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Title: Phytophthora palmivora establishes tissue-specific intracellular infection structures in the earliest divergent land plant lineage

Abstract

The expansion of plants onto land was a formative event that brought forth profound changes to the earth’s geochemistry and biota. Filamentous eukaryotic microbes developed the ability to colonize plant tissues early during the evolution of land plants, as demonstrated by intimate, symbiosis-like associations in >400 million-year-old fossils. However, the degree to which filamentous microbes establish pathogenic interactions with early divergent land plants is unclear. Here, we demonstrate that the broad host-range oomycete pathogen Phytophthora palmivora colonizes liverworts, the earliest divergent land plant lineage. We show that P. palmivora establishes a complex tissue-specific interaction with Marchantia polymorpha, where it completes a full infection cycle within air chambers of the dorsal photosynthetic layer. Remarkably, P. palmivora invaginates M. polymorpha cells with haustoria-like structures that accumulate host cellular trafficking machinery and the membrane syntaxin MpSYP13B, but not the related MpSYP13A. Furthermore, our results indicate that the intracellular accommodation of filamentous microbes is an ancient plant trait that is successfully exploited by pathogens like P. palmivora.

Authors:
 [1];  [1];  [1];  [1]; ORCiD logo [1]
  1. Univ. of Cambridge, Cambridge (United Kingdom)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, Oakland, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1543906
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 115; Journal Issue: 16; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Science & Technology; Other Topics; bryophyte; liverworts; oomycetes; Phytophthora; haustoria

Citation Formats

Carella, Philip, Gogleva, Anna, Tomaselli, Marta, Alfs, Carolin, and Schornack, Sebastian. Phytophthora palmivora establishes tissue-specific intracellular infection structures in the earliest divergent land plant lineage. United States: N. p., 2018. Web. doi:10.1073/pnas.1717900115.
Carella, Philip, Gogleva, Anna, Tomaselli, Marta, Alfs, Carolin, & Schornack, Sebastian. Phytophthora palmivora establishes tissue-specific intracellular infection structures in the earliest divergent land plant lineage. United States. doi:10.1073/pnas.1717900115.
Carella, Philip, Gogleva, Anna, Tomaselli, Marta, Alfs, Carolin, and Schornack, Sebastian. Tue . "Phytophthora palmivora establishes tissue-specific intracellular infection structures in the earliest divergent land plant lineage". United States. doi:10.1073/pnas.1717900115. https://www.osti.gov/servlets/purl/1543906.
@article{osti_1543906,
title = {Phytophthora palmivora establishes tissue-specific intracellular infection structures in the earliest divergent land plant lineage},
author = {Carella, Philip and Gogleva, Anna and Tomaselli, Marta and Alfs, Carolin and Schornack, Sebastian},
abstractNote = {The expansion of plants onto land was a formative event that brought forth profound changes to the earth’s geochemistry and biota. Filamentous eukaryotic microbes developed the ability to colonize plant tissues early during the evolution of land plants, as demonstrated by intimate, symbiosis-like associations in >400 million-year-old fossils. However, the degree to which filamentous microbes establish pathogenic interactions with early divergent land plants is unclear. Here, we demonstrate that the broad host-range oomycete pathogen Phytophthora palmivora colonizes liverworts, the earliest divergent land plant lineage. We show that P. palmivora establishes a complex tissue-specific interaction with Marchantia polymorpha, where it completes a full infection cycle within air chambers of the dorsal photosynthetic layer. Remarkably, P. palmivora invaginates M. polymorpha cells with haustoria-like structures that accumulate host cellular trafficking machinery and the membrane syntaxin MpSYP13B, but not the related MpSYP13A. Furthermore, our results indicate that the intracellular accommodation of filamentous microbes is an ancient plant trait that is successfully exploited by pathogens like P. palmivora.},
doi = {10.1073/pnas.1717900115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 16,
volume = 115,
place = {United States},
year = {2018},
month = {4}
}

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