花生根系的一般和特殊代谢物调控丛枝菌根共生体形成

doi:10.1016/j.jia.2023.09.011

Journal of Integrative Agriculture ›› 2024, Vol. 23 ›› Issue (8): 2618-2632.DOI: 10.1016/j.jia.2023.09.011

花生根系的一般和特殊代谢物调控丛枝菌根共生体形成

收稿日期:2023-04-25 接受日期:2023-08-09 出版日期:2024-08-20 发布日期:2024-07-29

General and specialized metabolites in peanut roots regulate arbuscular mycorrhizal symbiosis

Li Cui¹, Jianguo Wang¹, Zhaohui Tang¹, Zheng Zhang¹, Sha Yang¹, Feng Guo¹, Xinguo Li¹, Jingjing Meng¹, Jialei Zhang^2#, Yakov Kuzyakov^{3, 4, 5#}, Shubo Wan^2#

¹ Institute of Crop Germplasm Resources, Shandong Academy of Agricultural Sciences/Scientific Observing and Experimental Station of Crop Cultivation in East China, Ministry of Agriculture and Rural Affairs, Jinan 250100, China
² Shandong Academy of Agricultural Sciences, Jinan 250100, China
³Department of Soil Science of Temperate Ecosystems, Department of Agricultural Soil Science, University of Göttingen, Göttingen 37077, Germany
⁴Peoples Friendship University of Russia (RUDN University), Miklukho-Maklaya St, Moscow 117198, Russia
⁵Institute of Environmental Sciences, Kazan Federal University, 420049 Kazan, Russia

Received:2023-04-25 Accepted:2023-08-09 Online:2024-08-20 Published:2024-07-29
About author:#Correspondence Jialei Zhang, Tel: +86-531-66659047, E-mail: zhangjialei19@163.com; Yakov Kuzyakov, E-mail: kuzyakov@gwdg.de; Shubo Wan, E-mail: wanshubo2016@163.com
Supported by:
This work was supported by the National Key R&D Program of China (2022YFD1000105), the Key R&D Program of Shandong Province, China (2021CXGC010804), the Taishan Scholars Project, China (202211275), the Youth Found of Shandong Natural Science Foundation, China (ZR2021QC163), the Natural Science Foundation of Shandong Province, China (ZR2020MC094), the Strategic Academic Leadership Program “Priority 2030” of the Kazan Federal University, Russia, the RUDN University Strategic Academic Leadership Program, China, and the 2022 High-level Talent Innovation and Entrepreneurship (Platform) Project of Linyi, China.

摘要/Abstract

摘要：

丛枝菌根(Arbuscular mycorrhizae, AM)真菌与植物根系形成的共生关系能够为植物提供营养、促进植物生长和抵御各种逆境胁迫。AM真菌定殖过程中根部的代谢变化是研究这种共生关系形成和维持的关键。因此，我们分析花生(Arachis hypogaea L.)植株在AM共生定殖和发展过程中的代谢变化，并与未定殖的根系进行了比较。研究结果表明在AM定殖初期主要是苯丙素和黄酮类化合物含量和种类的变化，这些化合物在调节根系与AM真菌的识别、相互作用和预定殖的信号通路中起重要作用。与初始定殖阶段相比，当共生关系完全建立时类黄酮化合物种类减少了25%。AM共生体建立后，一般代谢物发生很大的变化，主要表现为脂质、氨基酸、羧酸和碳水化合物的形成。从AM真菌侵染根系到共生体完全形成，脂质类化合物增加了8.5%，其中溶磷脂酰胆碱作为一种信号化合物，仅存在于AM共生体完全建立的根系中，与为未定殖根系相比其含量显著减少。在AM建立初期，水杨酸含量增加2倍，而茉莉酸和脱落酸含量则显著降低，当共生关系建立后，根系中茉莉酸含量仍然显著降低。另外，AM根系中钙、镁和D-(+)-甘露糖含量显著增加，从而促进植株的生长。总体而言，有利于AM共生关系建立的特殊代谢物的变化主要发生在AM形成的早期阶段，但是AM完全建立后，一般代谢物则发生强烈变化。综上所述，特殊代谢物作为信号化合物参与了AM共生的形成，当根系与AM真菌的共生关系完全建立后，这些化合物的含量不再发生变化。

Abstract:

Arbuscular mycorrhizae (AM) fungi form symbiotic associations with plant roots, providing nutritional benefits and promoting plant growth and defenses against various stresses. Metabolic changes in the roots during AM fungal colonization are key to understanding the development and maintenance of these symbioses. Here, we investigated metabolic changes in the roots of peanut (Arachis hypogaea L.) plants during the colonization and development of AM symbiosis, and compared them to uncolonized roots. The primary changes during the initial stage of AM colonization were in the contents and compositions of phenylpropanoid and flavonoid compounds. These compounds function in signaling pathways that regulate recognition, interactions, and pre-colonization between roots and AM fungi. Flavonoid compounds decreased by 25% when the symbiosis was fully established compared to the initial colonization stage. After AM symbiosis was established, general metabolism strongly shifted toward the formation of lipids, amino acids, carboxylic acids, and carbohydrates. Lipid compounds increased by 8.5% from the pre-symbiotic stage to well-established symbiosis. Lyso-phosphatidylcholines, which are signaling compounds, were only present in AM roots, and decreased in content after the symbiosis was established. In the initial stage of AM establishment, the content of salicylic acid increased two-fold, whereas jasmonic acid and abscisic acid decreased compared to uncolonized roots. The jasmonic acid content decreased in roots after the symbiosis was well established. AM symbiosis was associated with high levels of calcium, magnesium, and D-(+)-mannose, which stimulated seedling growth. Overall, specific metabolites that favor the establishment of AM symbiosis were common in the roots, primarily during early colonization, whereas general metabolism was strongly altered when AM symbiosis was well-established. In conclusion, specialized metabolites function as signaling compounds to establish AM symbiosis. These compounds are no longer produced after the symbiosis between the roots and AM becomes fully established.

Key words: Arachis hypogaea L. , arbuscular mycorrhizal fungi , metabolites , symbiotic association

Li Cui, Jianguo Wang, Zhaohui Tang, Zheng Zhang, Sha Yang, Feng Guo, Xinguo Li, Jingjing Meng, Jialei Zhang, Yakov Kuzyakov, Shubo Wan. 花生根系的一般和特殊代谢物调控丛枝菌根共生体形成[J]. Journal of Integrative Agriculture, 2024, 23(8): 2618-2632.

Li Cui, Jianguo Wang, Zhaohui Tang, Zheng Zhang, Sha Yang, Feng Guo, Xinguo Li, Jingjing Meng, Jialei Zhang, Yakov Kuzyakov, Shubo Wan. General and specialized metabolites in peanut roots regulate arbuscular mycorrhizal symbiosis[J]. Journal of Integrative Agriculture, 2024, 23(8): 2618-2632.

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花生根系的一般和特殊代谢物调控丛枝菌根共生体形成

General and specialized metabolites in peanut roots regulate arbuscular mycorrhizal symbiosis

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