The Phytophthora parasitica effector AVH195 interacts with ATG8, attenuates host autophagy, and promotes biotrophic infection.
Autophagy
Biotrophy
Effector
Oomycete
Vacuoles
Journal
BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720
Informations de publication
Date de publication:
29 Apr 2024
29 Apr 2024
Historique:
received:
05
01
2024
accepted:
22
04
2024
medline:
29
4
2024
pubmed:
29
4
2024
entrez:
28
4
2024
Statut:
epublish
Résumé
Plant pathogens secrete effector proteins into host cells to suppress immune responses and manipulate fundamental cellular processes. One of these processes is autophagy, an essential recycling mechanism in eukaryotic cells that coordinates the turnover of cellular components and contributes to the decision on cell death or survival. We report the characterization of AVH195, an effector from the broad-spectrum oomycete plant pathogen, Phytophthora parasitica. We show that P. parasitica expresses AVH195 during the biotrophic phase of plant infection, i.e., the initial phase in which host cells are maintained alive. In tobacco, the effector prevents the initiation of cell death, which is caused by two pathogen-derived effectors and the proapoptotic BAX protein. AVH195 associates with the plant vacuolar membrane system and interacts with Autophagy-related protein 8 (ATG8) isoforms/paralogs. When expressed in cells from the green alga, Chlamydomonas reinhardtii, the effector delays vacuolar fusion and cargo turnover upon stimulation of autophagy, but does not affect algal viability. In Arabidopsis thaliana, AVH195 delays the turnover of ATG8 from endomembranes and promotes plant susceptibility to P. parasitica and the obligate biotrophic oomycete pathogen Hyaloperonospora arabidopsidis. Taken together, our observations suggest that AVH195 targets ATG8 to attenuate autophagy and prevent associated host cell death, thereby favoring biotrophy during the early stages of the infection process.
Sections du résumé
BACKGROUND
BACKGROUND
Plant pathogens secrete effector proteins into host cells to suppress immune responses and manipulate fundamental cellular processes. One of these processes is autophagy, an essential recycling mechanism in eukaryotic cells that coordinates the turnover of cellular components and contributes to the decision on cell death or survival.
RESULTS
RESULTS
We report the characterization of AVH195, an effector from the broad-spectrum oomycete plant pathogen, Phytophthora parasitica. We show that P. parasitica expresses AVH195 during the biotrophic phase of plant infection, i.e., the initial phase in which host cells are maintained alive. In tobacco, the effector prevents the initiation of cell death, which is caused by two pathogen-derived effectors and the proapoptotic BAX protein. AVH195 associates with the plant vacuolar membrane system and interacts with Autophagy-related protein 8 (ATG8) isoforms/paralogs. When expressed in cells from the green alga, Chlamydomonas reinhardtii, the effector delays vacuolar fusion and cargo turnover upon stimulation of autophagy, but does not affect algal viability. In Arabidopsis thaliana, AVH195 delays the turnover of ATG8 from endomembranes and promotes plant susceptibility to P. parasitica and the obligate biotrophic oomycete pathogen Hyaloperonospora arabidopsidis.
CONCLUSIONS
CONCLUSIONS
Taken together, our observations suggest that AVH195 targets ATG8 to attenuate autophagy and prevent associated host cell death, thereby favoring biotrophy during the early stages of the infection process.
Identifiants
pubmed: 38679707
doi: 10.1186/s12915-024-01899-w
pii: 10.1186/s12915-024-01899-w
doi:
Substances chimiques
Autophagy-Related Protein 8 Family
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
100Subventions
Organisme : Agence Nationale de la Recherche
ID : ANR-11-LABX-0028-0
Organisme : Agence Nationale de la Recherche
ID : ANR-11-IDEX-0001-02
Organisme : Agence Nationale de la Recherche
ID : ANR-13-JSV5-0005
Organisme : FP7 Food, Agriculture and Fisheries, Biotechnology
ID : Plant-KBBE dsRNAguard
Informations de copyright
© 2024. The Author(s).
Références
Kamoun S, Furzer O, Jones JD, Judelson HS, Ali GS, Dalio RJ, et al. The Top 10 oomycete pathogens in molecular plant pathology. Mol Plant Pathol. 2015;16(4):413–34.
pubmed: 25178392
doi: 10.1111/mpp.12190
Boevink PC, Birch PRJ, Turnbull D, Whisson SC. Devastating intimacy: the cell biology of plant-Phytophthora interactions. New Phytol. 2020;228(2):445–58.
pubmed: 32394464
pmcid: 7540312
doi: 10.1111/nph.16650
Franceschetti M, Maqbool A, Jiménez-Dalmaroni MJ, Pennington HG, Kamoun S, Banfield MJ. Effectors of filamentous plant pathogens: commonalities amid diversity. Microbiol Mol Biol Rev. 2017;81(2):e00066-e116.
pubmed: 28356329
pmcid: 5485802
doi: 10.1128/MMBR.00066-16
Kanja C, Hammond-Kosack KE. Proteinaceous effector discovery and characterization in filamentous plant pathogens. Mol Plant Pathol. 2020;21(10):1353–76.
pubmed: 32767620
pmcid: 7488470
doi: 10.1111/mpp.12980
Wang Y, Tyler BM, Wang Y. Defense and counterdefense during plant-pathogenic oomycete infection. Annu Rev Microbiol. 2019;73:667–96.
pubmed: 31226025
doi: 10.1146/annurev-micro-020518-120022
Bassham DC, Laporte M, Marty F, Moriyasu Y, Ohsumi Y, Olsen LJ, Yoshimoto K. Autophagy in development and stress responses of plants. Autophagy. 2006;2(1):2–11.
pubmed: 16874030
doi: 10.4161/auto.2092
Slavikova S, Ufaz S, Avin-Wittenberg T, Levanony H, Galili G. An autophagy-associated Atg8 protein is involved in the responses of Arabidopsis seedlings to hormonal controls and abiotic stresses. J Exp Bot. 2008;59(14):4029–43.
pubmed: 18836138
pmcid: 2576633
doi: 10.1093/jxb/ern244
Leary AY, Savage Z, Tumtas Y, Bozkurt TO. Contrasting and emerging roles of autophagy in plant immunity. Curr Opin Plant Biol. 2019;52:46–53.
pubmed: 31442734
doi: 10.1016/j.pbi.2019.07.002
Lal NK, Thanasuwat B, Chan B, Dinesh-Kumar SP. Pathogens manipulate host autophagy through injected effector proteins. Autophagy. 2020;16(12):2301–2.
pubmed: 33016188
pmcid: 7751661
doi: 10.1080/15548627.2020.1831816
Yang M, Zhang Y, Xie X, Yue N, Li J, Wang XB, et al. Barley stripe mosaic virus γb protein subverts autophagy to promote viral infection by disrupting the ATG7-ATG8 interaction. Plant Cell. 2018;30(7):1582–95.
pubmed: 29848767
pmcid: 6096602
doi: 10.1105/tpc.18.00122
Lal NK, Thanasuwat B, Huang PJ, Cavanaugh KA, Carter A, Michelmore RW, Dinesh-Kumar SP. Phytopathogen effectors use multiple mechanisms to manipulate plant autophagy. Cell Host Microbe. 2020;28(4):558-571.e6.
pubmed: 32810441
doi: 10.1016/j.chom.2020.07.010
Kabbage M, Williams B, Dickman MB. Cell death control: the interplay of apoptosis and autophagy in the pathogenicity of Sclerotinia sclerotiorum. PLoS Pathog. 2013;9(4):e1003287.
pubmed: 23592997
pmcid: 3623803
doi: 10.1371/journal.ppat.1003287
Dagdas YF, Belhaj K, Maqbool A, Chaparro-Garcia A, Pandey P, Petre B, et al. An effector of the Irish potato famine pathogen antagonizes a host autophagy cargo receptor. Elife. 2016;5:e10856.
pubmed: 26765567
pmcid: 4775223
doi: 10.7554/eLife.10856
Üstün S, Hafrén A, Liu Q, Marshall RS, Minina EA, Bozhkov PV, et al. Bacteria exploit autophagy for proteasome degradation and enhanced virulence in plants. Plant Cell. 2018;30(3):668–85.
pubmed: 29500318
pmcid: 5894834
doi: 10.1105/tpc.17.00815
Panabières F, Ali GS, Allagui MB, Dalio RJD, Gudmestad NC, Kuhn M-L, et al. Phytophthora nicotianae diseases worldwide: new knowledge of a long-recognised pathogen. Phytopathol Mediterr. 2016;55(1):20–40.
Judelson HS, Ah-Fong AMV. Exchanges at the plant-oomycete interface that influence disease. Plant Physiol. 2019;179(4):1198–211.
pubmed: 30538168
doi: 10.1104/pp.18.00979
Le Berre JY, Engler G, Panabières F. Exploration of the late stages of the tomato-Phytophthora parasitica interactions through histological analysis and generation of expressed sequence tags. New Phytol. 2008;177(2):480–92.
pubmed: 18028297
doi: 10.1111/j.1469-8137.2007.02269.x
Jacomin AC, Samavedam S, Promponas V, Nezis IP. iLIR database: a web resource for LIR motif-containing proteins in eukaryotes. Autophagy. 2016;12(10):1945–53.
pubmed: 27484196
pmcid: 5079668
doi: 10.1080/15548627.2016.1207016
Kalvari I, Tsompanis S, Mulakkal NC, Osgood R, Johansen T, Nezis IP, Promponas VJ. iLIR: a web resource for prediction of Atg8-family interacting proteins. Autophagy. 2014;10(5):913–25.
pubmed: 24589857
pmcid: 5119064
doi: 10.4161/auto.28260
Attard A, Gourgues M, Callemeyn-Torre N, Keller H. The immediate activation of defense responses in Arabidopsis roots is not sufficient to prevent Phytophthora parasitica infection. New Phytol. 2010;187(2):449–60.
pubmed: 20456058
doi: 10.1111/j.1469-8137.2010.03272.x
Jupe J, Stam R, Howden AJ, Morris JA, Zhang R, Hedley PE, Huitema E. Phytophthora capsici-tomato interaction features dramatic shifts in gene expression associated with a hemi-biotrophic lifestyle. Genome Biol. 2013;14(6):R63.
pubmed: 23799990
pmcid: 4054836
doi: 10.1186/gb-2013-14-6-r63
Shan L, Thara VK, Martin GB, Zhou JM, Tang X. The Pseudomonas AvrPto protein is differentially recognized by tomato and tobacco and is localized to the plant plasma membrane. Plant Cell. 2000;12(12):2323–38.
pubmed: 11148281
pmcid: 102221
doi: 10.1105/tpc.12.12.2323
Lacomme C, Santa CS. Bax-induced cell death in tobacco is similar to the hypersensitive response. Proc Natl Acad Sci U S A. 1999;96(14):7956–61.
pubmed: 10393929
pmcid: 22169
doi: 10.1073/pnas.96.14.7956
Li G, Huang S, Guo X, Li Y, Yang Y, Guo Z, et al. Cloning and characterization of r3b; members of the r3 superfamily of late blight resistance genes show sequence and functional divergence. Mol Plant Microbe Interact. 2011;24(10):1132–42.
pubmed: 21649512
doi: 10.1094/MPMI-11-10-0276
Gu B, Gao W, Liu Z, Shao G, Peng Q, Mu Y, et al. A single region of the Phytophthora infestans avirulence effector Avr3b functions in both cell death induction and plant immunity suppression. Mol Plant Pathol. 2023;24(4):317–30.
pubmed: 36696541
pmcid: 10013827
doi: 10.1111/mpp.13298
Liu Y, Schiff M, Czymmek K, Tallóczy Z, Levine B, Dinesh-Kumar SP. Autophagy regulates programmed cell death during the plant innate immune response. Cell. 2005;121(4):567–77.
pubmed: 15907470
doi: 10.1016/j.cell.2005.03.007
Feng Q, De Rycke R, Dagdas Y, Nowack MK. Autophagy promotes programmed cell death and corpse clearance in specific cell types of the Arabidopsis root cap. Curr Biol. 2022;32(20):4548.
pubmed: 36283347
pmcid: 9632325
doi: 10.1016/j.cub.2022.10.006
Kellner R, De la Concepcion JC, Maqbool A, Kamoun S, Dagdas YF. ATG8 expansion: a driver of selective autophagy diversification? Trends Plant Sci. 2017;22(3):204–14.
pubmed: 28038982
doi: 10.1016/j.tplants.2016.11.015
Seo E, Woo J, Park E, Bertolani SJ, Siegel JB, Choi D, Dinesh-Kumar SP. Comparative analyses of ubiquitin-like ATG8 and cysteine protease ATG4 autophagy genes in the plant lineage and cross-kingdom processing of ATG8 by ATG4. Autophagy. 2016;12(11):2054–68.
pubmed: 27540766
pmcid: 5103345
doi: 10.1080/15548627.2016.1217373
Avin-Wittenberg T, Honig A, Galili G. Variations on a theme: plant autophagy in comparison to yeast and mammals. Protoplasma. 2012;249(2):285–99.
pubmed: 21660427
doi: 10.1007/s00709-011-0296-z
Bu F, Yang M, Guo X, Huang W, Chen L. Multiple functions of ATG8 family proteins in plant autophagy. Front Cell Dev Biol. 2020;8:466.
pubmed: 32596242
pmcid: 7301642
doi: 10.3389/fcell.2020.00466
Grefen C, Obrdlik P, Harter K. The determination of protein-protein interactions by the mating-based split-ubiquitin system (mbSUS). Methods Mol Biol. 2009;479:217–33.
pubmed: 19083185
doi: 10.1007/978-1-59745-289-2_14
Schneider S, Beyhl D, Hedrich R, Sauer N. Functional and physiological characterization of Arabidopsis INOSITOL TRANSPORTER1, a novel tonoplast-localized transporter for myo-inositol. Plant Cell. 2008;20(4):1073–87.
pubmed: 18441213
pmcid: 2390729
doi: 10.1105/tpc.107.055632
Wolfenstetter S, Wirsching P, Dotzauer D, Schneider S, Sauer N. Routes to the tonoplast: the sorting of tonoplast transporters in Arabidopsis mesophyll protoplasts. Plant Cell. 2012;24(1):215–32.
pubmed: 22253225
pmcid: 3289566
doi: 10.1105/tpc.111.090415
Kim JH, Jung H, Choi YE, Chung T. Autophagy inducers lead to transient accumulation of autophagosomes in Arabidopsis roots. Plant Cell Rep. 2022;41(2):463–71.
pubmed: 34977975
doi: 10.1007/s00299-021-02821-2
Harris EH. Chlamydomonas as a model organism. Annu Rev Plant Physiol Plant Mol Biol. 2001;52:363–406.
pubmed: 11337403
doi: 10.1146/annurev.arplant.52.1.363
Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, et al. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science. 2007;318(5848):245–50.
pubmed: 17932292
pmcid: 2875087
doi: 10.1126/science.1143609
Lyons AB. Analysing cell division in vivo and in vitro using flow cytometric measurement of CFSE dye dilution. J Immunol Methods. 2000;243(1–2):147–54.
pubmed: 10986412
doi: 10.1016/S0022-1759(00)00231-3
Crespo JL, Díaz-Troya S, Florencio FJ. Inhibition of target of rapamycin signaling by rapamycin in the unicellular green alga Chlamydomonas reinhardtii. Plant Physiol. 2005;139(4):1736–49.
pubmed: 16299168
pmcid: 1310555
doi: 10.1104/pp.105.070847
Izumi M, Hidema J, Makino A, Ishida H. Autophagy contributes to nighttime energy availability for growth in Arabidopsis. Plant Physiol. 2013;161(4):1682–93.
pubmed: 23457226
pmcid: 3613448
doi: 10.1104/pp.113.215632
Yan HZ, Liou RF. Selection of internal control genes for real-time quantitative RT-PCR assays in the oomycete plant pathogen Phytophthora parasitica. Fungal Genet Biol. 2006;43(6):430–8.
pubmed: 16531084
doi: 10.1016/j.fgb.2006.01.010
Attard A, Evangelisti E, Kebdani-Minet N, Panabières F, Deleury E, Maggio C, et al. Transcriptome dynamics of Arabidopsis thaliana root penetration by the oomycete pathogen Phytophthora parasitica. BMC Genomics. 2014;15(1):538.
pubmed: 24974100
pmcid: 4111850
doi: 10.1186/1471-2164-15-538
Hok S, Danchin EG, Allasia V, Panabières F, Attard A, Keller H. An Arabidopsis (malectin-like) leucine-rich repeat receptor-like kinase contributes to downy mildew disease. Plant Cell Environ. 2011;34(11):1944–57.
pubmed: 21711359
doi: 10.1111/j.1365-3040.2011.02390.x
Wang Y, Wang Y. Phytophthora sojae effectors orchestrate warfare with host immunity. Curr Opin Microbiol. 2018;46:7–13.
pubmed: 29454192
doi: 10.1016/j.mib.2018.01.008
Ramirez-Garcés D, Camborde L, Pel MJ, Jauneau A, Martinez Y, Néant I, et al. CRN13 candidate effectors from plant and animal eukaryotic pathogens are DNA-binding proteins which trigger host DNA damage response. New Phytol. 2016;210(2):602–17.
pubmed: 26700936
doi: 10.1111/nph.13774
Couso I, Pérez-Pérez ME, Martínez-Force E, Kim HS, He Y, Umen JG, Crespo JL. Autophagic flux is required for the synthesis of triacylglycerols and ribosomal protein turnover in Chlamydomonas. J Exp Bot. 2018;69(6):1355–67.
pubmed: 29053817
doi: 10.1093/jxb/erx372
Pandey P, Leary AY, Tumtas Y, Savage Z, Dagvadorj B, Duggan C, et al. An oomycete effector subverts host vesicle trafficking to channel starvation-induced autophagy to the pathogen interface. Elife. 2021;10:e65285.
pubmed: 34424198
pmcid: 8382295
doi: 10.7554/eLife.65285
Gillaspy GE. The cellular language of myo-inositol signaling. New Phytol. 2011;192(4):823–39.
pubmed: 22050576
doi: 10.1111/j.1469-8137.2011.03939.x
Sarkar S, Floto RA, Berger Z, Imarisio S, Cordenier A, Pasco M, et al. Lithium induces autophagy by inhibiting inositol monophosphatase. J Cell Biol. 2005;170(7):1101–11.
pubmed: 16186256
pmcid: 2171537
doi: 10.1083/jcb.200504035
Cheong H, Klionsky DJ. Biochemical methods to monitor autophagy-related processes in yeast. Methods Enzymol. 2008;451:1–26.
pubmed: 19185709
doi: 10.1016/S0076-6879(08)03201-1
Patel S, Dinesh-Kumar SP. Arabidopsis ATG6 is required to limit the pathogen-associated cell death response. Autophagy. 2008;4(1):20–7.
pubmed: 17932459
doi: 10.4161/auto.5056
Coll NS, Smidler A, Puigvert M, Popa C, Valls M, Dangl JL. The plant metacaspase AtMC1 in pathogen-triggered programmed cell death and aging: functional linkage with autophagy. Cell Death Differ. 2014;21(9):1399–408.
pubmed: 24786830
pmcid: 4131171
doi: 10.1038/cdd.2014.50
Langin G, Gouguet P, Üstün S. Microbial effector proteins - a journey through the proteolytic landscape. Trends Microbiol. 2020;28(7):523–35.
pubmed: 32544439
doi: 10.1016/j.tim.2020.02.010
Le Berre JY, Gourgues M, Samans B, Keller H, Panabières F, Attard A. Transcriptome dynamic of Arabidopsis roots infected with Phytophthora parasitica identifies VQ29, a gene induced during the penetration and involved in the restriction of infection. PLoS ONE. 2017;12(12):e0190341.
pubmed: 29281727
pmcid: 5744986
doi: 10.1371/journal.pone.0190341
Evangelisti E, Govetto B, Minet-Kebdani N, Kuhn ML, Attard A, Ponchet M, et al. The Phytophthora parasitica RXLR effector penetration-specific effector 1 favours Arabidopsis thaliana infection by interfering with auxin physiology. New Phytol. 2013;199(2):476–89.
pubmed: 23594295
doi: 10.1111/nph.12270
Galiana E, Rivière MP, Pagnotta S, Baudouin E, Panabières F, Gounon P, Boudier L. Plant-induced cell death in the oomycete pathogen Phytophthora parasitica. Cell Microbiol. 2005;7(9):1365–78.
pubmed: 16098223
doi: 10.1111/j.1462-5822.2005.00565.x
Harris EH. The Chlamydomonas Sourcebook. A Comprehensive Guide to Biology and Laboratory Use. San Diego, CA: Academic Press; 1989.
Kong F, Liang Y, Légeret B, Beyly-Adriano A, Blangy S, Haslam RP, et al. Chlamydomonas carries out fatty acid β-oxidation in ancestral peroxisomes using a bona fide acyl-CoA oxidase. Plant J. 2017;90(2):358–71.
pubmed: 28142200
doi: 10.1111/tpj.13498
Panabières F, Le Berre JY. A family of repeated DNA in the genome of the oomycete plant pathogen Phytophthora cryptogea. Curr Genet. 1999;36(1–2):105–12.
pubmed: 10447602
Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16(6):735–43.
pubmed: 10069079
doi: 10.1046/j.1365-313x.1998.00343.x
Giordano L, Allasia V, Cremades A, Hok S, Panabières F, Bailly-Maître B, Keller H. A plant receptor domain with functional analogies to animal malectin disables ER stress responses upon infection. iScience. 2022;25(3):103877.
pubmed: 35243239
pmcid: 8861646
doi: 10.1016/j.isci.2022.103877
Le SQ, Gascuel O. An improved general amino acid replacement matrix. Mol Biol Evol. 2008;25(7):1307–20.
pubmed: 18367465
doi: 10.1093/molbev/msn067