Interaction Between Glycoside Hydrolase FsGH28c from Fusarium solani and PnPUB35 Confers Resistance in Piper nigrum
Abstract
1. Introduction
2. Results
2.1. Identification and Expression Patterns of the GH28 Family Genes in F. solani
2.2. The FsGH28c Induced Cell Death in N. benthamiana
2.3. FsGH28c Is Required for the Utilization of Certain Carbon Sources
2.4. FsGH28c Is Required for Microconidia Development
2.5. The FsGH28c Is Required for Full Virulence on Black Pepper
2.6. FsGH28c Interacts with PnPUB35
2.7. PnPUB35 Plays a Positive Role in Resistance to F. solani
3. Materials and Methods
3.1. Fungus and Plant
3.2. PVX Vector Construction and Transient Expression Assay
3.3. Yeast Signal Sequence Trap System
3.4. The Fungal Transformation Constructs
3.5. Fungal Transformations
3.6. Carbon Source Utilization Assays
3.7. Pathogenicity
3.8. Scanning Electron Microscope Assay
3.9. Yeast Two-Hybrid Assays
3.10. BiFC Analysis and Subcellular Localization
3.11. Virus-Induced Gene Silencing (VIGS)
3.12. Callose Deposition
3.13. Arabidopsis Transformation
3.14. Protein Extraction and Western Blotting
3.15. Nucleic Acid Extraction and Expression Analysis
3.16. Bioinformatics Analysis
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Kikot, G.E.; Hours, R.A.; Alconada, T.M. Contribution of cell wall degrading enzymes to pathogenesis of Fusarium graminearum: A review. J. Basic Microbiol. 2009, 49, 231–241. [Google Scholar] [CrossRef] [PubMed]
- Klöckner, A.; Bühl, H.; Viollier, P.; Henrichfreise, B. Deconstructing the Chlamydial Cell Wall. Biol. Chlamydia 2018, 412, 1–33. [Google Scholar]
- Brito, N.; Espino, J.J.; González, C. The endo-beta-1,4-xylanase xyn11A is required for virulence in Botrytis cinerea. Mol. Plant-Microbe Interact. 2006, 19, 25–32. [Google Scholar] [CrossRef] [PubMed]
- Hématy, K.; Cherk, C.; Somerville, S. Host–pathogen warfare at the plant cell wall. Curr. Opin. Plant Biol. 2009, 12, 406–413. [Google Scholar] [CrossRef] [PubMed]
- Tzima, A.K.; Paplomatas, E.J.; Rauyaree, P.; Ospina-Giraldo, M.D.; Kang, S. VdSNF1, the Sucrose Nonfermenting Protein Kinase Gene of Verticillium dahliae, Is Required for Virulence and Expression of Genes Involved in Cell-Wall Degradation. Mol. Plant-Microbe Interact. 2011, 24, 129–142. [Google Scholar] [CrossRef]
- Ben-Daniel, B.; Bar-Zvi, D.; Tsror, L. Pectate lyase affects pathogenicity in natural isolates of Colletotrichum coccodes and in pelA gene-disrupted and gene-overexpressing mutant lines. Mol. Plant Pathol. 2012, 13, 187–197. [Google Scholar] [CrossRef]
- Yang, Y.; Zhang, Y.; Li, B.; Yang, X.; Dong, Y.; Qiu, D. A Verticillium dahliae Pectate Lyase Induces Plant Immune Responses and Contributes to Virulence. Front. Plant Sci. 2018, 9, 1271. [Google Scholar] [CrossRef]
- Zhu, W.; Ronen, M.; Gur, Y.; Minz-Dub, A.; Masrati, G.; Ben-Tal, N.; Savidor, A.; Sharon, I.; Eizner, E.; Valerius, O.; et al. BcXYG1, a Secreted Xyloglucanase from Botrytis cinerea, Triggers Both Cell Death and Plant Immune Responses. Plant Physiol. 2017, 175, 438–456. [Google Scholar] [CrossRef]
- Ma, Z.; Song, T.; Zhu, L.; Ye, W.; Wang, Y.; Shao, Y.; Dong, S.; Zhang, Z.; Dou, D.; Zheng, X.; et al. A Phytophthora sojae Glycoside Hydrolase 12 Protein Is a Major Virulence Factor during Soybean Infection and Is Recognized as a PAMP. Plant Cell 2015, 27, 2057–2072. [Google Scholar] [CrossRef]
- Ascurra, Y.C.T.; Zhang, L.; Toghani, A.; Hua, C.; Rangegowda, N.J.; Posbeyikian, A.; Pai, H.; Lin, X.; Wolters, P.J.; Wouters, D.; et al. Functional diversification of a wild potato immune receptor at its center of origin. Science 2023, 381, 891–897. [Google Scholar] [CrossRef]
- Kubicek, C.P.; Starr, T.L.; Glass, N.L. Plant Cell Wall–Degrading Enzymes and Their Secretion in Plant-Pathogenic Fungi. Annu. Rev. Phytopathol. 2014, 52, 427–451. [Google Scholar] [CrossRef] [PubMed]
- Lewis, M.W.; E Leslie, M.; Liljegren, S.J. Plant separation: 50 ways to leave your mother. Curr. Opin. Plant Biol. 2006, 9, 59–65. [Google Scholar] [CrossRef] [PubMed]
- Rui, Y.; Xiao, C.; Yi, H.; Kandemir, B.; Wang, J.Z.; Puri, V.M.; Anderson, C.T. POLYGALACTURONASE INVOLVED IN EXPANSION3 Functions in Seedling Development, Rosette Growth, and Stomatal Dynamics in Arabidopsis thaliana. Plant Cell 2017, 29, 2413–2432. [Google Scholar] [CrossRef] [PubMed]
- Wen, Y.; Zhou, J.; Feng, H.; Sun, W.; Zhang, Y.; Zhao, L.; Cheng, Y.; Feng, Z.; Zhu, H.; Wei, F. VdGAL4 Modulates Microsclerotium Formation, Conidial Morphology, and Germination to Promote Virulence in Verticillium dahliae. Microbiol. Spectr. 2023, 11, e0351522. [Google Scholar] [CrossRef]
- Liu, S.; Liu, R.; Lv, J.; Feng, Z.; Wei, F.; Zhao, L.; Zhang, Y.; Zhu, H.; Feng, H. The glycoside hydrolase 28 member VdEPG1 is a virulence factor of Verticillium dahliae and interacts with the jasmonic acid pathway-related gene GhOPR9. Mol. Plant Pathol. 2023, 24, 1238–1255. [Google Scholar] [CrossRef]
- Ma, Z.; Zhu, L.; Song, T.; Wang, Y.; Zhang, Q.; Xia, Y.; Qiu, M.; Lin, Y.; Li, H.; Kong, L.; et al. A paralogous decoy protects Phytophthora sojae apoplastic effector PsXEG1 from a host inhibitor. Science 2017, 355, 710–714. [Google Scholar] [CrossRef]
- Gui, Y.-J.; Zhang, W.-Q.; Zhang, D.-D.; Zhou, L.; Short, D.P.G.; Wang, J.; Ma, X.-F.; Li, T.-G.; Kong, Z.-Q.; Wang, B.-L.; et al. A Verticillium dahliae Extracellular Cutinase Modulates Plant Immune Responses. Mol. Plant-Microbe Interact. 2018, 31, 260–273. [Google Scholar] [CrossRef]
- Reignault, P.; Valette-Collet, O.; Boccara, M. The importance of fungal pectinolytic enzymes in plant invasion, host adaptability and symptom type. Eur. J. Plant Pathol. 2008, 120, 1–11. [Google Scholar] [CrossRef]
- Poinssot, B.; Vandelle, E.; Bentéjac, M.; Adrian, M.; Levis, C.; Brygoo, Y.; Garin, J.; Sicilia, F.; Coutos-Thévenot, P.; Pugin, A. The Endopolygalacturonase 1 from Botrytis cinerea Activates Grapevine Defense Reactions Unrelated to Its Enzymatic Activity. Mol. Plant-Microbe Interact. 2003, 16, 553–564. [Google Scholar] [CrossRef]
- Kars, I.; Krooshof, G.H.; Wagemakers, L.; Joosten, R.; Benen, J.A.E.; Van Kan, J.A.L. Necrotizing activity of five Botrytis cinerea endopolygalacturonases produced in Pichia pastoris. Plant J. 2005, 43, 213–225. [Google Scholar] [CrossRef]
- Isshiki, A.; Akimitsu, K.; Yamamoto, M.; Yamamoto, H. Endopolygalacturonase Is Essential for Citrus Black Rot Caused by Alternaria citribut Not Brown Spot Caused by Alternaria alternata. Mol. Plant-Microbe Interact. 2001, 14, 749–757. [Google Scholar] [CrossRef] [PubMed]
- Thilini Chethana, K.W.; Peng, J.; Li, X.; Xing, Q.; Liu, M.; Zhang, W.; Hyde, K.D.; Zhao, W.; Yan, J. LtEPG1, a Secretory Endopolygalacturonase Protein, Regulates the Virulence of Lasiodiplodia theobromae in Vitis vinifera and Is Recognized as a Microbe-Associated Molecular Patterns. Phytopathology 2020, 110, 1727–1736. [Google Scholar] [CrossRef] [PubMed]
- Vierstra, R.D. The ubiquitin–26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 2009, 10, 385–397. [Google Scholar] [CrossRef] [PubMed]
- Buetow, L.; Huang, D.T. Structural insights into the catalysis and regulation of E3 ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 2016, 17, 626–642. [Google Scholar] [CrossRef]
- Ye, Q.; Wang, H.; Su, T.; Wu, W.-H.; Chen, Y.-F. The Ubiquitin E3 Ligase PRU1 Regulates WRKY6 Degradation to Modulate Phosphate Homeostasis in Response to Low-Pi Stress in Arabidopsis. Plant Cell 2018, 30, 1062–1076. [Google Scholar] [CrossRef]
- Zhou, J.; Liu, D.; Wang, P.; Ma, X.; Lin, W.; Chen, S.; Mishev, K.; Lu, D.; Kumar, R.; Vanhoutte, I. Regulation of Arabidopsis brassinosteroid receptor BRI1 endocytosis and degradation by plant U-box PUB12/PUB13-mediated ubiquitination. Proc. Natl. Acad. Sci. USA 2018, 115, E1906–E1915. [Google Scholar] [CrossRef]
- Xiao, Z.; Yang, C.; Liu, C.; Yang, L.; Yang, S.; Zhou, J.; Li, F.; Jiang, L.; Xiao, S.; Gao, C.; et al. SINAT E3 ligases regulate the stability of the ESCRT component FREE1 in response to iron deficiency in plants. J. Integr. Plant Biol. 2020, 62, 1399–1417. [Google Scholar] [CrossRef]
- Ma, A.; Zhang, D.; Wang, G.; Wang, K.; Li, Z.; Gao, Y.; Li, H.; Bian, C.; Cheng, J.; Han, Y.; et al. Verticillium dahlia effector VDAL protects MYB6 from degradation by interacting with PUB25 and PUB26 E3 ligases to enhance Verticillium wilt resistance. Plant Cell 2021, 33, 3675–3699. [Google Scholar] [CrossRef]
- Pringa, E.; Martinez-Noel, G.; Müller, U.; Harbers, K. Interaction of the RING Finger-related U-box Motif of a Nuclear Dot Protein with Ubiquitin-conjugating Enzymes. J. Biol. Chem. 2001, 276, 19617–19623. [Google Scholar] [CrossRef]
- Mudgil, Y.; Shiu, S.-H.; Stone, S.L.; Salt, J.N.; Goring, D.R. A Large Complement of the Predicted Arabidopsis ARM Repeat Proteins Are Members of the U-Box E3 Ubiquitin Ligase Family. Plant Physiol. 2004, 134, 59–66. [Google Scholar] [CrossRef]
- Stegmann, M.; Anderson, R.G.; Ichimura, K.; Pecenkova, T.; Reuter, P.; Žárský, V.; McDowell, J.M.; Shirasu, K.; Trujillo, M. The Ubiquitin Ligase PUB22 Targets a Subunit of the Exocyst Complex Required for PAMP-Triggered Responses in Arabidopsis. Plant Cell 2012, 24, 4703–4716. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.; Grubb, L.E.; Wang, J.; Liang, X.; Li, L.; Gao, C.; Ma, M.; Feng, F.; Li, M.; Li, L.; et al. A Regulatory Module Controlling Homeostasis of a Plant Immune Kinase. Mol. Cell 2018, 69, 493–504.e6. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Ding, Y.; Li, Z.; Shi, Y.; Wang, J.; Hua, J.; Gong, Z.; Zhou, J.-M.; Yang, S. PUB25 and PUB26 Promote Plant Freezing Tolerance by Degrading the Cold Signaling Negative Regulator MYB15. Dev. Cell 2019, 51, 222–235.e5. [Google Scholar] [CrossRef]
- Li, J.; Zhang, Y.; Gao, Z.; Xu, X.; Wang, Y.; Lin, Y.; Ye, P.; Huang, T. Plant U-box E3 ligases PUB25 and PUB26 control organ growth in Arabidopsis. New Phytol. 2021, 229, 403–413. [Google Scholar] [CrossRef]
- Qin, T.; Liu, S.; Zhang, Z.; Sun, L.; He, X.; Lindsey, K.; Zhu, L.; Zhang, X. GhCyP3 improves the resistance of cotton to Verticillium dahliae by inhibiting the E3 ubiquitin ligase activity of GhPUB17. Plant Mol. Biol. 2019, 99, 379–393. [Google Scholar] [CrossRef]
- Li, J.M.; Ye, M.Y.; Wang, C.; Ma, X.H.; Wu, N.N.; Zhong, C.L.; Zhang, Y.; Cheng, N.; Nakata, P.A.; Zeng, L.; et al. Soybean GmSAUL1, a Bona Fide U-Box E3 Ligase, Negatively Regulates Immunity Likely through Repressing the Activation of GmMPK3. Int. J. Mol. Sci. 2023, 24, 6240. [Google Scholar] [CrossRef]
- Han, P.-L.; Dong, Y.-H.; Gu, K.-D.; Yu, J.-Q.; Hu, D.-G.; Hao, Y.-J. The apple U-box E3 ubiquitin ligase MdPUB29 contributes to activate plant immune response to the fungal pathogen Botryosphaeria dothidea. Planta 2019, 249, 1177–1188. [Google Scholar] [CrossRef]
- Hu, L.; Xu, Z.; Wang, M.; Fan, R.; Yuan, D.; Wu, B.; Wu, H.; Qin, X.; Yan, L.; Tan, L.; et al. The chromosome-scale reference genome of black pepper provides insight into piperine biosynthesis. Nat. Commun. 2019, 10, 4702. [Google Scholar] [CrossRef]
- Liu, S.; Liu, R.; Chu, B.; Li, Z.; Meng, Q.; Gou, Y.; Xue, C.; Tian, T.; Chen, P.; Wei, F.; et al. Identification and screening of fungicides against Piper nigrum basal Fusarium wilt disease in Hainan, China. J. Basic Microbiol. 2023, 63, 1254–1264. [Google Scholar] [CrossRef]
- Kiba, A.; Nakano, M.; Ohnishi, K.; Hikichi, Y. The SEC14 phospholipid transfer protein regulates pathogen-associated molecular pattern-triggered immunity in Nicotiana benthamiana. Plant Physiol. Biochem. 2018, 125, 212–218. [Google Scholar] [CrossRef]
- Heese, A.; Hann, D.R.; Gimenez-Ibanez, S.; Jones, A.M.; He, K.; Li, J.; Schroeder, J.I.; Peck, S.C.; Rathjen, J.P. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl. Acad. Sci. USA 2007, 104, 12217–12222. [Google Scholar] [CrossRef] [PubMed]
- Asai, S.; Yoshioka, H. Nitric Oxide as a Partner of Reactive Oxygen Species Participates in Disease Resistance to Necrotrophic Pathogen Botrytis cinerea in Nicotiana benthamiana. Mol. Plant-Microbe Interact. 2009, 22, 619–629. [Google Scholar] [CrossRef] [PubMed]
- Ishihama, N.; Yamada, R.; Yoshioka, M.; Katou, S.; Yoshioka, H. Phosphorylation of the Nicotiana benthamiana WRKY8 Transcription Factor by MAPK Functions in the Defense Response. Plant Cell 2011, 23, 1153–1170. [Google Scholar] [CrossRef]
- Liu, J.; Wang, C.; Kong, L.; Yang, Y.; Cui, X.; Li, K.; Nian, H. Rho2 involved in development, stress response and pathogenicity of Fusarium oxysporum. World J. Microbiol. Biotechnol. 2023, 39, 272. [Google Scholar] [CrossRef]
- Lightfoot, J.D.; Fuller, K.K. CRISPR/Cas9-Mediated Gene Replacement in the Fungal Keratitis Pathogen Fusarium solani var. petroliphilum. Microorganisms 2019, 7, 457. [Google Scholar] [CrossRef]
- Liu, L.; Wang, Z.; Li, J.; Wang, Y.; Yuan, J.; Zhan, J.; Wang, P.; Lin, Y.; Li, F.; Ge, X. Verticillium dahliae secreted protein Vd424Y is required for full virulence, targets the nucleus of plant cells, and induces cell death. Mol. Plant Pathol. 2021, 22, 1109–1120. [Google Scholar] [CrossRef]
- Jacobs, K.A.; Collins-Racie, L.A.; Colbert, M.; Duckett, M.; Golden-Fleet, M.; Kelleher, K.; Kriz, R.; LaVallie, E.R.; Merberg, D.; Spaulding, V.; et al. A genetic selection for isolating cDNAs encoding secreted proteins. Gene 1997, 198, 289–296. [Google Scholar] [CrossRef]
- Su, X.; Rehman, L.; Guo, H.; Li, X.; Zhang, R.; Cheng, H. AAC as a Potential Target Gene to Control Verticillium dahliae. Genes 2017, 8, 25. [Google Scholar] [CrossRef]
- Rehman, L.; Su, X.; Guo, H.; Qi, X.; Cheng, H. Protoplast transformation as a potential platform for exploring gene function in Verticillium dahliae. BMC Biotechnol. 2016, 16, 57. [Google Scholar] [CrossRef]
- Yu, X.; Li, L.; Guo, M.; Chory, J.; Yin, Y. Modulation of brassinosteroid-regulated gene expression by jumonji domain-containing proteins ELF6 and REF6 in Arabidopsis. Proc. Natl. Acad. Sci. USA 2008, 105, 7618–7623. [Google Scholar] [CrossRef]
- Tang, Y.; Zhang, Z.; Lei, Y.; Hu, G.; Liu, J.; Hao, M.; Chen, A.; Peng, Q.; Wu, J. Cotton WATs Modulate SA Biosynthesis and Local Lignin Deposition Participating in Plant Resistance Against Verticillium dahliae. Front. Plant Sci. 2019, 10, 526. [Google Scholar] [CrossRef] [PubMed]
- Liu, S.; Sun, R.; Zhang, X.; Feng, Z.; Wei, F.; Zhao, L.; Zhang, Y.; Zhu, L.; Feng, H.; Zhu, H. Genome-Wide Analysis of OPR Family Genes in Cotton Identified a Role for GhOPR9 in Verticillium dahliae Resistance. Genes 2020, 11, 1134. [Google Scholar] [CrossRef] [PubMed]
- Clough, S.J.; Bent, A.F. Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998, 16, 735–743. [Google Scholar] [CrossRef] [PubMed]
- Bai, H.; Lan, J.P.; Gan, Q.; Wang, X.Y.; Hou, M.M.; Cao, Y.H.; Li, L.Y.; Liu, L.J.; Hao, Y.J.; Yin, C.C.; et al. Identification and expression analysis of components involved in rice Xa21-mediated disease resistance signalling. Plant Biol. 2012, 14, 914–922. [Google Scholar] [CrossRef]
- El-Gebali, S.; Mistry, J.; Bateman, A.; Eddy, S.R.; Luciani, A.; Potter, S.C.; Qureshi, M.; Richardson, L.J.; Salazar, G.A.; Smart, A.; et al. The Pfam protein families database in 2019. Nucleic Acids Res. 2019, 47, D427–D432. [Google Scholar] [CrossRef]
- Finn, R.D.; Clements, J.; Eddy, S.R. HMMER web server: Interactive sequence similarity searching. Nucleic Acids Res. 2011, 39, W29–W37. [Google Scholar] [CrossRef]
- Edgar, R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32, 1792–1797. [Google Scholar] [CrossRef]
- Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef]
- Nalim, F.A.; Samuels, G.J.; Wijesundera, R.L.; Geiser, D.M. New species from the Fusarium solani species complex derived from perithecia and soil in the Old World tropics. Mycologia 2011, 103, 1302–1330. [Google Scholar] [CrossRef]
- Da Luz, S.F.; Yamaguchi, L.F.; Kato, M.J.; De Lemos, O.F.; Xavier, L.P.; Maia, J.G.S.; Ramos, A.D.R.; Setzer, W.N.; Da Silva, J.K.D.R. Secondary Metabolic Profiles of Two Cultivars of Piper nigrum (Black Pepper) Resulting from Infection by Fusarium solani f. sp. piperis. Int. J. Mol. Sci. 2017, 18, 2434. [Google Scholar] [CrossRef]
- Kamali-Sarvestani, S.; Mostowfizadeh-Ghalamfarsa, R.; Salmaninezhad, F.; Cacciola, S.O. Fusarium and Neocosmospora Species Associated with Rot of Cactaceae and Other Succulent Plants. J. Fungi 2022, 8, 364. [Google Scholar] [CrossRef] [PubMed]
- Romberg, M.K.; Davis, R.M. Host Range and Phylogeny of Fusarium solani f. sp. eumartii from Potato and Tomato in California. Plant Dis. 2007, 91, 585–592. [Google Scholar]
- Villarino, M.; De la Lastra, E.; Basallote-Ureba, M.J.; Capote, N.; Larena, I.; Melgarejo, P.; De Cal, A. Characterization of Fusarium solani Populations Associated with Spanish Strawberry Crops. Plant Dis. 2019, 103, 1974–1982. [Google Scholar] [CrossRef]
- Gherbawy, Y.A.; Hussein, M.A.; Hassany, N.A.; Shebany, Y.M.; Hassan, S.; El-Dawy, E.G.A.E. Phylogeny and pathogenicity of Fusarium solani species complex (FSSC) associated with potato tubers. J. Basic Microbiol. 2021, 61, 1133–1144. [Google Scholar] [CrossRef]
- Li, J.; Li, C. Fusarium solani Causing Root Rot Disease on Gastrodia elata in Shaxi, China. Plant Dis. 2022, 106, 320. [Google Scholar] [CrossRef]
- O’Donnell, K.; Sutton, D.A.; Fothergill, A.; McCarthy, D.; Rinaldi, M.G.; Brandt, M.E.; Zhang, N.; Geiser, D.M. Molecular phylogenetic diversity, multilocus haplotype nomenclature, and in vitro antifungal resistance within the Fusarium solani species complex. J. Clin. Microbiol. 2008, 46, 2477–2490. [Google Scholar] [CrossRef]
- Muhammed, M.; Anagnostou, T.; Desalermos, A.; Kourkoumpetis, T.K.; Carneiro, H.A.; Glavis-Bloom, J.; Coleman, J.J.; Mylonakis, E. Fusarium infection: Report of 26 cases and review of 97 cases from the literature. Medicine 2013, 92, 305–316. [Google Scholar] [CrossRef]
- Xu, L.-J.; Xie, L.-X. Fusarium solani Activates Dectin-1 in Experimentally Induced Keratomycosis. Curr. Med. Sci. 2018, 38, 153–159. [Google Scholar] [CrossRef]
- Zipfel, C. Plant pattern-recognition receptors. Trends Immunol. 2014, 35, 345–351. [Google Scholar] [CrossRef]
- Gui, Y.; Chen, J.; Zhang, D.; Li, N.; Li, T.; Zhang, W.; Wang, X.; Short, D.P.G.; Li, L.; Guo, W.; et al. Verticillium dahliae manipulates plant immunity by glycoside hydrolase 12 proteins in conjunction with carbohydrate-binding module 1. Environ. Microbiol. 2017, 19, 1914–1932. [Google Scholar] [CrossRef]
- Kanneganti, T.-D.; Huitema, E.; Kamoun, S. In planta expression of oomycete and fungal genes. Methods Mol. Biol. 2007, 354, 35–43. [Google Scholar] [PubMed]
- Ma, L.; Lukasik, E.; Gawehns, F.; Takken, F.L.W. The use of agroinfiltration for transient expression of plant resistance and fungal effector proteins in Nicotiana benthamiana leaves. Methods Mol. Biol. 2012, 835, 61–74. [Google Scholar] [PubMed]
- Zhou, B.-J.; Jia, P.-S.; Gao, F.; Guo, H.-S. Molecular Characterization and Functional Analysis of a Necrosis- and Ethylene-Inducing, Protein-Encoding Gene Family from Verticillium dahliae. Mol. Plant-Microbe Interact. 2012, 25, 964–975. [Google Scholar] [CrossRef] [PubMed]
- Santhanam, P.; van Esse, H.P.; Albert, I.; Faino, L.; Nürnberger, T.; Thomma, B.P.H.J. Evidence for Functional Diversification Within a Fungal NEP1-Like Protein Family. Mol. Plant-Microbe Interact. 2013, 26, 278–286. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.; Yan, J.; Fu, Z.; Shi, W.; Ninkuu, V.; Li, G.; Yang, X.; Zeng, H. FoEG1, a secreted glycoside hydrolase family 12 protein from Fusarium oxysporum, triggers cell death and modulates plant immunity. Mol. Plant Pathol. 2021, 22, 522–538. [Google Scholar] [CrossRef]
- Fradin, E.F.; Thomma, B.P. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol. Plant Pathol. 2006, 7, 71–86. [Google Scholar] [CrossRef]
- Zhang, X.; Zhao, L.; Liu, S.; Zhou, J.; Wu, Y.; Feng, Z.; Zhang, Y.; Zhu, H.; Wei, F.; Feng, H. Identification and Functional Analysis of a Novel Hydrophobic Protein VdHP1 from Verticillium dahliae. Microbiol. Spectr. 2022, 10, e0247821. [Google Scholar] [CrossRef]
- Qian, H.; Wang, L.; Wang, B.; Liang, W. The secreted ribonuclease T2 protein FoRnt2 contributes to Fusarium oxysporum virulence. Mol. Plant Pathol. 2022, 23, 1346–1360. [Google Scholar] [CrossRef]
- Han, S.; Sheng, B.; Zhu, D.; Chen, J.; Cai, H.; Zhang, S.; Guo, C. Role of FoERG3 in Ergosterol Biosynthesis by Fusarium oxysporum and the Associated Regulation by Bacillus subtilis HSY21. Plant Dis. 2023, 107, 1565–1575. [Google Scholar] [CrossRef]
- Zhao, Y.-L.; Zhou, T.-T.; Guo, H.-S. Hyphopodium-Specific VdNoxB/VdPls1-Dependent ROS-Ca2+ Signaling Is Required for Plant Infection by Verticillium dahliae. PLoS Pathog. 2016, 12, e1005793. [Google Scholar] [CrossRef]
- Yu, J.; Li, T.; Tian, L.; Tang, C.; Klosterman, S.J.; Tian, C.; Wang, Y. Two Verticillium dahliae MAPKKKs, VdSsk2 and VdSte11, Have Distinct Roles in Pathogenicity, Microsclerotial Formation, and Stress Adaptation. Msphere 2019, 4, 10–1128. [Google Scholar] [CrossRef] [PubMed]
- Lv, J.; Liu, S.; Zhang, X.; Zhao, L.; Zhang, T.; Zhang, Z.; Feng, Z.; Wei, F.; Zhou, J.; Zhao, R.; et al. VdERG2 was involved in ergosterol biosynthesis, nutritional differentiation and virulence of Verticillium dahliae. Curr. Genet. 2023, 69, 25–40. [Google Scholar] [CrossRef] [PubMed]
- Gurdaswani, V.; Ghag, S.B.; Ganapathi, T.R. FocSge1 in Fusarium oxysporum f. sp. cubense race 1 is essential for full virulence. BMC Microbiol. 2020, 20, 255. [Google Scholar] [CrossRef] [PubMed]
- Zheng, L.; Qiu, B.; Su, L.; Wang, H.; Cui, X.; Ge, F.; Liu, D. Panax notoginseng WRKY Transcription Factor 9 Is a Positive Regulator in Responding to Root Rot Pathogen Fusarium solani. Front. Plant Sci. 2022, 13, 930644. [Google Scholar] [CrossRef]
- Liu, Y.; Liu, Q.; Li, X.; Tang, Z.; Zhang, Z.; Gao, H.; Ma, F.; Li, C. Exogenous Dopamine and MdTyDC Overexpression Enhance Apple Resistance to Fusarium solani. Phytopathology 2022, 112, 2503–2513. [Google Scholar] [CrossRef]
- Wang, M.; Tang, W.; Xiang, L.; Chen, X.; Shen, X.; Yin, C.; Mao, Z. Involvement of MdWRKY40 in the defense of mycorrhizal apple against Fusarium solani. BMC Plant Biol. 2022, 22, 385. [Google Scholar] [CrossRef]
- Li, J.; Luan, Q.; Han, J.; Chen, C.; Ren, Z. CsMYB60 Confers Enhanced Resistance to Fusarium solani by Increasing Proanthocyanidin Biosynthesis in Cucumber. Phytopathology 2022, 112, 588–594. [Google Scholar] [CrossRef]
- He, Q.; McLellan, H.; Boevink, P.C.; Sadanandom, A.; Xie, C.; Birch, P.R.J.; Tian, Z. U-box E3 ubiquitin ligase PUB17 acts in the nucleus to promote specific immune pathways triggered by Phytophthora infestans. J. Exp. Bot. 2015, 66, 3189–3199. [Google Scholar] [CrossRef]
- Orosa, B.; He, Q.; Mesmar, J.; Gilroy, E.M.; McLellan, H.; Yang, C.; Craig, A.; Bailey, M.; Zhang, C.; Moore, J.D.; et al. BTB-BACK Domain Protein POB1 Suppresses Immune Cell Death by Targeting Ubiquitin E3 ligase PUB17 for Degradation. PLoS Genet. 2017, 13, e1006540. [Google Scholar] [CrossRef]
- Amador, V.; Monte, E.; García-Martínez, J.-L.; Prat, S. Gibberellins Signal Nuclear Import of PHOR1, a Photoperiod-Responsive Protein with Homology to Drosophila armadillo. Cell 2001, 106, 343–354. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Liu, S.; Xing, T.; Liu, R.; Gao, S.; Yang, J.; Tian, T.; Zhang, C.; Sun, S.; Zhao, C. Interaction Between Glycoside Hydrolase FsGH28c from Fusarium solani and PnPUB35 Confers Resistance in Piper nigrum. Int. J. Mol. Sci. 2025, 26, 4189. https://doi.org/10.3390/ijms26094189
Liu S, Xing T, Liu R, Gao S, Yang J, Tian T, Zhang C, Sun S, Zhao C. Interaction Between Glycoside Hydrolase FsGH28c from Fusarium solani and PnPUB35 Confers Resistance in Piper nigrum. International Journal of Molecular Sciences. 2025; 26(9):4189. https://doi.org/10.3390/ijms26094189
Chicago/Turabian StyleLiu, Shichao, Tianci Xing, Ruibing Liu, Shengfeng Gao, Jianfeng Yang, Tian Tian, Chong Zhang, Shiwei Sun, and Chenchen Zhao. 2025. "Interaction Between Glycoside Hydrolase FsGH28c from Fusarium solani and PnPUB35 Confers Resistance in Piper nigrum" International Journal of Molecular Sciences 26, no. 9: 4189. https://doi.org/10.3390/ijms26094189
APA StyleLiu, S., Xing, T., Liu, R., Gao, S., Yang, J., Tian, T., Zhang, C., Sun, S., & Zhao, C. (2025). Interaction Between Glycoside Hydrolase FsGH28c from Fusarium solani and PnPUB35 Confers Resistance in Piper nigrum. International Journal of Molecular Sciences, 26(9), 4189. https://doi.org/10.3390/ijms26094189