IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-023-44234-7.html
   My bibliography  Save this article

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

Author

Listed:
  • Gaofei Jiang

    (Southwest University
    Nanjing Agricultural 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
    The Pennsylvania State University)

  • Yong Zhang

    (Southwest University
    Shaanxi University of Science & Technology)

  • Zhong Wei

    (Nanjing Agricultural University)

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.

Suggested Citation

  • 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 Oh, 2024. "Effects of plant tissue permeability on invasion and population bottlenecks of a phytopathogen," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44234-7
    DOI: 10.1038/s41467-023-44234-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-44234-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-44234-7?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Sasha F. Levy & Jamie R. Blundell & Sandeep Venkataram & Dmitri A. Petrov & Daniel S. Fisher & Gavin Sherlock, 2015. "Quantitative evolutionary dynamics using high-resolution lineage tracking," Nature, Nature, vol. 519(7542), pages 181-186, March.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Li Xie & Wenying Shou, 2021. "Steering ecological-evolutionary dynamics to improve artificial selection of microbial communities," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    2. Daniel P. G. H. Wong & Benjamin H. Good, 2024. "Quantifying the adaptive landscape of commensal gut bacteria using high-resolution lineage tracking," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    3. Sébastien Boyer & Lucas Hérissant & Gavin Sherlock, 2021. "Adaptation is influenced by the complexity of environmental change during evolution in a dynamic environment," PLOS Genetics, Public Library of Science, vol. 17(1), pages 1-27, January.
    4. Marie Rescan & Daphné Grulois & Enrique Ortega Aboud & Pierre de Villemereuil & Luis-Miguel Chevin, 2021. "Predicting population genetic change in an autocorrelated random environment: Insights from a large automated experiment," PLOS Genetics, Public Library of Science, vol. 17(6), pages 1-23, June.
    5. Miller, Craig R. & Van Leuven, James T. & Wichman, Holly A. & Joyce, Paul, 2018. "Selecting among three basic fitness landscape models: Additive, multiplicative and stickbreaking," Theoretical Population Biology, Elsevier, vol. 122(C), pages 97-109.
    6. Joao A. Ascensao & Kelly M. Wetmore & Benjamin H. Good & Adam P. Arkin & Oskar Hallatschek, 2023. "Quantifying the local adaptive landscape of a nascent bacterial community," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    7. Takeshi Matsui & Martin N. Mullis & Kevin R. Roy & Joseph J. Hale & Rachel Schell & Sasha F. Levy & Ian M. Ehrenreich, 2022. "The interplay of additivity, dominance, and epistasis on fitness in a diploid yeast cross," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44234-7. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.