Increased dependence on mycorrhizal fungi for nutrient acquisition under carbon limitation by tree girdling

doi:10.1016/j.pld.2025.02.004

Plant Diversity ›› 2025, Vol. 47 ›› Issue (03): 466-478.DOI: 10.1016/j.pld.2025.02.004

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Increased dependence on mycorrhizal fungi for nutrient acquisition under carbon limitation by tree girdling

Jing Chen^a, Jingjing Cao^a, Binglin Guo^a, Meixu Han^a, Zhipei Feng^a, Jinqi Tang^b, Xiaohan Mo^c,d,e, Junjian Wang^d,e, Qingpei Yang^a, Yuxin Pei^a, Yakov Kuzyakov^f,g, Junxiang Ding^h, Naoki Makitaⁱ, Xitian Yang^a, Haiyang Zhang^j,k, Yong Zhao^a, Deliang Kong^a

a. College of Forestry, Henan Agricultural University, Zhengzhou 450002, China;
b. College of Horticulture, China Agricultural University, Beijing 100193, China;
c. School of Urban Planning and Design, Peking University Shenzhen Graduate School, Peking University, Shenzhen 518055, China;
d. State Environmental Protection Key Laboratory of Integrated Surface Water-Groundwater Pollution Control, School of Environmental Science and Engineering, Southern University of Science and Technology, Shenzhen 518055, China;
e. Guangdong Provincial Key Laboratory of Soil and Groundwater Pollution Control, School of Environmental Science and Engineering, Southern University of Science and Technology, Shenzhen 518055, China;
f. Department of Soil Science of Temperate Ecosystem, University of Göttingen, Göttingen 37077, Germany;
g. Peoples Friendship University of Russia (RUDN University), Moscow 117198, Russia;
h. College of Ecology and Environment, Zhengzhou University, Zhengzhou 450001, China;
i. Faculty of Science, Shinshu University, 3-1-1 Asahi, Matsumoto, Nagano 390-8621, Japan;
j. Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales 2751, Australia;
k. College of Life Science, Hebei University, Baoding 071002, China

Received:2024-11-06 Revised:2025-02-17 Online:2025-05-21 Published:2025-05-25
Contact: Deliang Kong,E-mail:deliangkong1999@126.com,deliangkong@henau.edu.cn
Supported by:
This study was funded by the National Natural Science Foundation of China (32471824, 32171746, 42077450, 31870522, 31670550, 42122054), the leading talents of basic research in Henan Province, the Scientific Research Foundation of Henan Agricultural University (30500854), Excellent Youth Creative Research Group Project in Henan Province (252300421002), Foreign Scientists Studio in Henan province (GZS2025011), the Funding for Characteristic and Backbone Forestry Discipline Group of Henan Province, Guangdong Provincial Key Laboratory of Soil and Groundwater Pollution Control (2023B1212060002), Guangdong Basic and Applied Basic Research Foundation (2021B1515020082), the RUDN University Strategic Academic Leadership Program, Funding for Characteristic and backbone forestry discipline group of Henan Province and Research Funds for overseas returnee in Henan Province, China.

Increased dependence on mycorrhizal fungi for nutrient acquisition under carbon limitation by tree girdling

a. College of Forestry, Henan Agricultural University, Zhengzhou 450002, China;
b. College of Horticulture, China Agricultural University, Beijing 100193, China;
c. School of Urban Planning and Design, Peking University Shenzhen Graduate School, Peking University, Shenzhen 518055, China;
d. State Environmental Protection Key Laboratory of Integrated Surface Water-Groundwater Pollution Control, School of Environmental Science and Engineering, Southern University of Science and Technology, Shenzhen 518055, China;
e. Guangdong Provincial Key Laboratory of Soil and Groundwater Pollution Control, School of Environmental Science and Engineering, Southern University of Science and Technology, Shenzhen 518055, China;
f. Department of Soil Science of Temperate Ecosystem, University of Göttingen, Göttingen 37077, Germany;
g. Peoples Friendship University of Russia (RUDN University), Moscow 117198, Russia;
h. College of Ecology and Environment, Zhengzhou University, Zhengzhou 450001, China;
i. Faculty of Science, Shinshu University, 3-1-1 Asahi, Matsumoto, Nagano 390-8621, Japan;
j. Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales 2751, Australia;
k. College of Life Science, Hebei University, Baoding 071002, China

通讯作者: Deliang Kong,E-mail:deliangkong1999@126.com,deliangkong@henau.edu.cn
基金资助:
This study was funded by the National Natural Science Foundation of China (32471824, 32171746, 42077450, 31870522, 31670550, 42122054), the leading talents of basic research in Henan Province, the Scientific Research Foundation of Henan Agricultural University (30500854), Excellent Youth Creative Research Group Project in Henan Province (252300421002), Foreign Scientists Studio in Henan province (GZS2025011), the Funding for Characteristic and Backbone Forestry Discipline Group of Henan Province, Guangdong Provincial Key Laboratory of Soil and Groundwater Pollution Control (2023B1212060002), Guangdong Basic and Applied Basic Research Foundation (2021B1515020082), the RUDN University Strategic Academic Leadership Program, Funding for Characteristic and backbone forestry discipline group of Henan Province and Research Funds for overseas returnee in Henan Province, China.

Abstract

Abstract: Nutrient acquisition through symbiotic ectomycorrhizal fungi is carbon (C) costly but fundamental for plant growth, community, and ecosystem functioning. Here, we examined the functions of roots and mycorrhiza with respect to nutrient uptake after artificially inducing C limitation-seven months after girdling of an ectomycorrhizal tree, Pinus taeda. Root physiological activity (measured as root nitrogen content and root exudation) declined after girdling and was accompanied with 110% and 340% increases in mycorrhizal colonization and extramatrical hyphal length, respectively. Fungi colonizing roots switched to a community characterized by higher C efficiency (lower C cost) of nutrient acquisition (CENA, the amount of nutrient acquisition per unit C cost) and lower network complexity, indicating a tradeoff between CENA and stability of the fungal community. Root transcriptome analysis suggested a shift in metabolic pathways from a tricarboxylic acid cycle decomposition of carbohydrate to lipid biosynthesis to maintain closer associations with mycorrhiza for nutrient cycling after the girdling. By integrating multi-level evidence, including root transcriptome, fungal composition, and network complexity data, we demonstrate an increased dependence on mycorrhiza for nutrient acquisition under the C limitation condition, which is likely due to a shift to fungal community with higher CENA at the cost of lower stability.

Key words: Carbon limitation, Fungal network complexity, Girdling effects, Mycorrhizal and root strategies, Plant-microbiome interaction, Root transcriptome

摘要： Nutrient acquisition through symbiotic ectomycorrhizal fungi is carbon (C) costly but fundamental for plant growth, community, and ecosystem functioning. Here, we examined the functions of roots and mycorrhiza with respect to nutrient uptake after artificially inducing C limitation-seven months after girdling of an ectomycorrhizal tree, Pinus taeda. Root physiological activity (measured as root nitrogen content and root exudation) declined after girdling and was accompanied with 110% and 340% increases in mycorrhizal colonization and extramatrical hyphal length, respectively. Fungi colonizing roots switched to a community characterized by higher C efficiency (lower C cost) of nutrient acquisition (CENA, the amount of nutrient acquisition per unit C cost) and lower network complexity, indicating a tradeoff between CENA and stability of the fungal community. Root transcriptome analysis suggested a shift in metabolic pathways from a tricarboxylic acid cycle decomposition of carbohydrate to lipid biosynthesis to maintain closer associations with mycorrhiza for nutrient cycling after the girdling. By integrating multi-level evidence, including root transcriptome, fungal composition, and network complexity data, we demonstrate an increased dependence on mycorrhiza for nutrient acquisition under the C limitation condition, which is likely due to a shift to fungal community with higher CENA at the cost of lower stability.

关键词: Carbon limitation, Fungal network complexity, Girdling effects, Mycorrhizal and root strategies, Plant-microbiome interaction, Root transcriptome

Jing Chen, Jingjing Cao, Binglin Guo, Meixu Han, Zhipei Feng, Jinqi Tang, Xiaohan Mo, Junjian Wang, Qingpei Yang, Yuxin Pei, Yakov Kuzyakov, Junxiang Ding, Naoki Makita, Xitian Yang, Haiyang Zhang, Yong Zhao, Deliang Kong. Increased dependence on mycorrhizal fungi for nutrient acquisition under carbon limitation by tree girdling[J]. Plant Diversity, 2025, 47(03): 466-478.

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Increased dependence on mycorrhizal fungi for nutrient acquisition under carbon limitation by tree girdling

Increased dependence on mycorrhizal fungi for nutrient acquisition under carbon limitation by tree girdling

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