The secreted FoAPY1 peptidase promotes Fusarium oxysporum invasion

Qian, Hengwei; Song, Limin; Wang, Lulu; Wang, Baoshan; Liang, Wenxing

doi:10.3389/fmicb.2022.1040302

The secreted FoAPY1 peptidase promotes Fusarium oxysporum invasion

Journal Article · Wed Oct 19 00:00:00 EDT 2022 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2022.1040302· OSTI ID:1893792

Qian, Hengwei; Song, Limin; Wang, Lulu; Wang, Baoshan; Liang, Wenxing

The secretion of peptidases from several pathogens has been reported, but the biological function of these proteins in plant-pathogen interactions is poorly understood. Fusarium oxysporum , a soil-borne plant pathogenic fungus that causes Fusarium wilt in its host, can secrete proteins into host plant cells during the infection process to interfere with the host plant defense response and promote disease occurrence. In this study, we identified a peptidase, FoAPY1, that could be secreted from F. oxysporum depending on the N-terminal signal peptide of the protein. FoAPY1 belongs to the peptidase M28 family and exerts peptidase activity in vitro . Furthermore, the FoAYP1 gene knockout strain (∆FoAYP1) presented reduced virulence to tomato plants, but its mycelial growth and conidiation were unchanged. Moreover, FoAYP1 overexpression tomato seedlings exhibited enhanced susceptibility to F. oxysporum and Botrytis cinerea strains. These data demonstrated that FoAYP1 contributes to the virulence of F. oxysporum may through peptidase activity against host plant proteins.

View Journal Article

Sponsoring Organization:: USDOE Office of Electricity (OE), Advanced Grid Research & Development. Power Systems Engineering Research

OSTI ID:: 1893792

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 13; ISSN 1664-302X

Publisher:: Frontiers Media SACopyright Statement

Country of Publication:: Switzerland

Language:: English

References (53)

A Yeast Secretion Trap Assay for Identification of Secreted Proteins from Eukaryotic Phytopathogens and Their Plant Hosts Lee, Sang-Jik; Rose, Jocelyn K. C. Plant Fungal Pathogens https://doi.org/10.1007/978-1-61779-501-5_32	book	November 2011
The Structure and Enzyme Characteristics of a Recombinant Leucine Aminopeptidase rLap1 from Aspergillus sojae and Its Application in Debittering Huang, Wei-Qian; Zhong, Li-Fen; Meng, Zhi-Zhong Applied Biochemistry and Biotechnology, Vol. 177, Issue 1 https://doi.org/10.1007/s12010-015-1737-5	journal	July 2015
Plant secretome — From cellular process to biological activity Krause, Cornelia; Richter, Sandra; Knöll, Christian Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1834, Issue 11 https://doi.org/10.1016/j.bbapap.2013.03.024	journal	November 2013
Pathogen Recognition and Innate Immunity Akira, Shizuo; Uematsu, Satoshi; Takeuchi, Osamu Cell, Vol. 124, Issue 4, p. 783-801 https://doi.org/10.1016/j.cell.2006.02.015	journal	February 2006
SnRK1: a versatile plant protein kinase that limits geminivirus infection Shen, Wei; Hanley-Bowdoin, Linda Current Opinion in Virology, Vol. 47 https://doi.org/10.1016/j.coviro.2020.12.002	journal	April 2021
Purification and characterization of a lysine aminopeptidase from Kluyveromyces marxianus Ramirezzavala, B. FEMS Microbiology Letters, Vol. 235, Issue 2 https://doi.org/10.1016/j.femsle.2004.05.009	journal	June 2004
MdPR4, a pathogenesis-related protein in apple, is involved in chitin recognition and resistance response to apple replant disease pathogens Zhou, Zhe; Zhu, Yanmin; Tian, Yi Journal of Plant Physiology, Vol. 260 https://doi.org/10.1016/j.jplph.2021.153390	journal	May 2021
The role of propeptide-mediated autoinhibition and intermolecular chaperone in the maturation of cognate catalytic domain in leucine aminopeptidase Baltulionis, G.; Blight, M.; Robin, A. Journal of Structural Biology, Vol. 213, Issue 3 https://doi.org/10.1016/j.jsb.2021.107741	journal	September 2021
Verticillium dahliae secretory effector PevD1 induces leaf senescence by promoting ORE1-mediated ethylene biosynthesis Zhang, Yi; Gao, Yuhan; Wang, Hou-Ling Molecular Plant, Vol. 14, Issue 11 https://doi.org/10.1016/j.molp.2021.07.014	journal	November 2021
Protein kinase signaling networks in plant innate immunity Tena, Guillaume; Boudsocq, Marie; Sheen, Jen Current Opinion in Plant Biology, Vol. 14, Issue 5 https://doi.org/10.1016/j.pbi.2011.05.006	journal	October 2011
Crystal Structure and Biochemical Characterization of an Aminopeptidase LapB from Legionella pneumophila Zhang, Nannan; Yin, Shiyan; Zhang, Wei Journal of Agricultural and Food Chemistry, Vol. 65, Issue 34 https://doi.org/10.1021/acs.jafc.7b02849	journal	August 2017
Inhibitory effect of obovatol from Magnolia obovata on the Salmonella type III secretion system Choi, Won-Sik; Lee, Tae Hun; Son, Se Jin The Journal of Antibiotics, Vol. 70, Issue 11 https://doi.org/10.1038/ja.2017.98	journal	September 2017
The plant immune system Jones, Jonathan D. G.; Dangl, Jeffery L. Nature, Vol. 444, Issue 7117 https://doi.org/10.1038/nature05286	journal	November 2006
Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium Ma, Li-Jun; van der Does, H. Charlotte; Borkovich, Katherine A. Nature, Vol. 464, Issue 7287 https://doi.org/10.1038/nature08850	journal	March 2010
Two pathogenesis-related proteins interact with leucine-rich repeat proteins to promote Alternaria leaf spot resistance in apple Zhang, Qiulei; Xu, Chaoran; Wei, Haiyang Horticulture Research, Vol. 8, Issue 1 https://doi.org/10.1038/s41438-021-00654-4	journal	October 2021
Direct interaction of resistance gene and avirulence gene products confers rice blast resistance Jia, Yulin; McAdams, Sean A.; Bryan, Gregory T. The EMBO Journal, Vol. 19, Issue 15 https://doi.org/10.1093/emboj/19.15.4004	journal	August 2000
Verticillium dahliaePevD1, an Alt a 1-like protein, targets cotton PR5-like protein and promotes fungal infection Zhang, Yi; Gao, Yuhan; Liang, Yingbo Journal of Experimental Botany, Vol. 70, Issue 2 https://doi.org/10.1093/jxb/ery351	journal	October 2018
Synergistic Action of a Metalloprotease and a Serine Protease from Fusarium oxysporum f. sp. lycopersici Cleaves Chitin-Binding Tomato Chitinases, Reduces Their Antifungal Activity, and Enhances Fungal Virulence Jashni, Mansoor Karimi; Dols, Ivo H. M.; Iida, Yuichiro Molecular Plant-Microbe Interactions®, Vol. 28, Issue 9 https://doi.org/10.1094/MPMI-04-15-0074-R	journal	September 2015
A Comprehensive Analysis of Genes Encoding Small Secreted Proteins Identifies Candidate Effectors in Melampsora larici-populina (Poplar Leaf Rust) Hacquard, Stéphane; Joly, David L.; Lin, Yao-Cheng Molecular Plant-Microbe Interactions, Vol. 25, Issue 3 https://doi.org/10.1094/MPMI-09-11-0238	journal	March 2012
The Fusarium oxysporum Effector Six6 Contributes to Virulence and Suppresses I-2-Mediated Cell Death Gawehns, F.; Houterman, P. M.; Ichou, F. Ait Molecular Plant-Microbe Interactions®, Vol. 27, Issue 4 https://doi.org/10.1094/MPMI-11-13-0330-R	journal	April 2014
Induction of Resistance to Verticillium dahliae in Arabidopsis thaliana by the Biocontrol Agent K-165 and Pathogenesis-Related Proteins Gene Expression Tjamos, Sotirios E.; Flemetakis, Emmanouil; Paplomatas, Epaminondas J. Molecular Plant-Microbe Interactions®, Vol. 18, Issue 6 https://doi.org/10.1094/MPMI-18-0555	journal	June 2005
Molecular Characterization of a Subtilase from the Vascular Wilt Fungus Fusarium oxysporum Pietro, Antonio Di; Huertas-González, M. Dolores; Gutierrez-Corona, J. Felix Molecular Plant-Microbe Interactions, Vol. 14, Issue 5 https://doi.org/10.1094/MPMI.2001.14.5.653	journal	May 2001
Verticillium dahliae manipulates plant immunity by glycoside hydrolase 12 proteins in conjunction with carbohydrate-binding module 1 Gui, Yue-Jing; Chen, Jie-Yin; Zhang, Dan-Dan Environmental Microbiology, Vol. 19, Issue 5 https://doi.org/10.1111/1462-2920.13695	journal	March 2017
The mixed xylem sap proteome of Fusarium oxysporum-infected tomato plants Houterman, Petra M.; Speijer, Dave; Dekker, Henk L. Molecular Plant Pathology, Vol. 8, Issue 2 https://doi.org/10.1111/j.1364-3703.2007.00384.x	journal	March 2007
A bacterial cysteine protease effector protein interferes with photosynthesis to suppress plant innate immune responses: P. syringae HopN1 targets photosynthesis Rodríguez-Herva, José J.; González-Melendi, Pablo; Cuartas-Lanza, Raquel Cellular Microbiology, Vol. 14, Issue 5 https://doi.org/10.1111/j.1462-5822.2012.01749.x	journal	February 2012
Fg12 ribonuclease secretion contributes to Fusarium graminearum virulence and induces plant cell death Yang, Bo; Wang, Yuyin; Tian, Mengjun Journal of Integrative Plant Biology, Vol. 63, Issue 2 https://doi.org/10.1111/jipb.12997	journal	August 2020
Combined action of the major secreted exo- and endopolygalacturonases is required for full virulence ofFusarium oxysporum Bravo Ruiz, Gustavo; Di Pietro, Antonio; Roncero, M. Isabel G. Molecular Plant Pathology, Vol. 17, Issue 3 https://doi.org/10.1111/mpp.12283	journal	July 2015
FoEG1, a secreted glycoside hydrolase family 12 protein from Fusarium oxysporum , triggers cell death and modulates plant immunity Zhang, Lin; Yan, Jianpei; Fu, Zhenchao Molecular Plant Pathology, Vol. 22, Issue 5 https://doi.org/10.1111/mpp.13041	journal	March 2021
Verticillium dahliae secreted protein Vd424Y is required for full virulence, targets the nucleus of plant cells, and induces cell death Liu, Lisen; Wang, Zhaohan; Li, Jianing Molecular Plant Pathology, Vol. 22, Issue 9 https://doi.org/10.1111/mpp.13100	journal	July 2021
The secreted ribonuclease T2 protein FoRnt2 contributes to Fusarium oxysporum virulence Qian, Hengwei; Wang, Lulu; Wang, Baoshan Molecular Plant Pathology, Vol. 23, Issue 9 https://doi.org/10.1111/mpp.13237	journal	June 2022
Distinct regions of the Phytophthora essential effector Avh238 determine its function in cell death activation and plant immunity suppression Yang, Bo; Wang, Qunqing; Jing, Maofeng New Phytologist, Vol. 214, Issue 1 https://doi.org/10.1111/nph.14430	journal	January 2017
The Verticillium ‐specific protein VdSCP7 localizes to the plant nucleus and modulates immunity to fungal infections Zhang, Lisha; Ni, Hao; Du, Xuan New Phytologist, Vol. 215, Issue 1 https://doi.org/10.1111/nph.14537	journal	April 2017
Characterization of an antimicrobial and phytotoxic ribonuclease secreted by the fungal wheat pathogen Zymoseptoria tritici Kettles, Graeme J.; Bayon, Carlos; Sparks, Caroline A. New Phytologist, Vol. 217, Issue 1 https://doi.org/10.1111/nph.14786	journal	September 2017
A cerato-platanin protein SsCP1 targets plant PR1 and contributes to virulence ofSclerotinia sclerotiorum Yang, Guogen; Tang, Liguang; Gong, Yingdi New Phytologist, Vol. 217, Issue 2 https://doi.org/10.1111/nph.14842	journal	October 2017
Phytophthora infestans RXLR effector PITG20303 targets a potato MKK1 protein to suppress plant immunity Du, Yu; Chen, Xiaokang; Guo, Yalu New Phytologist, Vol. 229, Issue 1 https://doi.org/10.1111/nph.16861	journal	September 2020
Fosp9, a Novel Secreted Protein, Is Essential for the Full Virulence of Fusarium oxysporum f. sp. cubense on Banana ( Musa spp.) Guo, Lijia; Wang, Jun; Liang, Changcong Applied and Environmental Microbiology, Vol. 88, Issue 6 https://doi.org/10.1128/AEM.00604-21	journal	March 2022
Adaptation Mechanism of Roots to Low and High Nitrogen Revealed by Proteomic Analysis Xin, Wei; Zhang, Lina; Gao, Jiping Rice, Vol. 14, Issue 1 https://doi.org/10.1186/s12284-020-00443-y	journal	January 2021
A SIX1 homolog in Fusarium oxysporum f.sp. cubense tropical race 4 contributes to virulence towards Cavendish banana Widinugraheni, S.; Niño-Sánchez, J.; van der Does, H. C. PLOS ONE, Vol. 13, Issue 10 https://doi.org/10.1371/journal.pone.0205896	journal	October 2018
A Small Secreted Virulence-Related Protein Is Essential for the Necrotrophic Interactions of Sclerotinia sclerotiorum with Its Host Plants Lyu, Xueliang; Shen, Cuicui; Fu, Yanping PLOS Pathogens, Vol. 12, Issue 2 https://doi.org/10.1371/journal.ppat.1005435	journal	February 2016
A Phytophthora sojae CRN effector mediates phosphorylation and degradation of plant aquaporin proteins to suppress host immune signaling Ai, Gan; Xia, Qingyue; Song, Tianqiao PLOS Pathogens, Vol. 17, Issue 3 https://doi.org/10.1371/journal.ppat.1009388	journal	March 2021
An atypical Phytophthora sojae RxLR effector manipulates host vesicle trafficking to promote infection Wang, Haonan; Guo, Baodian; Yang, Bo PLOS Pathogens, Vol. 17, Issue 11 https://doi.org/10.1371/journal.ppat.1010104	journal	November 2021
Leucine aminopeptidases: diversity in structure and function Matsui, Mikiko; Fowler, Jonathan H.; Walling, Linda L. Biological Chemistry, Vol. 387, Issue 12 https://doi.org/10.1515/BC.2006.191	journal	January 2006
Secretome-Wide Analysis of Lysine Acetylation in Fusarium oxysporum f. sp. lycopersici Provides Novel Insights Into Infection-Related Proteins Li, Jingtao; Gao, Mingming; Gabriel, Dean W. Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.559440	journal	September 2020
Identification and Expression of Secreted In Xylem Pathogenicity Genes in Fusarium oxysporum f. sp. pisi Jenkins, Sascha; Taylor, Andrew; Jackson, Alison C. Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.593140	journal	April 2021
Extracellular peptidases of the cereal pathogen Fusarium graminearum Lowe, Rohan G. T.; McCorkelle, Owen; Bleackley, Mark Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00962	journal	November 2015
The effector repertoire of Fusarium oxysporum determines the tomato xylem proteome composition following infection Gawehns, Fleur; Ma, Lisong; Bruning, Oskar Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00967	journal	November 2015
Secreted in Xylem Genes: Drivers of Host Adaptation in Fusarium oxysporum Jangir, Pooja; Mehra, Namita; Sharma, Karuna Frontiers in Plant Science, Vol. 12 https://doi.org/10.3389/fpls.2021.628611	journal	April 2021
The Role of Pathogen-Secreted Proteins in Fungal Vascular Wilt Diseases de Sain, Mara; Rep, Martijn International Journal of Molecular Sciences, Vol. 16, Issue 10 https://doi.org/10.3390/ijms161023970	journal	October 2015
iTRAQ-Based Proteomics Analyses of Sterile/Fertile Anthers from a Thermo-Sensitive Cytoplasmic Male-Sterile Wheat with Aegilops kotschyi Cytoplasm Zhang, Gaoming; Ye, Jiali; Jia, Yulin International Journal of Molecular Sciences, Vol. 19, Issue 5 https://doi.org/10.3390/ijms19051344	journal	May 2018
The Novel Cerato-Platanin-Like Protein FocCP1 from Fusarium oxysporum Triggers an Immune Response in Plants Li, Songwei; Dong, Yijie; Li, Lin International Journal of Molecular Sciences, Vol. 20, Issue 11 https://doi.org/10.3390/ijms20112849	journal	June 2019
A Cerato-Platanin Family Protein FocCP1 Is Essential for the Penetration and Virulence of Fusarium oxysporum f. sp. cubense Tropical Race 4 Liu, Siwen; Wu, Bo; Yang, Jing International Journal of Molecular Sciences, Vol. 20, Issue 15 https://doi.org/10.3390/ijms20153785	journal	August 2019
Pathogenesis-Related Genes of PR1, PR2, PR4, and PR5 Families Are Involved in the Response to Fusarium Infection in Garlic (Allium sativum L.) Anisimova, Olga K.; Shchennikova, Anna V.; Kochieva, Elena Z. International Journal of Molecular Sciences, Vol. 22, Issue 13 https://doi.org/10.3390/ijms22136688	journal	June 2021
Transcriptome Analysis Reveals the Response Mechanism of Frl-Mediated Resistance to Fusarium oxysporum f. sp. radicis-lycopersici (FORL) Infection in Tomato Sun, Yuqing; Yang, Huanhuan; Li, Jingfu International Journal of Molecular Sciences, Vol. 23, Issue 13 https://doi.org/10.3390/ijms23137078	journal	June 2022

Similar Records

MicroRNAs Suppress NB Domain Genes in Tomato That Confer Resistance to Fusarium oxysporum

Journal Article · Wed Oct 15 20:00:00 EDT 2014 · PLoS Pathogens · OSTI ID:1263545

Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium

Journal Article · Thu Mar 18 00:00:00 EDT 2010 · Nature, 464:367-373 · OSTI ID:992359

Conservation and Expansion of Transcriptional Factor Repertoire in the Fusarium oxysporum Species Complex

Journal Article · Tue Mar 14 20:00:00 EDT 2023 · Journal of Fungi · OSTI ID:2470574

The secreted FoAPY1 peptidase promotes Fusarium oxysporum invasion

Citation Formats

References (53)

Similar Records

Related Subjects