北京地区油松与大叶黄杨叶际表生真菌多样性及群落组成

doi:10.17520/biods.2023498

生物多样性 ›› 2024, Vol. 32 ›› Issue (7): 23498. DOI: 10.17520/biods.2023498 cstr: 32101.14.biods.2023498

• 研究报告: 微生物多样性 • 上一篇下一篇

北京地区油松与大叶黄杨叶际表生真菌多样性及群落组成

崔玉进(), 李婉莹, 周青青, 赵恒, 吴芳^*()(), 员瑗^*()()

北京林业大学生态与自然保护学院, 林木资源高效生产全国重点实验室, 北京 100083

收稿日期:2023-12-28 接受日期:2024-05-06 出版日期:2024-07-20 发布日期:2024-06-12
通讯作者: *E-mail: fangwubjfu2014@bjfu.edu.cn; yuanyuan1018@bjfu.edu.cn
基金资助:
中央高校基本科研业务费专项资金(QNTD202307)

Diversity and community composition of epiphytic fungi in the phyllosphere of Pinus tabuliformis and Euonymus japonicus in Beijing, northern China

Yujin Cui(), Wanying Li, Qingqing Zhou, Heng Zhao, Fang Wu^*()(), Yuan Yuan^*()()

State Key Laboratory of Efficient Production of Forest Resources, School of Ecology and Nature Conservation, Beijing Forestry University, Beijing 100083

Received:2023-12-28 Accepted:2024-05-06 Online:2024-07-20 Published:2024-06-12
Contact: *E-mail: fangwubjfu2014@bjfu.edu.cn; yuanyuan1018@bjfu.edu.cn
Supported by:
Central Universities(QNTD202307)

摘要/Abstract

摘要：

叶际真菌在影响植物健康和促进生物地球化学循环等方面发挥着重要作用。然而, 目前还缺乏北京城市绿化树木叶际表生真菌多样性与群落组成的研究。本研究以北京常见的绿化树木油松(Pinus tabuliformis)与大叶黄杨(Euonymus japonicus)为研究对象, 对市中心向北的4个采样点(安定门地区、和平街地区、亚运村地区和北七家地区), 及4个月份(一月、四月、七月和十一月)的树木叶际表生真菌通过高通量测序技术进行多样性及群落组成研究。结果表明, 油松与大叶黄杨分别得到2,051和1,970个扩增子变异特征序列(ASVs), 其中座囊菌纲、锤舌菌纲和银耳纲是优势菌纲。不同地点间, 叶际表生真菌的α多样性指数由市中心向北呈现先降低后升高的变化趋势; 4个月份间, 油松的α多样性指数存在差异, 大叶黄杨则均为十一月最高。NMDS分析表明两种常绿树木间叶际表生真菌群落组成存在显著差异(ANOSIM, P = 0.001)。线性判别分析表明, 油松的差异指示属为短柄霉属(Aureobasidium)、拟盾壳霉属(Paraconiothyrium)、圆盘菌属(Orbilia)等7属, 大叶黄杨为白粉菌属(Erysiphe)、链格孢属(Alternaria)、黑孢霉属(Nigrospora)等7属。回归分析表明, 平均降水与油松叶际表生真菌丰富度呈显著正相关关系, 与大叶黄杨叶际表生真菌丰富度呈显著负相关。通过网络分析将油松中的空泡茎点霉属(Vacuiphoma)和大叶黄杨中的空泡茎点霉属(Vacuiphoma)、木拉克属(Mrakia)、弯孢属(Curvularia)、白粉菌属(Erysiphe)确定为核心节点菌属。真菌群落功能预测得出腐生功能类群和病理功能类群分别是油松和大叶黄杨叶际表生真菌的主要类群。深入研究绿化树木的叶际表生真菌多样性及其作用有助于在未来城市绿化管理中更科学地发挥叶际表生真菌的生态功能。

关键词: 叶际表生真菌, 城市绿化树木, Illumina MiSeq测序, 真菌多样性, 核心菌群, 网络分析

Abstract

Aims Phyllosphere fungi play crucial roles in influencing plant health and contributing to biogeochemical cycling. This study aims to investigate the diversity and community structure of epiphytic fungi in the phyllosphere of two most common evergreen trees in Beijing, namely Pinus tabuliformis and Euonymus japonicus to provide the basic data for management of urban evergreen trees.

Methods In this study, we collected leaves samples from four sites in Beijing (Andingmen area, Hepingjie area, Yayuncun area, and Beiqijia area) during four seasons (January, April, July and November) and analyzed the diversity and community composition of epiphytic fungi using high-throughput sequencing technique.

Results A total of 2,051 amplicon sequence variants (ASVs) was obtained from epiphytic fungi on P. tabuliformis while 1,970 ASVs were obtained from those on E. japonicus. The epiphytic fungi were dominated by Dothideomycetes, Leotiomycetes, and Tremellomycetes. Alpha diversity indices (Shannon diversity index, Chao1 richness index, Pielou evenness index) for epiphytic fungi varied among sampling plots but consistently showed lowest values at Hepingjie. The diversity showed a decreasing and then increasing trend from the center to north of the city. The three alpha diversity indices of fungi in P. tabuliformis varied in different months, while November had the highest index of fungi in E. japonicus during the four seasons. Result of non-metric multidimensional scaling revealed significant differences between composition patterns of epiphytic fungal communities associated with these two species (ANOSIM, P= 0.001). Linear discriminant analysis effect size identified significant biomarkers specific to each studied species, seven genera (e.g., Aureobasidium, Paraconiothyrium, Orbilia) served as biomarkers for P. tabuliformis, while seven fungal genera (e.g., Erysiphe, Alternaria, Nigrospora) represented biomarkers for E. japonicus. Regression analyses showed that mean precipitation was significantly and positively correlated with the abundance of epiphytic fungi in P. tabuliformis, and significantly and negatively correlated with the abundance of epiphytic fungi in E. japonicus. Network analysis identified the dominant core fungal genera for E. japonicus are Vacuiphoma, Mrakia, Curvularia, and Erysiphe, whereas Vacuiphoma was single core fungal genus for P. tabuliformis. The main functional groups of epiphytic fungi in the phyllosphere of P. tabuliformis and E. japonicus were pathotrophic and saprotrophic, respectively.

Conclusion The results of this study indicate that there is a significant difference in the composition of the epiphytic fungi in the phyllosphere between the two evergreen trees species and there are some patterns in the α diversity changes of different sites and seasons. Plant leaf diseases are most severe in April and should be emphasized for prevention and control.

Key words: epiphytic fungi in the phyllosphere, urban greening trees, Illumina MiSeq sequencing, fungal diversity, core fungal communities, network analysis

崔玉进, 李婉莹, 周青青, 赵恒, 吴芳, 员瑗 (2024) 北京地区油松与大叶黄杨叶际表生真菌多样性及群落组成. 生物多样性, 32, 23498. DOI: 10.17520/biods.2023498.

Yujin Cui, Wanying Li, Qingqing Zhou, Heng Zhao, Fang Wu, Yuan Yuan (2024) Diversity and community composition of epiphytic fungi in the phyllosphere of Pinus tabuliformis and Euonymus japonicus in Beijing, northern China. Biodiversity Science, 32, 23498. DOI: 10.17520/biods.2023498.

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链接本文: https://www.biodiversity-science.net/CN/10.17520/biods.2023498

https://www.biodiversity-science.net/CN/Y2024/V32/I7/23498

图/表 14

图1 油松与大叶黄杨样品的样点布局示意图

Fig. 1 The sampling sites of Pinus tabuliformis and Euonymus japonicus samples. ADM, Andingmen; HPJ, Hepingjie; YYC, Yayuncun; BQJ, Beiqijia.

图2 不同分组真菌的ASVs分布Venn图。A: 油松的不同采样地点之间; B: 油松的不同季节之间; C: 黄杨的不同采样地点之间; D: 黄杨的不同季节之间; E: 两种树木之间。

Fig. 2 Venn diagram of distribution of ASVs for different groups of fungi. A, Pinus tabuliformis in different sampling plots; B, P. tabuliformis in different seasons; C, Euonymus japonicus in different sampling plots; D, E. japonicus in different seasons; E, Between the two trees species.

表1 油松与大叶黄杨不同样点间的叶际表生真菌α多样性

Table 1 The alpha diversity index of epiphytic fungi in the phyllosphere of Pinus tabuliformis and Euonymus japonicus among different sampling plots

树种 Tree species	样点 Sample plot	Shannon 多样性指数 Shannon diversity index	Chao1丰富度指数 Chao1 richness index	Pielou均匀度指数 Pielou evenness index
油松 Pinus tabuliformis	安定门 ADM	3.92 ± 0.64^a	193.63 ± 83.48^a	0.53 ± 0.06^a
	和平街 HPJ	3.57 ± 1.06^a	161.04 ± 74.94^a	0.50 ± 0.13^a
	亚运村 YYC	3.87 ± 0.43^a	171.96 ± 60.35^a	0.52 ± 0.05^a
	北七家 BQJ	4.03 ± 0.42^a	174.95 ± 56.75^a	0.55 ± 0.07^a
大叶黄杨Euonymus japonicus	安定门 ADM	3.47 ± 0.62^a	190.72 ± 58.41^a	0.46 ± 0.07^a
	和平街 HPJ	2.69 ± 0.37^b	129.80 ± 39.43^b	0.39 ± 0.046^b
	亚运村 YYC	2.77 ± 0.98^b	143.34 ± 68.27^b	0.40 ± 0.13^b
	北七家 BQJ	3.06 ± 0.66^ab	192.09 ± 77.21^a	0.41 ± 0.06^b

图3 油松与大叶黄杨的叶际表生真菌在不同样点间的多样性与纲水平群落组成。A: 油松的α多样性指数; B: 大叶黄杨的α多样性指数; C: 油松的NMDS分析; D: 大叶黄杨的NMDS分析; E: 油松的群落结构; F: 大叶黄杨的群落结构。箱线图中的不同小写字母表示组间差异显著(Kruskal-Wallis, P < 0.05)。r表示样点间的相似程度。r数值越大, 差异越大。样点缩写全称见图1。

Fig. 3 The diversity and class level community structure of epiphytic fungi in the phyllosphere of Pinus tabuliformis and Euonymus japonicus among different sampling plots. A, The alpha diversity index of P. tabuliformis; B, The alpha diversity index of E. japonicus; C, Non-metric multidimensional scaling analysis of P. tabuliformis; D, Non-metric multidimensional scaling analysis of E. japonicus; E, The community structure of P. tabuliformis; F, The community structure of E. japonicus. Different letters in the box plot indicates that there was significant difference between groups (Kruskal-Wallis, P < 0.05). r denotes the degree of similarity between sample points. The larger the value of, the greater the difference. Full names of sample plot abbreviations see Fig. 1.

表2 油松与大叶黄杨不同样点间的叶际表生真菌相似性分析(ANOSIM)结果

Table 2 The analysis of similarities of epiphytic fungi in the phyllosphere of Pinus tabuliformis and Euonymus japonicus among different sampling plots

树种 Tree species	样点间对比 Comparison between sample plots	r	P
油松 Pinus tabuliformis	安定门/和平街 ADM/HPJ	0.4016	0.001
	安定门/亚运村 ADM/YYC	0.2931	0.001
	安定门/北七家 ADM/BQJ	0.4734	0.001
	和平街/亚运村 HPJ/YYC	0.0273	0.133
	和平街/北七家 HPJ/BQJ	0.2422	0.001
	亚运村/北七家 YYC/BQJ	0.2056	0.001
大叶黄杨Euonymus japonicus	亚运村/北七家 YYC/BQJ	0.1251	0.006
	亚运村/安定门 YYC/ADM	0.2292	0.001
	亚运村/和平街 YYC/HPJ	0.0683	0.044
	北七家/安定门 BQJ/ADM	0.2782	0.001
	北七家/和平街 BQJ/HPJ	0.1253	0.006
	安定门/和平街 ADM/HPJ	0.3554	0.001

表3 油松与大叶黄杨不同季节间的叶际表生真菌α多样性

Table 3 The alpha diversity index of epiphytic fungi in the phyllosphere of Pinus tabuliformis and Euonymus japonicus among different seasons

树种 Tree Species	季节 Seasons	Shannon多样性指数Shannon diversity index	Chao1丰富度指数 Chao1 richness index	Pielou均匀度指数Pielou evenness index
油松 Pinus tabuliformis	七月 July	3.96 ± 0.34^a	206.10 ± 31.82^a	0.52 ± 0.037^a
	十一月 Nov.	3.70 ± 1.13^a	149.69 ± 102.57^c	0.53 ± 0.14^a
	一月 Jan.	3.93 ± 0.63^a	174.34 ± 73.91^abc	0.54 ± 0.06^a
	四月 Apr.	3.79 ± 0.35^a	171.99 ± 33.95^b	0.51 ± 0.04^a
大叶黄杨Euonymus japonicus	七月 July	2.78 ± 0.26^bc	118.78 ± 34.40^b	0.41 ± 0.04^b
	十一月 Nov.	3.47 ± 0.60^a	185.69 ± 76.38^a	0.47 ± 0.06^a
	一月 Jan.	2.74 ± 0.58^c	179.19 ± 71.27^a	0.37 ± 0.05^c
	四月 Apr.	3.00 ± 1.11^ab	174.52 ± 61.58^a	0.40 ± 0.14^ab

图4 油松与大叶黄杨的叶际表生真菌在不同季节间的α多样性与纲水平群落组成。A: 油松的α多样性指数; B: 大叶黄杨的α多样性指数; C: 油松的NMDS分析; D: 大叶黄杨的NMDS分析; E: 油松的群落结构; F: 大叶黄杨的群落结构。箱线图中的不同小写字母表示组间差异显著(Kruskal-Wallis, P < 0.05)。r表示样点间的相似程度。r数值越大, 差异越大。

Fig. 4 The diversity and class level community structure of epiphytic fungi in the phyllosphere of Pinus tabuliformis and Euonymus japonicus across different seasons. A, The alpha diversity index of P. tabuliformis; B, The alpha diversity index of E. japonicus; C, Non-metric multidimensional scaling analysis of P. tabuliformis; D, Non-metric multidimensional scaling analysis of E. japonicus; E, The community structure of P. tabuliformis; F, The community structure of E. japonicus. Different letters in the box plot indicates that there was significant difference between groups (Kruskal-Wallis, P < 0.05). The larger the value of, the greater the difference.

表4 油松与大叶黄杨不同季节间的叶际表生真菌ANOSIM的分析结果

Table 4 The alpha diversity index of epiphytic fungi in the phyllosphere of Pinus tabuliformis and Euonymus japonicus among different seasons

	季节间对比 Comparison between seasons	r	P
油松 Pinus tabuliformis	七月/十一月 July/Nov.	0.1533	0.001
	七月/一月 July/Jan.	0.1938	0.001
	七月/四月 July/Apr.	0.2540	0.001
	十一月/一月 Nov./Jan.	0.0235	0.185
	十一月/四月 Nov./Apr.	0.1882	0.002
	一月/四月 Jan./Apr.	0.2520	0.001
大叶黄杨 Euonymus japonicus	十一月/七月 Nov./July	0.1918	0.001
	十一月/一月 Nov./Jan.	0.2062	0.002
	十一月/四月 Nov./Apr.	0.8448	0.001
	七月/一月 July/Jan.	0.1439	0.009
	七月/四月 July/Apr.	0.8940	0.001
	一月/四月 Jan./Apr.	0.9305	0.001

图5 油松与大叶黄杨的叶际表生真菌的多样性与群落组成。A: 油松与大叶黄杨相对丰度前30的属间热图(数据经过lg处理); B: 油松与大叶黄杨的群落组成桑基图; C: 油松与大叶黄杨的NMDS分析图; D: 油松与大叶黄杨的线性判别分析; E: 油松与大叶黄杨的α多样性箱线图。热图中的“*”与箱线图中的不同小写字母表示组间差异显著(Kruskal-Wallis, P < 0.05)。

Fig. 5 The diversity and community structure of epiphytic fungi in the phyllosphere of Pinus tabuliformis and Euonymus japonicus at different seasons; A, Heat map of top 30 genera in relative abundance ranking of fungi (data processed by log10); B, Sankey diagram of two trees; C, Non-metric multidimensional scaling analysis of two trees; D, Linear discriminant analysis effect size (LEfSe) of two trees; E, The alpha diversity index of two trees. YS, P. tabuliformis, HY, E. japonicus. The “*” in heat map and different letters in the box plot indicates that there was significant difference between groups (Kruskal-Wallis, P < 0.05).

图6 大叶黄杨(A)和油松(B)的群落组成与温度、PM2.5和降水的方差分解分析(VPA)。值小于0的未予展示。

Fig. 6 Variance partitioning analysis of community composition and temperature, PM2.5, and precipitation of Euonymus japonicas (A) and Pinus tabuliformis (B). Values < 0 was not shown.

图7 油松(A)和大叶黄杨(B)叶际表生真菌Chao1丰富度指数与温度、PM2.5、降水的线性回归分析

Fig. 7 Linear regression analysis of Chao1 richness index of epiphytic fungi in the phyllosphere with temperature, PM2.5 and precipitation in Pinus tabuliformis (A) and Euonymus japonicus (B)

图8 油松(A)与大叶黄杨(B)叶际表生真菌相对丰富度前40位的属间网络关系。线的粗细代表相关性关系的强弱, 圆的大小代表度的大小。

Fig. 8 Network of the top 40 epiphytic fungal genera in relative abundance in the phyllosphere of Pinus tabuliformis (A) and Euonymus japonicus (B). The thickness of the line represents the strength of the correlation relationship and the size of the circle represents the size of the degree.

表5 油松与大叶黄杨的叶际表生真菌功能分类

Table 5 Functional classification of epiphytic fungi in phyllosphere of Pinus tabuliformis and Euonymus japonicus

营养类型 Trophic mode	功能群 Guild	油松功能群比例 Proportion of guild in Pinus tabuliformis (%)	营养类型占比 Proportion of trophic mode (%)	大叶黄杨功能群比例 Proportion of guild in Euonymus japonicus (%)	营养类型占比Proportion of trophic mode (%)
腐生营养型 Saprotroph	未定义腐生真菌 Undefined saprotroph fungi	46.824	63.619	21.269	22.215
	粪腐生真菌 Dung saprotroph fungi	0.106		0.061
	木腐生真菌 Wood saprotroph fungi	16.668		0.630
	土壤腐生真菌 Soil saprotroph fungi	0.018		0.240
	叶片腐生真菌 Leaf saprotroph fungi	0.001		0.015
	凋落物腐生真菌 Litter saprotroph fungi	0.003		0.001
共生营养型 Symbiotroph	内生真菌 Endophyte fungi	0.595	0.651	0.266	0.315
	外生菌根真菌 Ectomycorrhizal fungi	0.005		0
	杜鹃类菌根真菌 Ericoid mycorrhizal fungi	0.002		0.001
	植物附生真菌 Epiphyte fungi	0.049		0.048
病理营养型 Pathotroph	植物病原真菌 Plant pathogen fungi	9.171	9.246	70.806	70.906
	动物病原真菌 Animal pathogen fungi	0.023		0.025
	真菌寄生真菌 Fungal parasite fungi	0.037		0.070
	苔藓植物寄生真菌 Bryophyte parasite fungi	0.002		0.001
	地衣寄生菌 Lichen parasite fungi	0.013		0.004
	其他 Other	26.484		6.564

图9 油松与大叶黄杨叶际表生真菌营养类型的相对丰度。A: 油松的不同采样地点之间; B: 油松的不同采样季节之间; C: 大叶黄杨的不同采样地点之间; D: 大叶黄杨的不同采样季节之间。样点缩写全称见图1。

Fig. 9 Trophic mode of epiphytic fungi in the phyllosphere of Pinus tabuliformis and Euonymus japonicus. A, P. tabuliformis in different sampling plots; B, P. tabuliformis in different seasons; C, E. japonicus in different sampling plots; D, E. japonicus in different seasons. Full names of sample plot abbreviations see Fig. 1.

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北京地区油松与大叶黄杨叶际表生真菌多样性及群落组成

Diversity and community composition of epiphytic fungi in the phyllosphere of Pinus tabuliformis and Euonymus japonicus in Beijing, northern China

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