Effects of plant tissue permeability on invasion and population bottlenecks of a phytopathogen

Gaofei Jiang, Yuling Zhang, Min Chen, Josep Ramoneda, Liangliang Han, Yu Shi, Rémi Peyraud, Yikui Wang, Xiaojun Shi, Xinping Chen, Wei Ding, Alexandre Jousset, Yasufumi Hikichi, Kouhei Ohnishi, Fang-Jie Zhao, Yangchun Xu, Qirong Shen, Francisco Dini-Andreote, Yong Zhang () and Zhong Wei ()
Additional contact information
Gaofei Jiang: Southwest University
Yuling Zhang: Nanjing Agricultural University
Min Chen: Shaanxi University of Science & Technology
Josep Ramoneda: University of Colorado
Liangliang Han: City University of Hong Kong, Kowloon Tong
Yu Shi: School of Life Sciences, Henan University
Rémi Peyraud: iMEAN, Ramonville Saint Agne
Yikui Wang: Guangxi Academy of Agricultural Science
Xiaojun Shi: Southwest University
Xinping Chen: Southwest University
Wei Ding: Southwest University
Alexandre Jousset: Nanjing Agricultural University
Yasufumi Hikichi: Kochi University
Kouhei Ohnishi: Kochi University
Fang-Jie Zhao: Nanjing Agricultural University
Yangchun Xu: Nanjing Agricultural University
Qirong Shen: Nanjing Agricultural University
Francisco Dini-Andreote: The Pennsylvania State University
Yong Zhang: Southwest University
Zhong Wei: Nanjing Agricultural University

Nature Communications, 2024, vol. 15, issue 1, 1-10

Abstract: Abstract Pathogen genetic diversity varies in response to environmental changes. However, it remains unclear whether plant barriers to invasion could be considered a genetic bottleneck for phytopathogen populations. Here, we implement a barcoding approach to generate a pool of 90 isogenic and individually barcoded Ralstonia solanacearum strains. We used 90 of these strains to inoculate tomato plants with different degrees of physical permeability to invasion (intact roots, wounded roots and xylem inoculation) and quantify the phytopathogen population dynamics during invasion. Our results reveal that the permeability of plant roots impacts the degree of population bottleneck, genetic diversity, and composition of Ralstonia populations. We also find that selection is the main driver structuring pathogen populations when barriers to infection are less permeable, i.e., intact roots, the removal of root physical and immune barriers results in the predominance of stochasticity in population assembly. Taken together, our study suggests that plant root permeability constitutes a bottleneck for phytopathogen invasion and genetic diversity.

Date: 2024
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DOI: 10.1038/s41467-023-44234-7

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