尖峰岭热带山地雨林根部真菌-植物互作网络结构特征

doi:10.17520/biods.2018339

生物多样性 ›› 2019, Vol. 27 ›› Issue (3): 314-326. DOI: 10.17520/biods.2018339

尖峰岭热带山地雨林根部真菌-植物互作网络结构特征

杨思琪¹,张琪¹,宋希强¹,王健¹,李意德²,许涵²,郭守玉³,丁琼^1,*()

1 海南大学热带农林学院环南海陆域生物多样性研究中心, 海口 570228
2 中国林业科学研究院热带林业研究所, 广州 510520
3 中国科学院微生物研究所真菌学国家重点实验室, 北京 100101

收稿日期:2018-12-25 接受日期:2019-02-27 出版日期:2019-03-20 发布日期:2019-04-09
通讯作者: 丁琼
基金资助:
国家自然科学基金(31360107);国家自然科学基金(31670628);中国林业科学研究院中央级公益性科研院所基本科研业务费专项资金(CAFYBB2017ZE01)

Structural features of root-associated fungus-plant interaction networks in the tropical montane rain forest of Jianfengling, China

Yang Siqi¹,Zhang Qi¹,Song Xiqiang¹,Wang Jian¹,Li Yide²,Xu Han²,Guo Shouyu³,Ding Qiong^1,*()

1 Research Center for Terrestrial Biodiversity of the South China Sea, Institute of Tropical Agriculture and Forestry, Hainan University, Haikou 570228
2 Research Institute of Tropical Forestry, Chinese Academy of Forestry, Guangzhou 510520
3 State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101

Received:2018-12-25 Accepted:2019-02-27 Online:2019-03-20 Published:2019-04-09
Contact: Ding Qiong

1. 附录1 尖峰岭热带山地雨林核心真菌的谱系和生态类型分类.xls(131KB)

摘要/Abstract

摘要：

不同功能群的根部真菌可能会与植物差异性地互作, 并进一步影响地下真菌与植物群落构建。本研究采用Illumina Miseq测序方法检测了海南尖峰岭热带山地雨林中常见植物的根部真菌; 采用网络分析法比较了丛枝菌根(AM)真菌、外生菌根(ECM)真菌, 以及所有根部真菌与植物互作的二分网络(bipartite networks)结构特性。从槭树科、番荔枝科、夹竹桃科、冬青科、棕榈科、壳斗科、樟科和木犀科等8科植物的根系中, 检测到297,831条真菌ITS1序列, 这些序列被划为1,279个真菌分类单元(OTUs), 其中子囊菌门748个、担子菌门354个、球囊菌亚门80个, 以及未知真菌97个。核心根部真菌群落(420个OTUs)中, 至少有三类不同生态功能的真菌常见, 即丛枝菌根真菌(40个OTUs, 占总序列数23.4%)、外生菌根真菌(48个OTUs, 13.9%)和腐生型真菌(83个OTUs, 19.8%)。尖峰岭山地雨林根部真菌-植物互作网络结构特性的指标普遍显著高于/低于假定物种随机互作的零模型期待值。在群落水平, 不同功能型的根部真菌-植物互作网络表现出不同或相反的结构特性, 如丛枝菌根互作网络表现为比零模型预测值高的嵌套性和连接性, 以及比零模型低的专一性, 而外生菌根互作网络呈现出比零模型预测值低的嵌套性和连接性, 以及比零模型高的专一性。在功能群水平, 植物的生态位重叠度在AM互作网络高, 而ECM互作网络低; 真菌的生态位宽度在ECM互作网络窄, 而在AM互作网络较宽。共现(co-occurrence)网络分析进一步揭示, ECM群落的物种对资源的高度种间竞争(植物、真菌高C-score), 以及AM群落的物种无明显种间竞争(低C-score), 可能分别是形成反嵌套ECM互作网络及高嵌套AM互作网络结构的原因。上述结果说明, 尖峰岭山地雨林中至少有两种及以上的种间互作机制调节群落构建: 驱动AM互作网络冗余(nestedness)及ECM互作网络的高生态位分化(专一性)。本研究在同一个森林内探讨了不同功能型的真菌-植物互作特性, 对深入理解热带森林的物种共存机制和生态恢复具有重要意义。

关键词: 根部真菌, 热带山地雨林, 互作网络, 嵌套性, 专一性

Abstract

Functionally diverse root-associated fungi may differentially interact with host plants, potentially affecting the assembly processes of belowground plant and fungi communities. Here, we applied the Illumina Miseq sequencing technique to identify root-associated fungi of plants which were co-dominant in a tropical montane rain forest on Hainan Island, China. Structural features of bipartite networks were compared among the whole root-associated, arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) fungus-plant interactions. A total of 297,831 fungal ITS1 sequences were obtained from eight families including Aceraceae, Annonaceae, Apocynaceae, Aquifoliaceae, Arecaceae, Fagaceae, Lauraceae, and Oleaceae. Fungal sequences were assigned to 1,279 OTUs comprised of Ascomycota (748 OTUs), Basidiomycota (354), Glomeromycota (80), and unidentified fungi (97). At least three functional groups of fungi i.e. putatively ECM (40 OTUs, represented 23.4% of the total fungal reads), AM (40, 13.9%) and saprophyte (83, 19.8%) were prevalent in the core root-associated fungal community (420 OTUs) of the tropical montane rain forest. Network analysis indicated that AM, ECM and root-associated fungus-plant interaction network showed structural features which cannot be predicate by null models assuming species interact randomly. Community level indices behaved differently among different ecotypes of fungus-plant interactions. Specifically, the degree of nestedness (NODF) and connectance were higher, while specialization was lower in the AM interaction network than the expected values from null models. In contrast, the ECM interaction network had a significantly higher degree of specialization and lower nestedness and connectance than the null models. At guild levels, plant niche overlap of AM and ECM interactions are higher and lower than the null model, respectively. Niche breadth of ECM fungi was narrower than that of AM fungi. Co-occurrence patterns of plant and fungus further confirmed competition for resources was intense in ECM interaction network (high C-score of both plants and fungi) and weak in the AM interaction network (low C-score). These findings suggest that at least two modes of interspecific interactions are critical for the assembly and coexistence of root-associated fungal communities, i.e. redundancy (nestedness) of AM interactions, and niche differentiation (specialization) of ECM interactions. Here we provide a comprehensive exploration of the interactions among functionally diverse root-associated fungal guild within a forest, which is key to understand the mechanisms maintaining species coexistence in tropical forests.

Key words: root-associated fungi, tropical montane rain forest, interaction network, nestedness, specialization

杨思琪,张琪,宋希强,王健,李意德,许涵,郭守玉,丁琼 (2019) 尖峰岭热带山地雨林根部真菌-植物互作网络结构特征. 生物多样性, 27, 314-326. DOI: 10.17520/biods.2018339.

Yang Siqi,Zhang Qi,Song Xiqiang,Wang Jian,Li Yide,Xu Han,Guo Shouyu,Ding Qiong (2019) Structural features of root-associated fungus-plant interaction networks in the tropical montane rain forest of Jianfengling, China. Biodiversity Science, 27, 314-326. DOI: 10.17520/biods.2018339.

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链接本文: https://www.biodiversity-science.net/CN/10.17520/biods.2018339

https://www.biodiversity-science.net/CN/Y2019/V27/I3/314

图/表 6

图1 尖峰岭热带山地雨林8科植物根部真菌物种累积曲线

Fig. 1 Rarefaction curves of root-associated fungi of eight plant families in the tropical montane rain forest of Jianfengling

表1 尖峰岭热带山地雨林8科植物的根部真菌群落物种丰富度和多样性

Table 1 Species diversity and richness of root-associated fungal community of eight plant families in the tropical montane rain forest of Jianfengling

宿主植物 Host plant	根样品数 No. of root samples	真菌物种数 / reads No. of fungal species/reads	核心真菌物种数 / reads No. of core fungal species/reads	Shannon多样性指数 Shannon diversity index
槭树科 Aceraceae	34	701 / 31,589	328 / 29,817	3.97
番荔枝科 Annonaceae	32	440 / 31,588	256 / 30,846	2.88
夹竹桃科 Apocynaceae	41	434 / 31,589	277 / 31,134	2.58
冬青科 Aquifoliaceae	39	675 / 31,588	334 / 29,932	4.05
棕榈科 Arecaceae	21	436 / 31,589	264 / 30,894	3.12
壳斗科 Fagaceae	31	359 / 31,589	217 / 30,983	2.58
樟科 Lauraceae	35	463 / 31,589	261 / 30,508	4.04
木犀科 Oleaceae	34	546 / 31,589	302 / 30,527	3.72

图2 尖峰岭热带山地雨林8科植物的根部真菌目组成差异。每科植物对应的左柱与右柱分别为OTUs和reads百分比。

Fig. 2 Compositional differences of root-associated fungi by order among the eight plant families in the tropical montane rain forest of Jianfengling. For each plant family, left and right column are percentage of OTUs and reads, respectively.

图3 尖峰岭热带山地雨林8科植物的根部不同共位群和营养型真菌的序列百分比组成差异

Fig. 3 Compositional differences in reads of root-associated fungi by guilds and trophic modes of the eight plant families in the tropical montane rain forest of Jianfengling

图4 尖峰岭热带山地雨林根部真菌与植物的种间相互作用网络结构(左)与嵌套性(NODF)密度函数图及嵌套性实际观察值 (红色垂直线)(右)。(A)丛枝菌根互作网络; (B)外生菌根互作网络; (C)所有根部真菌-植物互作网络。Acer: 槭树科; Anno: 番荔枝科; Apoc: 夹竹桃科; Aqui: 冬青科; Arec: 棕榈科; Faga: 壳斗科; 灰色连线代表真菌与宿主的种间互作, 线宽对应互作强弱。

Fig. 4 Root-associated fungus-plant interaction networks (left) with density plots showing the distribution of nestedness (NODF) predicted by Patefiled’s null model (right) and observed nestedness (red vertical line) in tropical montane rain forest of Jianfenling Mountain Hainan Island. (A) and (B) are partial networks of AM and ECM interactions, and (C) is the whole root-associated fungus-plant interaction network. Acer, Aceraceae; Anno, Annoaceae; Apoc, Apocynaceae; Aqui, Aquifoliaceae; Arec, Arecaceae; Faga, Fagaceae; Laur, Lauraceae; Olea, Oleaceae. Interactions between plant and fungi are indicated by grey lines with thickness proportional to interaction strength.

表2 根部真菌-植物互作网络结构特性指数

Table 2 Structural features of root-associated fungus-plant interaction networks

	丛枝菌根网络 Arbuscular mycorrhizal network		外生菌根网络 Ectomycorrhizal network		根部真菌-植物互作网络 Root-associated fungus-plant network
	观察值 Observed	零模型 Null model	观察值 Observed	零模型 Null model	观察值 Observed	零模型 Null model
网络嵌套性 Nestedness metric based on overlap and decreasing fill, NODF	68.39	60.70	26.06	58.36	32.59	9.40
网络加权嵌套性 Weighted NODF	45.12	53.76	18.04	48.44	20.46	7.69
网络专一性 Specialization (H°₂)	0.31	0.01	0.81	0.01	0.54	0.01
网络连接性 Connectance	0.42	0.88	0.21	0.89	0.26	0.99
植物生态位重叠 Niche overlap of plants	0.46	0.99	0.11	0.99	0.25	0.99
真菌生态位重叠 Niche overlap of fungi	0.35	0.97	0.39	0.98	0.19	0.91
植物的伙伴多样性 Generality of plants	5.46	7.87	5.32	10.92	34.14	87.31
真菌的伙伴多样性 Vulnerability of fungi	3.41	4.84	1.28	2.74	3.16	7.95
植物Checkboard值 C-score of plants	0.17	0.28	0.62	0.48	0.38	0.96
真菌Checkboard值 C-score of fungi	0.24	0.02	0.52	0.43	0.62	0.85

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尖峰岭热带山地雨林根部真菌-植物互作网络结构特征

Structural features of root-associated fungus-plant interaction networks in the tropical montane rain forest of Jianfengling, China

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