Conserved secreted effectors contribute to endophytic growth and multihost plant compatibility in a vascular wilt fungus

Redkar, Amey, Sabale, Mugdha, Schudoma, Christian, Zechmann, Bernd, Gupta, Yogesh K., López-Berges, Manuel S., Venturini, Giovanni, Gimenez-Ibanez, Selena, Turrà, David, Solano, Roberto and Di Pietro, Antonio (2022) Conserved secreted effectors contribute to endophytic growth and multihost plant compatibility in a vascular wilt fungus. Plant Cell, 34 (9). pp. 3214-3232. ISSN 1040-4651

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Abstract

Fungal interactions with plant roots, either beneficial or detrimental, have a crucial impact on agriculture and ecosystems. The cosmopolitan plant pathogen Fusarium oxysporum (Fo) provokes vascular wilts in more than a hundred different crops. Isolates of this fungus exhibit host-specific pathogenicity, which is conferred by lineage-specific Secreted In Xylem (SIX) effectors encoded on accessory genomic regions. However, such isolates also can colonize the roots of other plants asymptomatically as endophytes or even protect them against pathogenic strains. The molecular determinants of endophytic multihost compatibility are largely unknown. Here, we characterized a set of Fo candidate effectors from tomato (Solanum lycopersicum) root apoplastic fluid; these early root colonization (ERC) effectors are secreted during early biotrophic growth on main and alternative plant hosts. In contrast to SIX effectors, ERCs have homologs across the entire Fo species complex as well as in other plant-interacting fungi, suggesting a conserved role in fungus–plant associations. Targeted deletion of ERC genes in a pathogenic Fo isolate resulted in reduced virulence and rapid activation of plant immune responses, while ERC deletion in a nonpathogenic isolate led to impaired root colonization and biocontrol ability. Strikingly, some ERCs contribute to Fo infection on the nonvascular land plant Marchantia polymorpha, revealing an evolutionarily conserved mechanism for multihost colonization by root infecting fungi.

Item Type: Article
Additional Information: Funding Information: We thank M.I.G. Roncero (Universidad de Córdoba, Spain) for critical reading of the manuscript. We acknowledge the Central Service for Research Support (SCAI) of the University of Córdoba for use of the confocal microscopy facility. The high-performance computing resources and services in this work were supported by the Earlham Institute Scientific Computing group alongside the Norwich BioScience Institutes Partnership Computing infrastructure for Science (CiS) group. This work was supported by grants from the Spanish Ministry of Science and Innovation (MICINN, grant PID2019-108045RB-I00) and Junta de Andalucía (P20_00179) to A.D.P. A.R. and M.S. were supported by the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreements No. 750669 and 797256. A.R. also acknowledges funding from Juan de la Cierva Incorporación grant from the Spanish Research Agency (IJC2018-038468-I) as well as financial support from Ramalingaswami Re-entry Fellowship (BT/RLF/Re-entry/72/ 2020), Department of Biotechnology, Government of India. C.S. was supported by BBSRC strategic funding, Core Capability Grant BB/CCG1720/1, BBS/E/T/000PR9816. S.G.I is funded by the Spanish Ministry for Science and Innovation RTI2018-094526-J-I00 and the CSIC 2021AT006 grants. Research in the R.S. lab was funded by the Spanish Ministry for Science and Innovation grant PID2019-107012RB-100 (MICINN/FEDER). Publisher Copyright: © American Society of Plant Biologists 2022. All rights reserved.
Uncontrolled Keywords: plant science ,/dk/atira/pure/subjectarea/asjc/1100/1110
Faculty \ School: Faculty of Science > The Sainsbury Laboratory
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Depositing User: LivePure Connector
Date Deposited: 18 Jan 2025 01:08
Last Modified: 18 Jan 2025 01:08
URI: https://ueaeprints.uea.ac.uk/id/eprint/98252
DOI: 10.1093/plcell/koac174

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