica

位点编号 Loci ID	适应的气候因子 Adapted climate	序列功能描述 Sequence description	同源性E值 Blastn E-value
1223^*	bio 04	伴侣蛋白clpb1 Chaperone protein clpb1-like	1.00E-101
2427^*	bio 04, bio 07	gdsl酯酶/脂肪酶at1g54790 x4亚型 gdsl esterase/lipase at1g54790-like isoform x4	1.00E-101
2666^*	bio 04	自噬相关蛋白23 x2亚型 Autophagy-related protein 23-like isoform x2	1.00E-101
3144	bio 04	12-氧代植二烯酸还原酶11 x2亚型 Putative 12-oxophytodienoate reductase 11 isoform x2	1.00E-101
3157^*	bio 04	无义转录物upf3调控因子x6亚型 Regulator of nonsense transcripts upf3-like isoform x6	1.00E-101
4537	bio 02, bio 04, bio 07	电压门控钾通道亚基 Probable voltage-gated potassium channel subunit beta	1.00E-101
5799^*	bio 11	核糖体生物合成蛋白brx1-2 Ribosome biogenesis protein brx1 homolog 2-like	1.00E-101
5897^*	bio 04	酰基辅酶A硫酯酶, 线粒体 Acyl-coenzyme a thioesterase 9, mitochondrial-like	1.00E-101
6586	bio 16	苯丙氨酸-tRNA连接酶α亚基, 细胞质 Phenylalanine-tRNA ligase alpha subunit, cytoplasmic	1.00E-101
6766	bio 04	2-异丙基苹果酸合酶 2-isopropylmalate synthase a-like	1.00E-101
6936	bio 16	三角状五肽重复蛋白at4g21065 Pentatricopeptide repeat-containing protein at4g21065	1.00E-101
8821	bio 04	谷酰基tRNA转移酶亚基A, 叶绿体/线粒体x1亚型 Glutamyl-tRNA(Gln) amidotransferase subunit A, chloroplastic/mitochondrial-like isoform x1	1.00E-101
9378	bio 04	转录因子myb3r-1 Transcription factor myb3r-1-like	1.00E-101
9683	bio 04	丝氨酸/苏氨酸蛋白激酶蛋白ccr4 Serine/threonine-protein kinase-like protein ccr4	1.00E-101
9684^*	bio 04	磷脂酰肌醇磷酸酶sac1 x1亚型 Phosphoinositide phosphatase sac1 isoform x1	1.00E-101

表3 基于LFMM分析识别并比对到栽培苹果参考基因组上的15个适应性位点

Table 3 List of 15 candidate loci under selection based on LFMM analyses that alignment to the genome of Malus domestica

位点编号 Loci ID	适应的气候因子 Adapted climate	序列功能描述 Sequence description	同源性E值 Blastn E-value
1223^*	bio 04	伴侣蛋白clpb1 Chaperone protein clpb1-like	1.00E-101
2427^*	bio 04, bio 07	gdsl酯酶/脂肪酶at1g54790 x4亚型 gdsl esterase/lipase at1g54790-like isoform x4	1.00E-101
2666^*	bio 04	自噬相关蛋白23 x2亚型 Autophagy-related protein 23-like isoform x2	1.00E-101
3144	bio 04	12-氧代植二烯酸还原酶11 x2亚型 Putative 12-oxophytodienoate reductase 11 isoform x2	1.00E-101
3157^*	bio 04	无义转录物upf3调控因子x6亚型 Regulator of nonsense transcripts upf3-like isoform x6	1.00E-101
4537	bio 02, bio 04, bio 07	电压门控钾通道亚基 Probable voltage-gated potassium channel subunit beta	1.00E-101
5799^*	bio 11	核糖体生物合成蛋白brx1-2 Ribosome biogenesis protein brx1 homolog 2-like	1.00E-101
5897^*	bio 04	酰基辅酶A硫酯酶, 线粒体 Acyl-coenzyme a thioesterase 9, mitochondrial-like	1.00E-101
6586	bio 16	苯丙氨酸-tRNA连接酶α亚基, 细胞质 Phenylalanine-tRNA ligase alpha subunit, cytoplasmic	1.00E-101
6766	bio 04	2-异丙基苹果酸合酶 2-isopropylmalate synthase a-like	1.00E-101
6936	bio 16	三角状五肽重复蛋白at4g21065 Pentatricopeptide repeat-containing protein at4g21065	1.00E-101
8821	bio 04	谷酰基tRNA转移酶亚基A, 叶绿体/线粒体x1亚型 Glutamyl-tRNA(Gln) amidotransferase subunit A, chloroplastic/mitochondrial-like isoform x1	1.00E-101
9378	bio 04	转录因子myb3r-1 Transcription factor myb3r-1-like	1.00E-101
9683	bio 04	丝氨酸/苏氨酸蛋白激酶蛋白ccr4 Serine/threonine-protein kinase-like protein ccr4	1.00E-101
9684^*	bio 04	磷脂酰肌醇磷酸酶sac1 x1亚型 Phosphoinositide phosphatase sac1 isoform x1	1.00E-101

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新疆野苹果种群遗传结构及其环境适应性

Population genetic structure of Malus sieversii and environmental adaptations

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