Diversified alternaria pathogenicity alters plant-soil feedbacks through leaf-root-microbiome dynamics in agroforestry systems

Abstract

Interspecific interactions including plant-plant, plant-microbe, and plant-insect are the important elements to drive the positive plant-soil feedback for maintaining ecosystem stability in biodiversity ecosystems. Yet, the role of diversified foliar pathogens in biodiversity system in influencing the plant-soil feedback (PSF) has often been underestimated. Here, we assessed the effects of foliar Alternaria panax pathogenicity diversity from agroforestry system on PSF and rhizosphere microbial community. We show that a moderate intensity of foliar pathogen infection by A. panax could activate jasmonic acid (JA)-mediated defense from shoots to roots. This activation enhanced the synthesis and secretion of 2-aminoethanesulfonic acid into the rhizosphere for a disease-suppressive rhizo-microbiota assembly, contributing to positive PSF. However, excessive foliar pathogen infection allocated JA-mediated defense only in leaf and disrupted this rhizomicrobial enrichment, resulting negative PSF. This study enhances the understanding of the ecological roles of foliar pathogen within agroforestry systems and provides an insight into agricultural sustainability.

Acknowledgments

This work was supported by the Natural Science Foundation of China (U23A20202 and 32060719 ), the Major Science and Technology Project of Kunming (2021JH002), the Agricultural Joint Program Key Project of Yunnan Province (202101BD070001-003), National Key R&D Program of China (2023YFE0107500), and the Yunnan Xingdian Talent Support Program (to M.Y. and S.Z.).

Author Contributions

Min Yang, Shusheng Zhu-, and Lifen Luo conceived the ideas and designed methodology; Lifen Luo led the writing of the manuscript. Lifen Luo, Zhengping Wang, and Xiubei Yan collected the data; Lifen Luo and Chen Ye analyzed the data; and Jianjun Hao and Xili Liu edited the manuscript and provided critical suggestions. All authors contributed critically to the drafts and gave final approval for publication.

Data availability

All sequences of ITS and 16S rRNA genes of rhizosphere microbiome following different pathogenicity levels or intensity of foliar infection by A. panax can be found in the NCBI database under accession number PRJNA1104181. All sequences of ITS and 16S rRNA genes of rhizosphere microbiome following soil drenching with 2-aminoethanesulfonic acid at concentration of 0 to 100 μg/ml can be found in the NCBI database under accession number PRJNA1106096. All raw reads generated by transcriptome sequencing were deposited in the NCBI database with accession number PRJNA1104498. All data are available in the main text or the supplementary materials.

Conflict of interest statement

The authors declare that they have no competing interests.

Supplementary data

Supplementary data is available at Horticulture Research online.

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