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

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America

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.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, Oakland, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1543906
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, Issue 16; ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)Copyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 42 works
Citation information provided by
Web of Science

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A Renaissance of Elicitors: Perception of Microbe-Associated Molecular Patterns and Danger Signals by Pattern-Recognition Receptors journal June 2009
From algae to angiosperms–inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes journal January 2014
Interactions of beneficial and detrimental root-colonizing filamentous microbes with plant hosts journal June 2013
Phytophthora capsici-tomato interaction features dramatic shifts in gene expression associated with a hemi-biotrophic lifestyle journal June 2013
Time-resolved dual transcriptomics reveal early induced Nicotiana benthamiana root genes and conserved infection-promoting Phytophthora palmivora effectors journal May 2017
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
How Do Filamentous Pathogens Deliver Effector Proteins into Plant Cells? journal February 2014
Development of Gateway Binary Vector Series with Four Different Selection Markers for the Liverwort Marchantia polymorpha journal September 2015
The Plasmodesmal Protein PDLP1 Localises to Haustoria-Associated Membranes during Downy Mildew Infection and Regulates Callose Deposition journal November 2014
Hydathode pit development in the alpine plant Saxifraga cochlearis journalarticle January 2017
Plant carbon nourishment of arbuscular mycorrhizal fungi. text January 2017
SecretSanta: flexible pipelines for functional secretome prediction. text January 2018
Plant vacuole morphology and vacuolar trafficking journal September 2014
Adaptation Mechanisms in the Evolution of Moss Defenses to Microbes journal March 2017
featureCounts: An efficient general-purpose program for assigning sequence reads to genomic features text January 2013
FIGURE 3. Rhizoidal ascomycete associations. A-C. Scanning electron micrographs. D. Light micrograph. E-G. Transmission electron micrographs. A in Fungal symbioses in bryophytes: New insights in the Twenty First Century image January 2010

Cited By (9)

An evolutionary framework for host shifts – jumping ships for survival journal June 2019
The coming of age of EvoMPMI: evolutionary molecular plant–microbe interactions across multiple timescales journal August 2018
An Evolutionarily Conserved Receptor-like Kinases Signaling Module Controls Cell Wall Integrity During Tip Growth journal December 2019
Developmental Modulation of Root Cell Wall Architecture Confers Resistance to an Oomycete Pathogen journal November 2020
On plant defense signaling networks and early land plant evolution journal May 2018
The plant–pathogen haustorial interface at a glance journal March 2020
Manipulation of Bryophyte Hosts by Pathogenic and Symbiotic Microbes. text January 2018
A secreted protein of 15 kDa plays an important role in Phytophthora palmivora development and pathogenicity. text January 2020
Plant SYP12 syntaxins mediate an evolutionarily conserved general immunity to filamentous pathogens journal February 2022