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Haustorium formation and a distinct biotrophic transcriptome characterize infection of Nicotiana benthamiana by the tree pathogen Phytophthora kernoviae

Wang, Shumei and Vetukuri, Ramesh and Kushwaha, Sandeep Kumar and Hedley, Pete E. and Morris, Jenny and Studholme, David J. and Welsh, Lydia R. J. and Boevink, Petra C. and Birch, Paul R. J. and Whisson, Stephen C. (2021). Haustorium formation and a distinct biotrophic transcriptome characterize infection of Nicotiana benthamiana by the tree pathogen Phytophthora kernoviae. Molecular Plant Pathology. 22 , 954-968
[Research article]

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Abstract

Phytophthora species cause some of the most serious diseases of trees and threaten forests in many parts of the world. Despite the generation of genome sequence assemblies for over 10 tree-pathogenic Phytophthora species and improved detection methods, there are many gaps in our knowledge of how these pathogens interact with their hosts. To facilitate cell biology studies of the infection cycle we examined whether the tree pathogen Phytophthora kernoviae could infect the model plant Nicotiana benthamiana. We transformed P. kernoviae to express green fluorescent protein (GFP) and demonstrated that it forms haustoria within infected N. benthamiana cells. Haustoria were also formed in infected cells of natural hosts, Rhododendron ponticum and European beech (Fagus sylvatica). We analysed the transcriptome of P. kernoviae in cultured mycelia, spores, and during infection of N. benthamiana, and detected 12,559 transcripts. Of these, 1,052 were predicted to encode secreted proteins, some of which may function as effectors to facilitate disease development. From these, we identified 87 expressed candidate RXLR (Arg-any amino acid-Leu-Arg) effectors. We transiently expressed 12 of these as GFP fusions in N. benthamiana leaves and demonstrated that nine significantly enhanced P. kernoviae disease progression and diversely localized to the cytoplasm, nucleus, nucleolus, and plasma membrane. Our results show that N. benthamiana can be used as a model host plant for studying this tree pathogen, and that the interaction likely involves suppression of host immune responses by RXLR effectors. These results establish a platform to expand the understanding of Phytophthora tree diseases.

Authors/Creators:Wang, Shumei and Vetukuri, Ramesh and Kushwaha, Sandeep Kumar and Hedley, Pete E. and Morris, Jenny and Studholme, David J. and Welsh, Lydia R. J. and Boevink, Petra C. and Birch, Paul R. J. and Whisson, Stephen C.
Title:Haustorium formation and a distinct biotrophic transcriptome characterize infection of Nicotiana benthamiana by the tree pathogen Phytophthora kernoviae
Series Name/Journal:Molecular Plant Pathology
Year of publishing :2021
Volume:22
Page range:954-968
Number of Pages:15
Publisher:WILEY
ISSN:1464-6722
Language:English
Publication Type:Research article
Article category:Scientific peer reviewed
Version:Published version
Copyright:Creative Commons: Attribution 4.0
Full Text Status:Public
Subjects:(A) Swedish standard research categories 2011 > 4 Agricultural Sciences > 401 Agricultural, Forestry and Fisheries > Agricultural Science
Keywords:biotrophy, effector, pathogenicity, RNA‐Seq, RXLR, tree disease
URN:NBN:urn:nbn:se:slu:epsilon-p-112006
Permanent URL:
http://urn.kb.se/resolve?urn=urn:nbn:se:slu:epsilon-p-112006
Additional ID:
Type of IDID
DOI10.1111/mpp.13072
Web of Science (WoS)000652360100001
ID Code:25012
Faculty:LTV - Fakulteten för landskapsarkitektur, trädgårds- och växtproduktionsvetenskap
Department:(LTJ, LTV) > Department of Plant Breeding (from 130101)
Deposited By: SLUpub Connector
Deposited On:24 Aug 2021 14:24
Metadata Last Modified:24 Aug 2021 14:31

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