The tomato P69 subtilase family is involved in resistance to bacterial wilt.
Ralstonia solanacearum
Solanum lycopersicum
apoplast
plant defence
serine protease
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
27 Dec 2023
27 Dec 2023
Historique:
revised:
13
12
2023
received:
01
09
2023
accepted:
15
12
2023
medline:
27
12
2023
pubmed:
27
12
2023
entrez:
27
12
2023
Statut:
aheadofprint
Résumé
The intercellular space or apoplast constitutes the main interface in plant-pathogen interactions. Apoplastic subtilisin-like proteases-subtilases-may play an important role in defence and they have been identified as targets of pathogen-secreted effector proteins. Here, we characterise the role of the Solanaceae-specific P69 subtilase family in the interaction between tomato and the vascular bacterial wilt pathogen Ralstonia solanacearum. R. solanacearum infection post-translationally activated several tomato P69s. Among them, P69D was exclusively activated in tomato plants resistant to R. solanacearum. In vitro experiments showed that P69D activation by prodomain removal occurred in an autocatalytic and intramolecular reaction that does not rely on the residue upstream of the processing site. Importantly P69D-deficient tomato plants were more susceptible to bacterial wilt and transient expression of P69B, D and G in Nicotiana benthamiana limited proliferation of R. solanacearum. Our study demonstrates that P69s have conserved features but diverse functions in tomato and that P69D is involved in resistance to R. solanacearum but not to other vascular pathogens like Fusarium oxysporum.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Ministerio de Universidades
ID : FPU15/02125
Organisme : Agence Nationale de la Recherche
ID : ANR11-BTBR-0001-GENIUS
Organisme : Ministerio de Ciencia e Innovación
ID : CEX2019-000917
Organisme : Ministerio de Ciencia e Innovación
ID : MCIN/AEI/PID2019-108595RB-I00
Organisme : Ministerio de Ciencia e Innovación
ID : TED2021-131457B-I00
Organisme : Nederlandse Organisatie voor Toegepast Natuurwetenschappelijk Onderzoek
ID : 865.14.003
Organisme : Consejo Superior de Investigaciones Científicas
Informations de copyright
© 2023 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Beck, S., Michalski, A., Raether, O., Lubeck, M., Kaspar, S., Goedecke, N. et al. (2015) The impact II, a very high-resolution quadrupole time-of-flight instrument (QTOF) for deep shotgun proteomics. Molecular & Cellular Proteomics, 14(7), 2014-2029.
Boersema, P.J., Raijmakers, R., Lemeer, S., Mohammed, S. & Heck, A.J. (2009) Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nature Protocols, 4(4), 484-494.
Bykova, N.V., Rampitsch, C., Krokhin, O., Standing, K.G. & Ens, W. (2006) Determination and characterization of site-specific N-glycosylation using MALDI-Qq-TOF tandem mass spectrometry: case study with a plant protease. Analytical Chemistry, 78(4), 1093-1103.
Cedzich, A., Huttenlocher, F., Kuhn, B.M., Pfannstiel, J., Gabler, L., Stintzi, A. et al. (2009) The protease-associated domain and C-terminal extension are required for zymogen processing, sorting within the secretory pathway, and activity of tomato subtilase 3 (SlSBT3). The Journal of Biological Chemistry, 284(21), 14068-14078.
Chen, Y.L., Lee, C.Y., Cheng, K.T., Chang, W.H., Huang, R.N., Nam, H.G. et al. (2014) Quantitative peptidomics study reveals that a wound-induced peptide from PR-1 regulates immune signaling in tomato. The Plant Cell, 26(10), 4135-4148.
Chichkova, N.V., Shaw, J., Galiullina, R.A., Drury, G.E., Tuzhikov, A.I., Kim, S.H. et al. (2010) Phytaspase, a relocalisable cell death promoting plant protease with caspase specificity. The EMBO Journal, 29(6), 1149-1161.
Colaert, N., Helsens, K., Martens, L., Vandekerckhove, J. & Gevaert, K. (2009) Improved visualization of protein consensus sequences by iceLogo. Nature Methods, 6(11), 786-787.
Cruz, A.P., Ferreira, V., Pianzzola, M.J., Siri, M.I., Coll, N.S. & Valls, M. (2014) A novel, sensitive method to evaluate potato germplasm for bacterial wilt resistance using a luminescent Ralstonia solanacearum reporter strain. Molecular Plant-Microbe Interactions, 27(3), 277-285.
Danilo, B., Perrot, L., Botton, E., Nogue, F. & Mazier, M. (2018) The DFR locus: a smart landing pad for targeted transgene insertion in tomato. PLoS One, 13(12), e0208395.
de Lamo, F.J., Constantin, M.E., Fresno, D.H., Boeren, S., Rep, M. & Takken, F.L.W. (2018) Xylem sap proteomics reveals distinct differences between R gene- and endophyte-mediated resistance against Fusarium wilt disease in tomato. Frontiers in Microbiology, 9, 2977.
de Lamo, F.J., Simkovicova, M., Fresno, D.H., de Groot, T., Tintor, N., Rep, M. et al. (2021) Pattern-triggered immunity restricts host colonization by endophytic fusaria, but does not affect endophyte-mediated resistance. Molecular Plant Pathology, 22(2), 204-215.
Demir, F. & Huesgen, P.F. (2022) A user guide to validation, annotation, and evaluation of N-Terminome datasets with MANTI. Methods in Molecular Biology, 2447, 271-283.
Demir, F., Kizhakkedathu, J.N., Rinschen, M.M. & Huesgen, P.F. (2021) MANTI: automated annotation of protein N-termini for rapid interpretation of N-Terminome data sets. Analytical Chemistry, 93(13), 5596-5605.
Demir, F., Niedermaier, S., Villamor, J.G. & Huesgen, P.F. (2018) Quantitative proteomics in plant protease substrate identification. The New Phytologist, 218(3), 936-943.
Demir, F., Perrar, A., Mantz, M. & Huesgen, P.F. (2022) Sensitive plant N-terminome profiling with HUNTER. Methods in Molecular Biology, 2447, 139-158.
Deutsch, E.W., Bandeira, N., Perez-Riverol, Y., Sharma, V., Carver, J.J., Mendoza, L. et al. (2023) The ProteomeXchange consortium at 10 years: 2023 update. Nucleic Acids Research, 51(D1), D1539-D1548.
Du, Y., Stegmann, M. & Misas Villamil, J.C. (2016) The apoplast as battleground for plant-microbe interactions. The New Phytologist, 209(1), 34-38.
French, E., Kim, B.S., Rivera-Zuluaga, K. & Iyer-Pascuzzi, A.S. (2018) Whole root transcriptomic analysis suggests a role for auxin pathways in resistance to Ralstonia solanacearum in tomato. Molecular Plant-Microbe Interactions, 31(4), 432-444.
Gawehns, F., Ma, L., Bruning, O., Houterman, P.M., Boeren, S., Cornelissen, B.J. et al. (2015) The effector repertoire of Fusarium oxysporum determines the tomato xylem proteome composition following infection. Frontiers in Plant Science, 6, 967.
Gleave, A.P. (1992) A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Molecular Biology, 20(6), 1203-1207.
Granell, A., Bellés, J.M. & Conejero, V. (1987) Induction of pathogenesis-related proteins in tomato by citrus exocortis viroid, silver ion and ethephon. Physiological and Molecular Plant Pathology, 31(1), 83-90.
Grimault, V., Gélie, B., Lemattre, M., Prior, P. & Schmit, J. (1994) Comparative histology of resistant and susceptible tomato cultivars infected by Pseudomonas solanacearum. Physiological and Molecular Plant Pathology, 44, 105-123.
Gupta, R., Lee, S.E., Agrawal, G.K., Rakwal, R., Park, S., Wang, Y. et al. (2015) Understanding the plant-pathogen interactions in the context of proteomics-generated apoplastic proteins inventory. Frontiers in Plant Science, 6, 352.
Haeussler, M., Schonig, K., Eckert, H., Eschstruth, A., Mianne, J., Renaud, J.B. et al. (2016) Evaluation of off-target and on-target scoring algorithms and integration into the guide RNA selection tool CRISPOR. Genome Biology, 17(1), 148.
Hayward, A.C. (1991) Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annual Review of Phytopathology, 29, 65-87.
Homma, F., Huang, J. & van der Hoorn, R.A.L. (2023) Alphafold-multimer predicts cross-kingdom interactions at the plant-pathogen interface. bioRxiv. 2023:2023.04.03.535425.
Ishihara, T., Mitsuhara, I., Takahashi, H. & Nakaho, K. (2012) Transcriptome analysis of quantitative resistance-specific response upon Ralstonia solanacearum infection in tomato. PLoS One, 7(10), e46763.
Jorda, L., Coego, A., Conejero, V. & Vera, P. (1999) A genomic cluster containing four differentially regulated subtilisin-like processing protease genes is in tomato plants. The Journal of Biological Chemistry, 274(4), 2360-2365.
Jorda, L., Conejero, V. & Vera, P. (2000) Characterization of P69E and P69F, two differentially regulated genes encoding new members of the subtilisin-like proteinase family from tomato plants. Plant Physiology, 122(1), 67-74.
Macho, A.P. & Zipfel, C. (2014) Plant PRRs and the activation of innate immune signaling. Molecular Cell, 54(2), 263-272.
Mahon, P. & Bateman, A. (2000) The PA domain: a protease-associated domain. Protein Science, 9(10), 1930-1934.
Marlatt, M., Correll, J.C., Kaufmann, P. & Cooper, P. (1996) Two genetically distinct populations of Fusarium oxysporum f.sp. lycopersicirace 3 in the United States. Plant Disease, 80(12), 1336.
Mazier, M., Flamain, F., Nicolai, M., Sarnette, V. & Caranta, C. (2011) Knock-down of both eIF4E1 and eIF4E2 genes confers broad-spectrum resistance against potyviruses in tomato. PLoS One, 6(12), e29595.
Meichtry, J., Amrhein, N. & Schaller, A. (1999) Characterization of the subtilase gene family in tomato (Lycopersicon esculentum Mill.). Plant Molecular Biology, 39(4), 749-760.
Mes, J.J., Weststeijn, E.A., Herlaar, F., Lambalk, J.J., Wijbrandi, J., Haring, M.A. et al. (1999) Biological and molecular characterization of Fusarium oxysporum f.sp. lycopersici divides race 1 isolates into separate virulence groups. Phytopathology, 89(2), 156-160.
Meyer, M., Leptihn, S., Welz, M. & Schaller, A. (2016) Functional characterization of propeptides in plant Subtilases as intramolecular chaperones and inhibitors of the mature protease. The Journal of Biological Chemistry, 291(37), 19449-19461.
Mirdita, M., Schutze, K., Moriwaki, Y., Heo, L., Ovchinnikov, S. & Steinegger, M. (2022) ColabFold: making protein folding accessible to all. Nature Methods, 19(6):679-+, 679-682.
Muller, L., Cameron, A., Fortenberry, Y., Apletalina, E.V. & Lindberg, I. (2000) Processing and sorting of the prohormone convertase 2 propeptide. The Journal of Biological Chemistry, 275(50), 39213-39222.
Nebes, V.L. & Jones, E.W. (1991) Activation of the proteinase B precursor of the yeast Saccharomyces cerevisiae by autocatalysis and by an internal sequence. The Journal of Biological Chemistry, 266(34), 22851-22857.
Ottmann, C., Rose, R., Huttenlocher, F., Cedzich, A., Hauske, P., Kaiser, M. et al. (2009) Structural basis for Ca2+-independence and activation by homodimerization of tomato subtilase 3. Proceedings of the National Academy of Sciences of the United States of America, 106(40), 17223-17228.
Paulus, J.K., Kourelis, J., Ramasubramanian, S., Homma, F., Godson, A., Horger, A.C. et al. (2020) Extracellular proteolytic cascade in tomato activates immune protease Rcr3. Proceedings of the National Academy of Sciences of the United States of America, 117(29), 17409-17417.
Perez-Riverol, Y., Bai, J., Bandla, C., Garcia-Seisdedos, D., Hewapathirana, S., Kamatchinathan, S. et al. (2022) The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences. Nucleic Acids Research, 50(D1), D543-D552.
Planas-Marques, M., Bernardo-Faura, M., Paulus, J., Kaschani, F., Kaiser, M., Valls, M. et al. (2018) Protease activities triggered by Ralstonia solanacearum infection in susceptible and tolerant tomato lines. Molecular & Cellular Proteomics, 17(6), 1112-1125.
Planas-Marques, M., Kressin, J.P., Kashyap, A., Panthee, D.R., Louws, F.J., Coll, N.S. et al. (2020) Four bottlenecks restrict colonization and invasion by the pathogen Ralstonia solanacearum in resistant tomato. Journal of Experimental Botany, 71(6), 2157-2171.
Poueymiro, M., Cunnac, S., Barberis, P., Deslandes, L., Peeters, N., Cazale-Noel, A.C. et al. (2009) Two type III secretion system effectors from Ralstonia solanacearum GMI1000 determine host-range specificity on tobacco. Molecular Plant-Microbe Interactions, 22(5), 538-550.
Power, S.D., Adams, R.M. & Wells, J.A. (1986) Secretion and autoproteolytic maturation of subtilisin. Proceedings of the National Academy of Sciences of the United States of America, 83(10), 3096-3100.
Rappsilber, J., Mann, M. & Ishihama, Y. (2007) Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nature Protocols, 2(8), 1896-1906.
Reichardt, S., Repper, D., Tuzhikov, A.I., Galiullina, R.A., Planas-Marques, M., Chichkova, N.V. et al. (2018) The tomato subtilase family includes several cell death-related proteinases with caspase specificity. Scientific Reports, 8(1), 10531.
Rep, M., van der Does, H.C., Meijer, M., van Wijk, R., Houterman, P.M., Dekker, H.L. et al. (2004) A small, cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3-mediated resistance in tomato. Molecular Microbiology, 53(5), 1373-1383.
Royek, S., Bayer, M., Pfannstiel, J., Pleiss, J., Ingram, G., Stintzi, A. et al. (2022) Processing of a plant peptide hormone precursor facilitated by posttranslational tyrosine sulfation. Proceedings of the National Academy of Sciences of the United States of America, 119(16), e2201195119.
Schaller, A., Stintzi, A., Rivas, S., Serrano, I., Chichkova, N.V., Vartapetian, A.B. et al. (2018) From structure to function - a family portrait of plant subtilases. The New Phytologist, 218(3), 901-915.
Schilling, O., Huesgen, P.F., Barre, O., Auf dem Keller, U. & Overall, C.M. (2011) Characterization of the prime and non-prime active site specificities of proteases by proteome-derived peptide libraries and tandem mass spectrometry. Nature Protocols, 6(1), 111-120.
Schilling, O. & Overall, C.M. (2008) Proteome-derived, database-searchable peptide libraries for identifying protease cleavage sites. Nature Biotechnology, 26(6), 685-694.
Smith, E.L., Markland, F.S., Kasper, C.B., DeLange, R.J., Landon, M. & Evans, W.H. (1966) The complete amino acid sequence of two types of subtilisin, BPN and Carlsberg. The Journal of Biological Chemistry, 241(24), 5974-5976.
Song, J., Win, J., Tian, M., Schornack, S., Kaschani, F., Ilyas, M. et al. (2009) Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. Proceedings of the National Academy of Sciences of the United States of America, 106(5), 1654-1659.
Tan-Wilson, A., Bandak, B. & Prabu-Jeyabalan, M. (2012) The PA domain is crucial for determining optimum substrate length for soybean protease C1: structure and kinetics correlate with molecular function. Plant Physiology and Biochemistry, 53, 27-32.
Tian, M., Benedetti, B. & Kamoun, S. (2005) A second Kazal-like protease inhibitor from Phytophthora infestans inhibits and interacts with the apoplastic pathogenesis-related protease P69B of tomato. Plant Physiology, 138(3), 1785-1793.
Tian, M., Huitema, E., Da Cunha, L., Torto-Alalibo, T. & Kamoun, S. (2004) A Kazal-like extracellular serine protease inhibitor from Phytophthora infestans targets the tomato pathogenesis-related protease P69B. The Journal of Biological Chemistry, 279(25), 26370-26377.
Tian, M., Win, J., Song, J., van der Hoorn, R., van der Knaap, E. & Kamoun, S. (2007) A Phytophthora infestans cystatin-like protein targets a novel tomato papain-like apoplastic protease. Plant Physiology, 143(1), 364-377.
Tornero, P., Conejero, V. & Vera, P. (1997) Identification of a new pathogen-induced member of the subtilisin-like processing protease family from plants. The Journal of Biological Chemistry, 272(22), 14412-14419.
Tornero, P., Mayda, E., Gomez, M.D., Canas, L., Conejero, V. & Vera, P. (1996) Characterization of LRP, a leucine-rich repeat (LRR) protein from tomato plants that is processed during pathogenesis. The Plant Journal, 10(2), 315-330.
Tyanova, S., Temu, T. & Cox, J. (2016) The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nature Protocols, 11(12), 2301-2319.
Vartapetian, A.B., Tuzhikov, A.I., Chichkova, N.V., Taliansky, M. & Wolpert, T.J. (2011) A plant alternative to animal caspases: subtilisin-like proteases. Cell Death and Differentiation, 18(8), 1289-1297.
Vasse, J., Frey, P. & Trigalet, A. (1995) Microscopic studies of intercellular infection and protoxylem invasion of tomato roots by Pseudomonas solanacearum. Molecular Plant-Microbe Interactions, 8, 241-251.
Vera, P. & Conejero, V. (1988) Pathogenesis-related proteins of tomato: p-69 as an alkaline endoproteinase. Plant Physiology, 87(1), 58-63.
Vera, P. & Conejero, V. (1989) The induction and accumulation of the pathogenesis-related P69 proteinase in tomato during citrus exocortis viroid infection and in response to chemical treatments. Physiological and Molecular Plant Pathology, 34(4), 323-334.
Vera, P., Yago, J.H. & Conejero, V. (1989) Immunogold localization of the citrus exocortis viroid-induced pathogenesis-related proteinase p69 in tomato leaves. Plant Physiology, 91(1), 119-123.
Vey, M., Schafer, W., Berghofer, S., Klenk, H.D. & Garten, W. (1994) Maturation of the trans-Golgi network protease furin: compartmentalization of propeptide removal, substrate cleavage, and COOH-terminal truncation. The Journal of Cell Biology, 127(6 Pt 2), 1829-1842.
Wang, S., Xing, R., Wang, Y., Shu, H., Fu, S., Huang, J. et al. (2021) Cleavage of a pathogen apoplastic protein by plant subtilases activates host immunity. The New Phytologist, 229(6), 3424-3439.
Xiao, Y., Hsiao, T.H., Suresh, U., Chen, H.I., Wu, X., Wolf, S.E. et al. (2014) A novel significance score for gene selection and ranking. Bioinformatics, 30(6), 801-807.
Yu, S.H., Ferretti, D., Schessner, J.P., Rudolph, J.D., Borner, G.H.H. & Cox, J. (2020) Expanding the Perseus software for omics data analysis with custom plugins. Current Protocols in Bioinformatics, 71(1), e105.
Zuluaga, A.P., Sole, M., Lu, H., Gongora-Castillo, E., Vaillancourt, B., Coll, N. et al. (2015) Transcriptome responses to Ralstonia solanacearum infection in the roots of the wild potato Solanum commersonii. BMC Genomics, 16, 246.
Zuluaga, A.P., Vega-Arreguin, J.C., Fei, Z., Matas, A.J., Patev, S., Fry, W.E. et al. (2016) Analysis of the tomato leaf transcriptome during successive hemibiotrophic stages of a compatible interaction with the oomycete pathogen Phytophthora infestans. Molecular Plant Pathology, 17(1), 42-54.