不同生长期樟子松外生菌根真菌群落物种组成及其驱动因素

doi:10.17521/cjpe.2022.0480

植物生态学报 ›› 2023, Vol. 47 ›› Issue (9): 1298-1309.DOI: 10.17521/cjpe.2022.0480 cstr: 32100.14.cjpe.2022.0480

所属专题：菌根真菌

不同生长期樟子松外生菌根真菌群落物种组成及其驱动因素

任悦¹, 高广磊¹^,²^,³^,^*(), 丁国栋¹^,²^,³, 张英¹^,², 赵珮杉¹, 柳叶¹

¹北京林业大学水土保持学院, 北京 100083
²北京林业大学林业生态工程教育部工程研究中心, 北京林业大学水土保持国家林业和草原局重点实验室, 北京 100083
³宁夏盐池毛乌素沙地生态系统国家定位观测研究站, 宁夏盐池 751500

收稿日期:2022-11-28 接受日期:2023-04-26 出版日期:2023-09-20 发布日期:2023-09-28
基金资助:
内蒙古自治区科技计划项目(2022YFHH0131);中央高校基本科研业务费项目(2021ZY47)

Species composition and driving factors of the ectomycorrhizal fungal community associated with Pinus sylvestris var. mongolica at different growth periods

REN Yue¹, GAO Guang-Lei¹^,²^,³^,^*(), DING Guo-Dong¹^,²^,³, ZHANG Ying¹^,², ZHAO Pei-Shan¹, LIU Ye¹

¹School of Soil and Water Conservation, Beijing Forestry University, Beijing 100083, China
²Engineering Research Center of Forestry Ecological Engineering, Ministry of Education, Key Laboratory of State Forestry and Grassland Administration on Soil and Water Conservation, Beijing Forestry University, Beijing 100083, China
³Yanchi Ecology Research Station of the Mu Us Sandy Land, Yanchi, Ningxia 751500, China

Received:2022-11-28 Accepted:2023-04-26 Online:2023-09-20 Published:2023-09-28
Supported by:
Science and Technology Project of Nei Mongol Autonomous Region(2022YFHH0131);Fundamental Research Funds for the Central Universities(2021ZY47)

摘要/Abstract

摘要：

阐明不同生长期樟子松(Pinus sylvestris var. mongolica)外生菌根真菌群落物种组成、分子生态网络特征及其驱动因子, 可为樟子松人工林可持续经营管理提供理论依据。该研究以毛乌素沙地不同树龄(23、33和44年)樟子松为研究对象, 采用野外调查取样、Illumina MiSeq技术和分子生态网络等生物信息学分析相结合的方法, 比较分析生长季初期(4月)、生长旺盛期(7月)和生长季末期(9月)外生菌根真菌群落物种组成、菌群间相互作用关系及群落变化主要影响因子。主要结果有: 1)生长期对樟子松外生菌根真菌丰富度和Chao1指数影响显著, 生长旺盛期Chao1指数和Simpson多样性指数显著高于其他两个生长期; 树龄对外生菌根真菌多样性没有显著影响。2)毛乌素沙地樟子松根尖共鉴定到外生菌根真菌2门4纲7目18科28属; 生长季初期、旺盛期和末期的优势类群分别为棉革菌属(Tomentella)、丝盖伞属(Inocybe)和地孔菌属(Geopora), 不同树龄优势类群均为地孔菌属; 优势类群棉革菌属和丝盖伞属为生长旺盛期和生长季末期的共有指示菌属。3)生长季末期外生菌根真菌网络节点数、边数最大, 其群落结构更加复杂, 菌种间存在较强的相互作用。4)土壤pH和年平均相对湿度是显著影响樟子松外生菌根真菌群落物种组成差异的环境因子。结论: 生长期和树龄均对樟子松外生菌根真菌多样性与群落物种组成产生影响, 其中生长期的作用强于树龄; 外生菌根真菌季节动态分布主要取决于土壤性质和气候条件。

关键词: 樟子松, 外生菌根真菌, 物种组成, 分子生态网络

Abstract:

Aims This study aimed to illustrate community structure, molecular ecological network and driving factors of ectomycorrhizal fungi associated with Pinus sylvestris var. mongolica at different growth periods, and provide a theoretical basis for sustainable management of P. sylvestris var. mongolica plantation.
Methods Pinus sylvestris var. mongolica with different tree ages (23, 33 and 44 a) in Mau Us Sandy Land were targeted. The species compositions, interaction and main drivers of ectomycorrhizal fungi at the early growth period (Apr.), vigorous growth period (July) and the late growth period (Sept.) were identified by field investigation and sampling, illumina high-throughput sequencing and molecular ecological network analysis, respectively.
Important findings 1) The growth period had significant effect on the richness and Chao1 index of ectomycorrhizal fungi, with significantly higher Chao1 and Simpson diversity index in vigorous growth period than in early and late growth periods. The tree age had no significant effect on the ectomycorrhizal fungal diversity index. 2) In Mau Us Sandy Land, the ectomycorrhizal fungi associated with P. sylvestris var. mongolica were identified into 2 phyla, 4 classes, 7 orders, 18 families, and 28 genera. The dominant genera were Tomentella, Inocybe and Geopora at the early, vigorous and late growth periods, respectively. The Tomentella and Inocybe were the common indicator genera in both vigorous and late growth periods. 3) At the end of the growing season, the nodes and edges of the ectomycorrhizal fungal networks were the largest, indicating that the ectomycorrhizal fungal community was more complex and there was strong interaction between fungal species. 4) Soil pH and annual relative humidity were the key environmental factors that significantly affected the community composition of ectomycorrhizal fungi. Our results demonstrated that the diversity and community composition of ectomycorrhizal fungi were affected by the growth stage and tree age, with a stronger effect in growth stage than in tree age. The seasonal dynamic distribution of ectomycorrhizal fungi mainly depended on soil properties and climate conditions.

Key words: Pinus sylvestris var. mongolica, ectomycorrhizal fungi, species composition, molecular ecological network

任悦, 高广磊, 丁国栋, 张英, 赵珮杉, 柳叶. 不同生长期樟子松外生菌根真菌群落物种组成及其驱动因素. 植物生态学报, 2023, 47(9): 1298-1309. DOI: 10.17521/cjpe.2022.0480

REN Yue, GAO Guang-Lei, DING Guo-Dong, ZHANG Ying, ZHAO Pei-Shan, LIU Ye. Species composition and driving factors of the ectomycorrhizal fungal community associated with Pinus sylvestris var. mongolica at different growth periods. Chinese Journal of Plant Ecology, 2023, 47(9): 1298-1309. DOI: 10.17521/cjpe.2022.0480

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2022.0480

https://www.plant-ecology.com/CN/Y2023/V47/I9/1298

图/表 10

表1 陕西榆林樟子松人工林研究样地概况(平均值±标准差)

Table 1 Basic characteristics of the sample areas of Pinus sylvestris var. mongolica plantation in Yulin, Shaanxi Province (mean ± SD)

龄组 Age group	林龄 Stand age (a)	纬度 Longitude (° N)	经度 Longitude (° E)	平均树高 Average tree height (m)	平均胸径 Average tree DBH (cm)	郁闭度 Canopy density
中龄林 MUh	23	38.33	109.72	9.91 ± 1.02	14.15 ± 3.05	0.72
近熟林 MUn	33	38.34	109.73	13.05 ± 0.94	18.63 ± 2.46	0.80
成熟林 MUm	44	38.34	109.73	14.65 ± 0.81	21.98 ± 3.04	0.76

图1 不同生长期(A)和不同树龄(B)樟子松外生菌根真菌可操作分类单元(OTU)韦恩图。Apr., 生长季初期; July, 生长旺盛期; Sept., 生长季末期。MUh, 中龄林; MUm, 成熟林; MUn, 近熟林。

Fig. 1 Venn diagram of ectomycorrhizal fungal operational taxonomic unit (OUT) associated with Pinus sylvestris var. mongolica at different growth period (A) and age group (B). Apr., early growth period; July, vigorous growth period; Sept., late growth period. MUh, middle-aged forest; MUm, mature forest; MUn, nearly mature forest.

图2 樟子松外生菌根真菌相对丰度堆积图(属水平)。图中左半边表示真菌属在不同样地的相对丰度, 右半边表示样地中不同真菌属在不同生长期的相对丰度。其他, 相对丰度<1%的所有真菌属。

Fig. 2 Relative abundance of ectomycorrhizal fungi associated with Pinus sylvestris var. mongolica at genus level. The left half of figure shows the relative abundance of ectomycorrhizal fungal genera in different plots, and the right half shows the relative abundance of different ectomycorrhizal fungal genera at different growth period. Others, all genera with a relative abundance less than 1%.

表2 不同生长期樟子松外生菌根真菌群落α多样性(平均值±标准差)

Table 2 Α diversity of ectomycorrhizal fungal community associated with Pinus sylvestris var. mongolica at different growth periods (mean ± SD)

生长期 Growth period	龄组 Age group	丰富度 Richness	Chao1指数 Chao1 index	ACE指数 ACE index	Shannon-Wiener指数 Shannon-Wiener index	Simpson指数 Simpson index	Pielou指数 Pielou index
Apr.	MUh	13 ± 1^Ba	15.78 ± 2.91^Ba	16.44 ± 0.81^Aa	1.64 ± 0.25^Aa	0.75 ± 0.05^Aa	2.64 ± 0.93^Aa
	MUn	13 ± 1^Ba	14.61 ± 2.96^Ba	20.22 ± 2.17^Aa	1.15 ± 0.45^Aa	0.56 ± 0.17^Aa	1.93 ± 0.49^Ba
	MUm	12 ± 1^Ba	17.00 ± 7.86^Ba	24.65 ± 1.43^Aa	1.02 ± 0.32^Aa	0.46 ± 0.19^Aa	2.43 ± 0.48^Aa
July	MUh	24 ± 5^Aa	28.75 ± 8.74^Aa	35.83 ± 2.72^Aa	1.77 ± 0.19^Aa	0.78 ± 0.03^Aa	3.00 ± 0.83^Aa
	MUn	22 ± 2^Aa	26.67 ± 3.06^Aa	26.62 ± 3.04^Aa	1.38 ± 0.28^Aa	0.64 ± 0.09^Aa	2.60 ± 0.27^ABa
	MUm	23 ± 4^Aa	27.17 ± 6.95^Aa	30.44 ± 3.65^Aa	1.56 ± 0.30^Aa	0.70 ± 0.11^Aa	2.83 ± 0.53^Aa
Sept.	MUh	19 ± 3^Aa	19.92 ± 3.02^Aa	20.94 ± 3.42^Aa	1.16 ± 0.46^Aa	0.54 ± 0.19^Ba	2.63 ± 0.50^Aa
	MUn	23 ± 1^Aa	24.92 ± 1.13^Aa	29.09 ± 3.09^Aa	1.53 ± 0.53^Aa	0.66 ± 0.22^Aa	2.95 ± 0.13^Aa
	MUm	19 ± 5^Aa	26.83 ± 11.73^Aa	26.45 ± 2.41^Aa	1.18 ± 0.54^Aa	0.54 ± 0.20^Aa	2.48 ± 0.77^Aa
F_{growth period}		31.705^**	6.606^**	1.804	1.676	1.955	1.424
F_{age group}		0.462	0.235	0.130	1.075	1.485	0.204
F_{growth period × age group}		1.051	0.352	0.538	1.296	1.249	1.003

图3 不同生长期樟子松外生菌根真菌群落结构。A, 非度量多维尺度(NMDS)分析。B, 相关性聚类热图(top 10属)。Apr., 生长季初期; July, 生长旺盛期; Sept., 生长季末期。MUh, 中龄林; MUm, 成熟林; MUn, 近熟林。Stress, 应力函数值。

Fig. 3 Community structure of the ectomycorrhizal fungi associated with Pinus sylvestris var. mongolica at different growth periods. A, Non-metric multidimensional scaling (NMDS) analysis. B, Corheatmap (top10 genera). Apr., early growth period; July, vigorous growth period; Sept., late growth period. MUh, middle-aged forest; MUm, mature forest; MUn, nearly mature forest.

表3 不同生长期樟子松外生菌根真菌指示菌种

Table 3 Indicator species of ectomycorrhizal fungal community associated with Pinus sylvestris var. mongolica at different growth periods

组别 Group	指示种 Indicator species	属 Genus	指示值 Indicator value	p
Apr.	OTU216	盾盘菌属 Scutellinia	0.970	0.001
July	OTU27	茸盖亚属 Mallocybe	0.976	0.001
	OTU104	茸盖亚属 Mallocybe	0.960	0.003
	OTU20	丝盖伞属 Inocybe	0.975	0.001
	OTU88	丝盖伞属 Inocybe	0.957	0.003
	OTU142	丝盖伞属 Inocybe	0.930	0.001
	OTU892	阿太菌属 Amphinema	0.879	0.001
	OTU368	棉革菌属 Tomentella	0.846	0.028
	OTU441	棉革菌属 Tomentella	0.789	0.047
Sept.	OTU207	丝盖伞属 Inocybe	0.922	0.006
	OTU420	棉革菌属 Tomentella	0.839	0.024
	OTU264	地孔菌属 Geopora	0.815	0.001

图4 不同生长期樟子松外生菌根真菌相互作用。颜色代表不同模块, 连接线代表节点间为正相互作用。Apr., 生长季初期; July, 生长旺盛期; Sept., 生长季末期。MUh, 中龄林; MUm, 成熟林; MUn, 近熟林。

Fig. 4 Interactions of ectomycorrhizal fungi community associated with Pinus sylvestris var. mongolica at different growth periods. Colors represent different modules. Links represent the positive interaction between nodes. Apr., early growth period; July, vigorous growth period; Sept., late growth period. MUh, middle-aged forest; MUm, mature forest; MUn, nearly mature forest.

表4 不同生长期樟子松外生菌根真菌网络拓扑性质

Table 4 Topological characteristics of ectomycorrhizal fungal community associated with Pinus sylvestris var. mongolica at different growth periods

拓扑特征 Topological feature		生长期 Growth period			龄组 Age group
拓扑特征 Topological feature		Apr.	July	Sept.	MUh	MUn	MUm
经验网络 Empirical network	节点 Node	37	65	69	65	67	66
	边 Edge	87	201	241	243	211	201
	模块化 Modularity	0.663	0.730	0.798	0.772	0.819	0.776
	平均度 Average degree	4.703	6.185	6.986	7.477	6.299	6.091
	平均路径长度 Average path length	1.215	1.659	1.159	1.349	1.202	2.120
	平均聚类系数 Average clustering coefficient	0.901	0.911	0.952	0.923	0.941	0.820
	正相关 Positive	87 (100%)	201 (100%)	241 (100%)	243 (100%)	211 (100%)	201 (100%)
随机网络 Random network	平均路径长度 Average path length	1.025	1.512	1.100	1.196	1.087	1.864
随机网络 Random network	平均聚类系数 Average clustering coefficient	0.841	0.865	0.912	0.918	0.921	0.798

表5 樟子松外生菌根真菌属相对丰度与环境因子的冗余分析(RDA)中环境因子的排序

Table 5 Constrained ordination of environmental factors in the redundancy analysis (RDA) of relative abundance of ectomycorrhizal fungal genus associated with Pinus sylvestris var. mongolica and environmental factors

因子 Factor	顺序 Order	RDA1	RDA2	R²	p
pH	1	0.644	-0.765	0.691	0.024
RH_a	2	-0.094	-0.996	0.641	0.028
SD_a	3	-0.627	0.779	0.389	0.134
T_a	4	0.688	-0.726	0.474	0.134
SOC	5	0.974	-0.228	0.365	0.250
P_a	6	0.549	-0.836	0.278	0.410
TN	7	-0.872	0.490	0.196	0.525
SP	8	-0.259	0.966	0.199	0.550
AP	9	0.703	-0.711	0.180	0.584
SWC	10	0.588	-0.809	0.057	0835
AN	11	-0.747	0.665	0.013	0.954
TP	12	0.736	-0.677	0.003	0.992

图5 樟子松外生菌根真菌群落与环境因子的相关关系。A, 外生菌根真菌群落与环境因子的冗余分析(RDA)。B, 外生菌根真菌属相对丰度与土壤因子的相关性分析。C, 环境因子间相关性分析。*, p < 0.05; **, p < 0.01。RDA图中点的大小代表属的相对丰度, 点越大相对丰度越高; 环境因子间相关性的椭圆越扁、颜色越深代表相关性越强, 红色代表正相关, 蓝色代表负相关。AN, 土壤铵态氮含量; AP, 土壤速效磷含量; Pa, 年降水量; RHa, 年平均相对湿度; SDa, 年日照时间; SOC, 土壤有机碳含量; SP, 土壤孔隙度; SWC, 土壤含水量; Ta, 年平均气温; TN, 土壤全氮含量; TP, 土壤全磷含量。

Fig. 5 Relationship of ectomycorrhizal fungal communities and soil properties associated with Pinus sylvestris var. mongolica plantation. A, Redundancy analysis (RDA) between ectomycorrhizal fungi and environmental factors. B, Correlation analysis between relative abundance of main ectomycorrhizal fungal genera and environmental factors. C, Correlation analysis between environmental factors. *, p < 0.05; **, p < 0.01. The dots’ size in the RDA analysis represents the relative abundance of ectomycorrhizal fungal genera, the bigger the size, the higher of the relative abundance. The oblate and the darker the color of the ellipse between soil physical and chemical factors represent the stronger correlation, red represents the positive and blue represents the negative. AN, soil ammonia nitrogen content; AP, soil available phosphorus content; Pa, annual precipitation; RHa, annual relative humidity; SDa, annual sunshine duration; SOC, soil organic carbon content; SP, soil porosity; SWC, soil water content; Ta, annual air temperature; TN, soil total nitrogen content; TP, soil total phosphorus content.

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不同生长期樟子松外生菌根真菌群落物种组成及其驱动因素

Species composition and driving factors of the ectomycorrhizal fungal community associated with Pinus sylvestris var. mongolica at different growth periods

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