A Secreted Lignin Peroxidase Required for Fungal Growth and Virulence and Related to Plant Immune Response
Abstract
:1. Introduction
2. Results
2.1. Seven Lignin Peroxidase Paralogs Detected in B. kuwatsukai
2.2. BkLiP1 Contributes to the Vegetative Growth and Virulence in B. kuwatsukai
2.3. BkLiP2 Has No Obvious Impact on the Virulence in B. kuwatsukai
2.4. The SP in BkLiP1 Required for Its Secretion and Function
2.5. BkLiP1 Localizes on the Cell Wall of B. kuwatsukai
2.6. BkLiP1 Can Be Delivered into Plant Extracellular Space with the Aid of SP
2.7. BkLiP1 Induces Plant Immunity Responses
3. Discussion
4. Materials and Methods
4.1. Culture Conditions and Fungal Transformation
4.2. Bioinformatics Analyses
4.3. RNA Extraction and RT-qPCR
4.4. Plant Growth and Virulence Assays
4.5. Assays for the Function of the SP of BkLiP1
4.6. Assay for the Location of the BkLiP1 in B. kuwatsukai
4.7. Subcellular Localization Assay
4.8. Cell Death, ROS Activity, and Callose Deposition Induction Assay
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Marsberg, A.; Kemler, M.; Jami, F.; Nagel, J.H.; Postma-Smidt, A.; Naidoo, S.; Wingfield, M.J.; Crous, P.W.; Spatafora, J.W.; Hesse, C.N.; et al. Botryosphaeria dothidea: A latent pathogen of global importance to woody plant health. Mol. Plant Pathol. 2017, 18, 477–488. [Google Scholar] [CrossRef]
- Moral, J.; Morgan, D.; Trapero, A.; Michailides, T.J. Ecology and epidemiology of diseases of nut crops and olives caused by Botryosphaeriaceae fungi in California and Spain. Plant Dis. 2019, 103, 1809–1827. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xu, C.; Wang, C.S.; Ju, L.L.; Zhang, R.; Biggs, A.R.; Tanaka, E.; Li, B.Z.; Sun, G.Y. Multiple locus genealogies and phenotypic characters reappraise the causal agents of apple ring rot in China. Fungal Divers. 2015, 71, 215–231. [Google Scholar] [CrossRef]
- Yan, J.Y.; Zhao, W.S.; Chen, Z.; Xing, Q.K.; Zhang, W.; Chethana, K.W.T.; Xue, M.F.; Xu, J.P.; Phillips, A.J.L.; Wang, Y.; et al. Comparative genome and transcriptome analyses reveal adaptations to opportunistic infections in woody plant degrading pathogens of Botryosphaeriaceae. DNA Res. 2017, 25, 87–102. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Slippers, B.; Crous, P.W.; Jami, F.; Groenewald, J.Z.; Wingfield, M.J. Diversity in the Botryosphaeriales: Looking back, looking forward. Fungal Biol. 2017, 121, 307–321. [Google Scholar] [CrossRef]
- Zhai, L.F.; Zhang, M.X.; Lv, G.; Chen, X.R.; Jia, N.N.; Hong, N.; Wang, G.P. Biological and molecular characterization of four Botryosphaeria species isolated from pear plants showing stem wart and stem canker in China. Plant Dis. 2014, 98, 716–726. [Google Scholar] [CrossRef] [Green Version]
- Hu, W.C.; Luo, H.; Yang, Y.K.; Wang, Q.; Hong, N.; Wang, G.P.; Wang, A.M.; Wang, L.P. Comprehensive analysis of full genome sequence and Bd-milRNA/target mRNAs to discover the mechanism of hypovirulence in Botryosphaeria dothidea strains on pear infection with BdCV1 and BdPV1. IMA Fungus 2019, 10, 3. [Google Scholar] [CrossRef] [Green Version]
- Wang, B.; Liang, X.F.; Gleason, M.L.; Zhang, R.; Sun, G.Y. Comparative genomics of Botryosphaeria dothidea and B. kuwatsukai, causal agents of apple ring rot, reveals both species expansion of pathogenicity-related genes and variations in virulence gene content during speciation. IMA Fungus 2018, 9, 243–257. [Google Scholar] [CrossRef] [Green Version]
- Morales-Cruz, A.; Amrine, K.C.H.; Blanco-Ulate, B.; Lawrence, D.P.; Travadon, R.; Rolshausen, P.E.; Baumgartner, K.; Cantu, D. Distinctive expansion of gene families associated with plant cell wall degradation, secondary metabolism, and nutrient uptake in the genomes of grapevine trunk pathogens. BMC Genom. 2015, 16, 469. [Google Scholar] [CrossRef] [Green Version]
- Lombard, V.; Ramulu, H.G.; Drula, E.; Coutinho, P.M.; Henrissat, B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014, 42, D490–D495. [Google Scholar] [CrossRef] [Green Version]
- Ospina-Giraldo, M.D.; Griffith, J.G.; Laird, E.W.; Mingora, C. The CAZyome of Phytophthora spp.: A comprehensive analysis of the gene complement coding for carbohydrate-active enzymes in species of the genus Phytophthora. BMC Genom. 2010, 11, 525. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lyu, X.L.; Shen, C.C.; Fu, Y.P.; Xie, J.T.; Jiang, D.H.; Li, G.Q.; Cheng, J.S. Comparative genomic and transcriptional analyses of the carbohydrate-active enzymes and secretomes of phytopathogenic fungi reveal their significant roles during infection and development. Sci. Rep. 2015, 5, 15565. [Google Scholar] [CrossRef] [PubMed]
- Yang, Y.K.; Yang, X.F.; Dong, Y.J.; Qiu, D.W. The Botrytis cinerea xylanase BcXyl1 modulates plant immunity. Front. Microbiol. 2018, 9, 2535. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhu, W.J.; 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] [PubMed] [Green Version]
- Zhang, L.; Yan, J.P.; Fu, Z.C.; Shi, W.J.; Ninkuu, V.; Li, G.Y.; Yang, X.F.; Zeng, H.M. 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]
- Thilini Chethana, K.W.; Peng, J.B.; Li, X.H.; Xing, Q.K.; Liu, M.; Zhang, W.; Hyde, K.D.; Zhao, W.S.; Yan, J.Y. 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]
- Yang, C.; Liu, R.; Pang, J.H.; Ren, B.; Zhou, H.B.; Wang, G.; Wang, E.T.; Liu, J. Poaceae-specific cell wall-derived oligosaccharides activate plant immunity via OsCERK1 during Magnaporthe oryzae infection in rice. Nat. Commun. 2021, 12, 2178. [Google Scholar] [CrossRef]
- Lai, M.W.; Liou, R.F. Two genes encoding GH10 xylanases are essential for the virulence of the oomycete plant pathogen Phytophthora parasitica. Curr. Genet. 2018, 64, 931–943. [Google Scholar] [CrossRef]
- Yu, Y.; Xiao, J.F.; Du, J.; Yang, Y.H.; Bi, C.W.; Qing, L. Disruption of the gene encoding endo-β-1, 4-xylanase affects the growth and virulence of Sclerotinia sclerotiorum. Front. Microbiol. 2016, 7, 1787. [Google Scholar] [CrossRef] [Green Version]
- Yu, C.L.; Li, T.; Shi, X.P.; Saleem, M.; Li, B.H.; Liang, W.X.; Wang, C.X. Deletion of endo-β-1,4-xylanase VmXyl1 impacts the virulence of Valsa mali in apple tree. Front. Plant Sci. 2018, 9, 663. [Google Scholar] [CrossRef] [Green Version]
- Yang, Y.K.; Zhang, Y.; Li, B.B.; Yang, X.F.; Dong, Y.J.; Qiu, D.W. A Verticillium dahliae pectate lyase induces plant immune responses and contributes to virulence. Front. Plant Sci. 2018, 9, 1271. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dong, B.Z.; Zhu, X.Q.; Fan, J.; Guo, L.Y. The cutinase Bdo_10846 play an important role in the virulence of Botryosphaeria dothidea and in inducing the wart symptom on apple plant. Int. J. Mol. Sci. 2021, 22, 1910. [Google Scholar] [CrossRef] [PubMed]
- Jones, J.D.G.; Dangl, J.L. The plant immune system. Nature 2006, 444, 323–329. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lu, Y.; Tsuda, K. Intimate association of PRR- and NLR-mediated signaling in plant immunity. Mol. Plant. Microbe Interact. 2021, 34, 3–14. [Google Scholar] [CrossRef] [PubMed]
- Zipfel, C.; Robatzek, S.; Navarro, L.; Oakeley, E.J.; Jones, J.D.G.; Felix, G.; Boller, T. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 2004, 428, 764–767. [Google Scholar] [CrossRef] [PubMed]
- Felix, G.; Duran, J.D.; Volko, S.; Boller, T. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 1999, 18, 265–276. [Google Scholar] [CrossRef]
- Zipfel, C.; Kunze, G.; Chinchilla, D.; Caniard, A.; Jones, J.D.G.; Boller, T.; Felix, G. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 2006, 125, 749–760. [Google Scholar] [CrossRef]
- Kunze, G.; Zipfel, C.; Robatzek, S.; Niehaus, K.; Boller, T.; Felix, G. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 2004, 16, 3496–3507. [Google Scholar] [CrossRef] [Green Version]
- Derevnina, L.; Dagdas, Y.F.; De la Concepcion, J.C.; Bialas, A.; Kellner, R.; Petre, B.; Domazakis, E.; Du, J.; Wu, C.H.; Lin, X.; et al. Nine things to know about elicitins. New Phytol. 2016, 212, 888–895. [Google Scholar] [CrossRef] [Green Version]
- Bar, M.; Sharfman, M.; Ron, M.; Avni, A. BAK1 is required for the attenuation of ethylene-inducing xylanase (Eix)-induced defense responses by the decoy receptor LeEix1. Plant J. 2010, 63, 791–800. [Google Scholar] [CrossRef]
- Ma, Z.C.; Song, T.Q.; Zhu, L.; Ye, W.W.; Wang, Y.; Shao, Y.Y.; Dong, S.M.; Zhang, Z.G.; Dou, D.L.; Zheng, X.B.; 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] [PubMed] [Green Version]
- 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] [PubMed] [Green Version]
- Chaparro-Garcia, A.; Wilkinson, R.C.; Gimenez-Ibanez, S.; Findlay, K.; Coffey, M.D.; Zipfel, C.; Rathjen, J.P.; Kamoun, S.; Schornack, S. The receptor-like kinase SERK3/BAK1 is required for basal resistance against the late blight pathogen Phytophthora infestans in Nicotiana benthamiana. PLoS ONE 2011, 6, e16608. [Google Scholar] [CrossRef]
- Zipfel, C. Early molecular events in PAMP-triggered immunity. Curr. Opin. Plant Biol. 2009, 12, 414–420. [Google Scholar] [CrossRef] [PubMed]
- Mengiste, T. Plant immunity to necrotrophs. Annu. Rev. Phytopathol. 2012, 50, 267–294. [Google Scholar] [CrossRef] [PubMed]
- van Doorn, W.G. Classes of programmed cell death in plants, compared to those in animals. J. Exp. Bot. 2011, 62, 4749–4761. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, C.J.; Wang, S.X.; Liang, Y.N.; Wen, S.H.; Dong, B.Z.; Ding, Z.; Guo, L.Y.; Zhu, X.Q. Candidate effectors from Botryosphaeria dothidea suppress plant immunity and contribute to virulence. Int. J. Mol. Sci. 2021, 22, 552. [Google Scholar] [CrossRef]
- Liu, N.; Lian, S.; Zhou, S.Y.; Wang, C.X.; Ren, W.C.; Li, B.H. Involvement of the autophagy-related gene BdATG8 in development and pathogenicity in Botryosphaeria dothidea. J. Integr. Agric. 2021. Available online: https://www.chinaagrisci.com/Jwk_zgnykxen/fileup/PDF/JIA-2021-1350.pdf (accessed on 10 December 2021).
- Xiao, J.L.; Zhang, S.T.; Chen, G. Mechanisms of lignin-degrading enzymes. Protein Pept. Lett. 2020, 27, 574–581. [Google Scholar] [CrossRef]
- Datta, R.; Kelkar, A.; Baraniya, D.; Molaei, A.; Moulick, A.; Meena, R.S.; Formanek, P. Enzymatic degradation of lignin in soil: A review. Sustainability 2017, 9, 1163. [Google Scholar] [CrossRef] [Green Version]
- Glenn, J.K.; Morgan, M.A.; Mayfield, M.B.; Kuwahara, M.; Gold, M.H. An extracellular H2O2-requiring enzyme preparation involved in lignin biodegradation by the white rot basidiomycete Phanerochaete chrysosporium. Biochem. Biophys. Res. Commun. 1983, 114, 1077–1083. [Google Scholar] [CrossRef]
- Coconi-Linares, N.; Magaña-Ortíz, D.; Guzmán-Ortiz, D.A.; Fernández, F.; Loske, A.M.; Gómez-Lim, M.A. High-yield production of manganese peroxidase, lignin peroxidase, and versatile peroxidase in Phanerochaete chrysosporium. Appl. Microbiol. Biotechnol. 2014, 98, 9283–9294. [Google Scholar] [CrossRef] [PubMed]
- Sadaqat, B.; Khatoon, N.; Malik, A.Y.; Jamal, A.; Farooq, U.; Ali, M.I.; He, H.; Liu, F.J.; Guo, H.G.; Urynowicz, M.; et al. Enzymatic decolorization of melanin by lignin peroxidase from Phanerochaete chrysosporium. Sci. Rep. 2020, 10, 20240. [Google Scholar] [CrossRef] [PubMed]
- Vandana, T.; Rao, R.G.; Kumar, S.A.; Swaraj, S.; Manpal, S. Enhancing production of lignin peroxidase from white rot fungi employing statistical optimization and evaluation of its potential in delignification of crop residues. Int. J. Curr. Microbiol. App. Sci. 2018, 7, 2599–2621. [Google Scholar] [CrossRef] [Green Version]
- Bholay, A.D.; Borkhataria, B.V.; Jadhav, P.U.; Palekar, K.S.; Dhalkari, M.V.; Nalawade, P.M. Bacterial lignin peroxidase: A tool for biobleaching and biodegradation of industrial effluents. Univers. J. Environ. Res. Technol. 2012, 2, 58–64. [Google Scholar]
- Lin, S.Y.; Okuda, S.; Ikeda, K.; Okuno, T.; Takano, Y. LAC2 encoding a secreted laccase is involved in appressorial melanization and conidial pigmentation in Colletotrichum orbiculare. Mol. Plant. Microbe Interact. 2012, 25, 1552–1561. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Y.; Dong, Z.Q.; Luo, Y.; Yang, E.; Xu, H.N.; Chagan, I.; Yan, J.P. The manganese peroxidase gene family of Trametes trogii: Gene identification and expression patterns using various metal ions under different culture conditions. Microorganisms 2021, 9, 2595. [Google Scholar] [CrossRef]
- Falade, A.O.; Nwodo, U.U.; Iweriebor, B.C.; Green, E.; Mabinya, L.V.; Okoh, A.I. Lignin peroxidase functionalities and prospective applications. MicrobiologyOpen 2017, 6, e00394. [Google Scholar] [CrossRef] [Green Version]
- Yin, W.X.; Wang, Y.F.; Chen, T.; Lin, Y.; Luo, C.X. Functional evaluation of the signal peptides of secreted proteins. Bio-Protocol 2018, 8, e2839. [Google Scholar] [CrossRef]
- Khang, C.H.; Berruyer, R.; Giraldo, M.C.; Kankanala, P.; Park, S.-Y.; Czymmek, K.; Kang, S.; Valent, B. Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 2010, 22, 1388–1403. [Google Scholar] [CrossRef] [Green Version]
- Kalderon, D.; Roberts, B.L.; Richardson, W.D.; Smith, A.E. A short amino acid sequence able to specify nuclear location. Cell 1984, 39, 499–509. [Google Scholar] [CrossRef]
- Zhao, G.P.; Zhu, Y.L.; Eno, C.O.; Liu, Y.L.; DeLeeuw, L.; Burlison, J.A.; Chaires, J.B.; Trent, J.O.; Li, C. Activation of the proapoptotic Bcl-2 protein Bax by a small molecule induces tumor cell apoptosis. Mol. Cell. Biol. 2014, 34, 1198–1207. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bloois, E.v.; Torres Pazmino, D.E.; Winter, R.T.; Fraaije, M.W. A robust and extracellular heme-containing peroxidase from Thermobifida fusca as prototype of a bacterial peroxidase superfamily. Appl. Microbiol. Biotechnol. 2010, 86, 1419–1430. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vlasova, I.I. Peroxidase activity of human hemoproteins: Keeping the fire under control. Molecules 2018, 23, 2561. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- González, M.; Brito, N.; González, C. The Botrytis cinerea elicitor protein BcIEB1 interacts with the tobacco PR5-family protein osmotin and protects the fungus against its antifungal activity. New Phytol. 2017, 215, 397–410. [Google Scholar] [CrossRef] [Green Version]
- Lyu, X.L.; Shen, C.C.; Fu, Y.P.; Xie, J.T.; Jiang, D.H.; Li, G.Q.; Cheng, J.S. A small secreted virulence-related protein is essential for the necrotrophic interactions of Sclerotinia sclerotiorum with its host plants. PLoS Pathog. 2016, 12, e1005435. [Google Scholar] [CrossRef]
- Yang, G.G.; Tang, L.G.; Gong, Y.D.; Xie, J.T.; Fu, Y.P.; Jiang, D.H.; Li, G.Q.; Collinge, D.B.; Chen, W.D.; Cheng, J.S. A cerato-platanin protein SsCP1 targets plant PR1 and contributes to virulence of Sclerotinia sclerotiorum. New Phytol. 2018, 217, 739–755. [Google Scholar] [CrossRef] [Green Version]
- Lo Presti, L.; Kahmann, R. How filamentous plant pathogen effectors are translocated to host cells. Curr. Opin. Plant Biol. 2017, 38, 19–24. [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]
- Li, H.Y.; Wang, H.N.; Jing, M.F.; Zhu, J.Y.; Guo, B.D.; Wang, Y.; Lin, Y.C.; Chen, H.; Kong, L.; Ma, Z.C.; et al. A Phytophthora effector recruits a host cytoplasmic transacetylase into nuclear speckles to enhance plant susceptibility. eLife 2018, 7, e40039. [Google Scholar] [CrossRef]
- Liu, X.Q.; Xie, J.T.; Fu, Y.P.; Jiang, D.H.; Chen, T.; Cheng, J.S. The subtilisin-like protease Bcser2 affects the sclerotial formation, conidiation and virulence of Botrytis cinerea. Int. J. Mol. Sci. 2020, 21, 603. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ruiz, G.B.; Pietro, A.D.; Roncero, M.I.G. Combined action of the major secreted exo- and endopolygalacturonases is required for full virulence of Fusarium oxysporum. Mol. Plant Pathol. 2016, 17, 339–353. [Google Scholar] [CrossRef] [PubMed]
- Jiang, C.; Hei, R.N.; Yang, Y.; Zhang, S.J.; Wang, Q.H.; Wang, W.; Zhang, Q.; Yan, M.; Zhu, G.R.; Huang, P.P.; et al. An orphan protein of Fusarium graminearum modulates host immunity by mediating proteasomal degradation of TaSnRK1α. Nat. Commun. 2020, 11, 4382. [Google Scholar] [CrossRef] [PubMed]
- Doehlemann, G.; Hemetsberger, C. Apoplastic immunity and its suppression by filamentous plant pathogens. New Phytol. 2013, 198, 1001–1016. [Google Scholar] [CrossRef] [PubMed]
- Mott, G.A.; Middleton, M.A.; Desveaux, D.; Guttman, D.S. Peptides and small molecules of the plant-pathogen apoplastic arena. Front. Plant Sci. 2014, 5, 677. [Google Scholar] [CrossRef] [Green Version]
- Franco-Orozco, B.; Berepiki, A.; Ruiz, O.; Gamble, L.; Griffe, L.L.; Wang, S.M.; Birch, P.R.J.; Kanyuka, K.; Avrova, A. A new proteinaceous pathogen-associated molecular pattern (PAMP) identified in Ascomycete fungi induces cell death in Solanaceae. New Phytol. 2017, 214, 1657–1672. [Google Scholar] [CrossRef] [Green Version]
- Li, Y.; Han, Y.J.; Qu, M.Y.; Chen, J.; Chen, X.F.; Geng, X.Q.; Wang, Z.H.; Chen, S.B. Apoplastic cell death-inducing proteins of filamentous plant pathogens: Roles in plant-pathogen interactions. Front. Genet. 2020, 11, 661. [Google Scholar] [CrossRef]
- Xiao, X.Q.; Xie, J.T.; Cheng, J.S.; Li, G.Q.; Yi, X.H.; Jiang, D.H.; Fu, Y.P. Novel secretory protein Ss-Caf1 of the plant-pathogenic fungus Sclerotinia sclerotiorum is required for host penetration and normal sclerotial development. Mol. Plant. Microbe Interact. 2014, 27, 40–55. [Google Scholar] [CrossRef] [Green Version]
- Nie, J.J.; Yin, Z.Y.; Li, Z.P.; Wu, Y.X.; Huang, L.L. A small cysteine-rich protein from two kingdoms of microbes is recognized as a novel pathogen-associated molecular pattern. New Phytol. 2019, 222, 995–1011. [Google Scholar] [CrossRef]
- Zhang, L.S.; Kars, I.; Essenstam, B.; Liebrand, T.W.H.; Wagemakers, L.; Elberse, J.; Tagkalaki, P.; Tjoitang, D.; van den Ackerveken, G.; van Kan, J.A.L. Fungal endopolygalacturonases are recognized as microbe-associated molecular patterns by the arabidopsis receptor-like protein responsiveness to botrytis polygalacturonases1. Plant Physiol. 2014, 164, 352–364. [Google Scholar] [CrossRef] [Green Version]
- Couto, D.; Zipfel, C. Regulation of pattern recognition receptor signalling in plants. Nat. Rev. Immunol. 2016, 16, 537–552. [Google Scholar] [CrossRef] [PubMed]
- Yu, X.; Feng, B.M.; He, P.; Shan, L.B. From chaos to harmony: Responses and signaling upon microbial pattern recognition. Annu. Rev. Phytopathol. 2017, 55, 109–137. [Google Scholar] [CrossRef] [PubMed]
- Dong, B.Z.; Guo, L.Y. An efficient gene disruption method for the woody plant pathogen Botryosphaeria dothidea. BMC Biotechnol. 2020, 20, 14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, L.; Sun, G.W.; Wang, H.K.; Wu, S.J.; Lin, F.C.; Liu, H.X. Protoplast preparation and gfp transformation of Botryosphaeria dothidea. Sci. Silvae Sin. 2014, 50, 131–137. [Google Scholar]
- Larkin, M.A.; Blackshields, G.; Brown, N.P.; Chenna, R.; McGettigan, P.A.; McWilliam, H.; Valentin, F.; Wallace, I.M.; Wilm, A.; Lopez, R.; et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23, 2947–2948. [Google Scholar] [CrossRef] [Green Version]
- Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 2016, 33, 1870–1874. [Google Scholar] [CrossRef] [Green Version]
- Wang, L.H.; Luo, H.; Hu, W.C.; Yang, Y.K.; Hong, N.; Wang, G.P.; Wang, A.M.; Wang, L.P. De novo transcriptomic assembly and mRNA expression patterns of Botryosphaeria dothidea infection with mycoviruses chrysovirus 1 (BdCV1) and partitivirus 1 (BdPV1). Virol. J. 2018, 15, 126. [Google Scholar] [CrossRef]
- Liu, J.; Zhang, X.J.; Zhang, F.P.; Hong, N.; Wang, G.P.; Wang, A.M.; Wang, L.P. Identification and characterization of microRNAs from in vitro-grown pear shoots infected with Apple stem grooving virus in response to high temperature using small RNA sequencing. BMC Genom. 2015, 16, 945. [Google Scholar] [CrossRef] [Green Version]
- Gui, Y.J.; Chen, J.Y.; Zhang, D.D.; Li, N.Y.; Li, T.G.; Zhang, W.Q.; Wang, X.Y.; 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] [Green Version]
- 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]
- Oh, S.K.; Young, C.; Lee, M.; Oliva, R.; Bozkurt, T.O.; Cano, L.M.; Win, J.; Bos, J.I.B.; Liu, H.Y.; van Damme, M.; et al. In planta expression screens of Phytophthora infestans RXLR effectors reveal diverse phenotypes, including activation of the Solanum bulbocastanum disease resistance protein Rpi-blb2. Plant Cell 2009, 21, 2928–2947. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dou, D.L.; Kale, S.D.; Wang, X.; Jiang, R.H.Y.; Bruce, N.A.; Arredondo, F.D.; Zhang, X.M.; Tyler, B.M. RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. Plant Cell 2008, 20, 1930–1947. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martin, K.; Kopperud, K.; Chakrabarty, R.; Banerjee, R.; Brooks, R.; Goodin, M.M. Transient expression in Nicotiana benthamiana fluorescent marker lines provides enhanced definition of protein localization, movement and interactions in planta. Plant J. 2009, 59, 150–162. [Google Scholar] [CrossRef] [PubMed]
- Piisilä, M.; Keceli, M.A.; Brader, G.; Jakobson, L.; Jõesaar, I.; Sipari, N.; Kollist, H.; Palva, E.T.; Kariola, T. The F-box protein MAX2 contributes to resistance to bacterial phytopathogens in Arabidopsis thaliana. BMC Plant Biol. 2015, 15, 53. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schenk, S.T.; Hernández-Reyes, C.; Samans, B.; Stein, E.; Neumann, C.; Schikora, M.; Reichelt, M.; Mithöfer, A.; Becker, A.; Kogel, K.-H.; et al. N-Acyl-Homoserine lactone primes plants for cell wall reinforcement and induces resistance to bacterial pathogens via the salicylic acid/oxylipin pathway. Plant Cell 2014, 26, 2708–2723. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, Y.M.; Wu, J.N.; Kim, S.G.; Tsuda, K.; Gupta, R.; Park, S.-Y.; Kim, S.T.; Kang, K.Y. Magnaporthe oryzae-secreted protein MSP1 induces cell death and elicits defense responses in rice. Mol. Plant. Microbe Interact. 2016, 29, 299–312. [Google Scholar] [CrossRef] [Green Version]
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Xiao, F.; Xu, W.; Hong, N.; Wang, L.; Zhang, Y.; Wang, G. A Secreted Lignin Peroxidase Required for Fungal Growth and Virulence and Related to Plant Immune Response. Int. J. Mol. Sci. 2022, 23, 6066. https://doi.org/10.3390/ijms23116066
Xiao F, Xu W, Hong N, Wang L, Zhang Y, Wang G. A Secreted Lignin Peroxidase Required for Fungal Growth and Virulence and Related to Plant Immune Response. International Journal of Molecular Sciences. 2022; 23(11):6066. https://doi.org/10.3390/ijms23116066
Chicago/Turabian StyleXiao, Feng, Wenxing Xu, Ni Hong, Liping Wang, Yongle Zhang, and Guoping Wang. 2022. "A Secreted Lignin Peroxidase Required for Fungal Growth and Virulence and Related to Plant Immune Response" International Journal of Molecular Sciences 23, no. 11: 6066. https://doi.org/10.3390/ijms23116066