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Research Paper

Overexpression of chitinase PbChia1 from Plasmodiophora brassicae improves broad-spectrum disease resistance of Arabidopsis

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Article: 2233147 | Received 13 Nov 2022, Accepted 17 Apr 2023, Published online: 11 Jul 2023

References

  • Dixon, GR. The occurrence and economic impact of Plasmodiophora Brassicae and clubroot disease. J. Plant Growth Regul. 2009;28(3):194–202.
  • Burki F, Kudryavtsev A, Matz MV, et al. Evolution of Rhizaria: new insights from phylogenomic analysis of uncultivated protists. BMC Evol Biol. 2010;10(1):377. doi: 10.1186/1471-2148-10-377
  • Hwang SF, Strelkov SE, Feng J, et al. Plasmodiophora brassicae: a review of an emerging pathogen of the Canadian canola (Brassica napus) crop. Mol Plant Pathol. 2012;13(2):105–18. doi: 10.1111/j.1364-3703.2011.00729.x
  • Kamoun S. Molecular genetics of pathogenic oomycetes. Eukaryotic Cell. 2003;2:191–199. doi: 10.1128/EC.2.2.191-199.2003
  • Michielse CB, Hooykaas PJ, van den Hondel CA, et al. Agrobacterium-mediated transformation as a tool for functional genomics in fungi. Curr Genet. 2005;48:1–17. doi: 10.1007/s00294-005-0578-0
  • Nakayashiki H, Hanada S, Quoc NB, et al. RNA silencing as a tool for exploring gene function in ascomycete fungi. Fungal Genet Biol. 2005;42(4):275–283. doi: 10.1016/j.fgb.2005.01.002
  • Rolfe SA, Strelkov SE, Links MG, et al. The compact genome of the plant pathogen Plasmodiophora brassicae is adapted to intracellular interactions with host Brassica spp. BMC Genomics. 2016;17(1):272. doi: 10.1186/s12864-016-2597-2
  • Schwelm A, Fogelqvist J, Knaust A, et al. The Plasmodiophora brassicae genome reveals insights in its life cycle and ancestry of chitin synthases. Sci Rep. 2015;5(1):11153. doi: 10.1038/srep11153
  • Chen T, Bi K, Zhao Y, et al. MAPKK inhibitor U0126 inhibits Plasmodiophora brassicae development. Phytopathology. 2018;108:711–720. doi: 10.1094/PHYTO-07-17-0240-R
  • Schwelm A, Dixelius C, Ludwig-Müller J. New kid on the block – the clubroot pathogen genome moves the plasmodiophorids into the genomic era. Eur J Plant Pathol. 2016;145(3):531–542. doi: 10.1007/s10658-015-0839-9
  • Singh K, Tzelepis G, Zouhar M, et al. The immunophilin repertoire of Plasmodiophora brassicae and functional analysis of PbCYP3 cyclophilin. Mol Genet Genomics. 2018;293(2):381–390. doi: 10.1007/s00438-017-1395-0
  • Bulman S, Richter F, Marschollek S, et al. Arabidopsis thaliana expressing PbBSMT, a gene encoding a SABATH-type methyltransferase from the plant pathogenic protist Plasmodiophora brassicae, show leaf chlorosis and altered host susceptibility. Plant Biol. 2019;21(S1):120–130. doi: 10.1111/plb.12728
  • Djavaheri M, Ma L, Klessig DF, et al. Mimicking the host regulation of salicylic acid: a virulence strategy by the clubroot pathogen Plasmodiophora brassicae. Mol Genet Genomics. 2019;32(3):296–305. doi: 10.1094/MPMI-07-18-0192-R
  • Pérez-López E, Hossain MM, Tu J, et al. Transcriptome analysis identifies Plasmodiophora brassicae secondary infection effector candidates. J Eukaryot Microbiol. 2020;67:337–351. doi: 10.1111/jeu.12784
  • Pérez-López E, Hossain MM, Wei Y, et al. A clubroot pathogen effector targets cruciferous cysteine proteases to suppress plant immunity. Virulence. 2021;12(1):2327–2340. doi: 10.1080/21505594.2021.1968684
  • Chen W, Li Y, Yan R, et al. SnRK1.1-mediated resistance of Arabidopsis thaliana to clubroot disease is inhibited by the novel Plasmodiophora brassicae effector PBZF1. Mol Plant Pathol. 2021;22(9):1057–1069. doi: 10.1111/mpp.13095
  • Merzendorfer H. The cellular basis of chitin synthesis in fungi and insects: common principles and differences. Eur J Cell Biol. 2011;90(9):759–769. doi: 10.1016/j.ejcb.2011.04.014
  • Moxham SE, Buczacki ST. Chemical composition of the resting spore wall of Plasmodiophora brassicae. Trans Br Mycol Soc. 1983;80(2):297–304. doi: 10.1016/S0007-1536(83)80013-8
  • Kombrink A, Sánchez-Vallet A, Thomma BPHJ. The role of chitin detection in plant–pathogen interactions. Microbes Infect. 2011;13:1168–1176. doi: 10.1016/j.micinf.2011.07.010
  • Pentecost JWG. Potential application of chitin signaling in engineering broad-spectrum disease resistance to fungal and bacterial pathogens in plants. Adv Crop Sci Tech. 2013;1:e103.
  • Kishimoto K, Kouzai Y, Kaku H, et al. Perception of the chitin oligosaccharides contributes to disease resistance to blast fungus Magnaporthe oryzae in rice. Plant J. 2010;64(2):343–354. doi: 10.1111/j.1365-313X.2010.04328.x
  • Wan J, Tanaka K, Zhang XC, et al. Lyk4, a lysin motif receptor-like kinase, is important for chitin signaling and plant innate immunity in Arabidopsis. Plant Physiol. 2012;160(1):396–406. doi: 10.1104/pp.112.201699
  • Jin RD, Han T, Kim Y, et al. Suppression of clubroot formation in Chinese cabbage by the chitin compost and broth. J Biol Chem. 2006;49:171–175.
  • Muirhead K, Pérez-López E. Plasmodiophora brassicae CBM18 proteins bind chitin and suppress chitin-triggered immunity. PhytoFrontiers. 2022;2:21–29. doi: 10.1094/PHYTOFR-04-21-0032-R
  • Bravo JM, Campo S, Murillo I, et al. Fungus- and wound-induced accumulation of mRNA containing a class II chitinase of the pathogenesis-related protein 4 (PR-4) family of maize. Plant Mol Biol. 2003;52(4):745–759. doi: 10.1023/A:1025016416951
  • Wang LY, Wang YS, Zhang JP, et al. Molecular cloning of class III chitinase gene from Avicennia marina and its expression analysis in response to cadmium and lead stress. Ecotoxicology. 2015;24(7–8):1697–1704. doi: 10.1007/s10646-015-1501-1
  • Li P, Zhang Y, Wu X, et al. Drought stress impact on leaf proteome variations of faba bean (vicia faba L.) in the Qinghai-Tibet Plateau of China. Biotech. 2018;8:110. doi: 10.1007/s13205-018-1088-3
  • Roby D, Toppan A, Esquerré-Tugayé MT. Systemic induction of chitinase activity and resistance in melon plants upon fungal infection or elicitor treatment. Physiol Mol Plant P. 1988;33:409–417. doi: 10.1016/0885-5765(88)90007-0
  • Ntui VO, Azadi P, Thirukkumaran G, et al. Increased resistance to fusarium wilt in transgenic tobacco lines co-expressing chitinase and wasabi defensin genes. Plant Pathol. 2011;60(2):221–231. doi: 10.1111/j.1365-3059.2010.02352.x
  • Jabeen N, Chaudhary Z, Gulfraz M, et al. Expression of rice chitinase gene in genetically engineered tomato confers enhanced resistance to fusarium wilt and early blight. Plant Pathol. 2015;31(3):252–258. doi: 10.5423/PPJ.OA.03.2015.0026
  • Nookaraju A, Agrawal DC. Enhanced tolerance of transgenic grapevines expressing chitinase and β-1,3-glucanase genes to downy mildew. Plant Cell Tissue Organ Cult. 2012;111(1):15–28. doi: 10.1007/s11240-012-0166-1
  • Marchant R, Davey MR, Lucas JA, et al. Expression of a chitinase transgene in rose (Rosa hybrida L.) reduces development of blackspot disease (Diplocarpon rosae Wolf). Mol Breed. 1998;4:187–194. doi: 10.1023/A:1009642707505
  • Chen J, Piao Y, Liu Y, et al. Genome-wide identification and expression analysis of chitinase gene family in Brassica rapa reveals its role in clubroot resistance. Plant Sci. 2018;270:257–267. doi: 10.1016/j.plantsci.2018.02.017
  • Abeles FB, Bosshart RP, Forrence LE, et al. Preparation and purification of glucanase and chitinase from bean leaves. Plant Physiol. 1971;47(1):129–134. doi: 10.1104/pp.47.1.129
  • Staehelin C, Granado J, Müller J, et al. Perception of Rhizobium nodulation factors by tomato cells and inactivation by root chitinases. P Natl Acad Sci USA. 1994;91(6):2196–2200. doi: 10.1073/pnas.91.6.2196
  • Khan A, Nasir IA, Tabassum B, et al. Expression studies of chitinase gene in transgenic potato against Alternaria solani. Plant Cell Tissue Organ Cult. 2017;128(3):563–576. doi: 10.1007/s11240-016-1134-y
  • Zhao X, Situ G, He K, et al. Functional analysis of eight chitinase genes in rice stem borer and their potential application in pest control. Insect Mol Biol. 2018;27:835–846. doi: 10.1111/imb.12525
  • Fan XJ, Mi YX, Ren H, et al. Cloning and functional expression of a chitinase cDNA from the apple leaf miner moth Lithocolletis ringoniella. Biochem Moscow. 2015;80(2):242–250. doi: 10.1134/S000629791502011X
  • Asano T, Kageyama K, Hyakumachi M. Surface disinfestation of resting spores of Plasmodiophora brassicae used to infect hairy roots of Brassica spp. Phytopathology. 1999;89:314–319. doi: 10.1094/PHYTO.1999.89.4.314
  • Siemens J, Nagel M, Ludwig-Muller J, et al. The interaction of Plasmodiophora brassicae and Arabidopsis thaliana: parameters for disease quantification and screening of mutant lines. J Phytopathol. 2002;150(11–12):592–605. doi: 10.1046/j.1439-0434.2002.00818.x
  • Zhao Y, Chen X, Cheng J, et al. Application of Trichoderma Hz36 and Hk37 as biocontrol agents against clubroot caused by Plasmodiophora brassicae. J Fungi. 2022;28:777. doi: 10.3390/jof8080777
  • Yang C, Yu Y, Huang J, et al. Binding of the Magnaporthe oryzae Chitinase MoChia1 by a Rice Tetratricopeptide Repeat Protein Allows Free Chitin to Trigger Immune Responses. Plant Cell. 2019;31(1):172–128. doi: 10.1105/tpc.18.00382
  • Dhanabalan V, Xavier KAM, Eppen S, et al. Characterization of chitin extracted from enzymatically deproteinized Acetes shell residue with varying degree of hydrolysis. Carbohydr Polym. 2021;253:117203. doi: 10.1016/j.carbpol.2020.117203
  • Bi K, He Z, Gao Z, et al. Integrated omics study of lipid droplets from Plasmodiophora brassicae. Sci Rep. 2016;6(1):36965. doi: 10.1038/srep36965
  • Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4(4):406. doi: 10.1093/oxfordjournals.molbev.a040454
  • Sandhya C, Adapa LK, Nampoothiri KM, et al. Extracellular chitinase production by Trichoderma harzianum in submerged fermentation. J Basic Microbiol. 2004;44(1):49–58. doi: 10.1002/jobm.200310284
  • Zhang FL, Ruan XL, Wang X, et al. Overexpression of a chitinase gene from Trichoderma asperellum increases disease resistance in transgenic soybean. Appl Biochem Biotechnol. 2016;180(8):1542–1558. doi: 10.1007/s12010-016-2186-5
  • Liu B, Li JF, Ao Y, et al. Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell. 2012;24:3406–3419. doi: 10.1105/tpc.112.102475
  • Jacobs KA, Collins-Racie LA, Colbert M, et al. A genetic selection for isolating cDnas encoding secreted proteins. Gene. 1997;198(1–2):289–296. doi: 10.1016/S0378-1119(97)00330-2
  • Gietz RD, Schiestl RH. High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc. 2007;2(1):31–34. doi: 10.1038/nprot.2007.13
  • Lyda TA, Joshi MB, Andersen JF, et al. A unique, highly conserved secretory invertase is differentially expressed by promastigote developmental forms of all species of the human pathogen, Leishmania. Mol Cell Biochem. 2015;404(1–2):53–77. doi: 10.1007/s11010-015-2366-6
  • Chen T, Bi K, He Z, et al. Arabidopsis mutant bik1 exhibits strong resistance to Plasmodiophora brassicae. Front Physiol. 2016;7:402. doi: 10.3389/fphys.2016.00402
  • Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16(6):735–743. doi: 10.1046/j.1365-313x.1998.00343.x
  • Liesche J, Marek M, Günther-Pomorski T. Cell wall staining with Trypan blue enables quantitative analysis of morphological changes in yeast cells. Front Microbiol. 2015;6:107. doi: 10.3389/fmicb.2015.00107
  • Qi P, Huang M, Hu X, et al. A Ralstonia solanacearum effector targets TGA transcription factors to subvert salicylic acid signaling. Plant Cell. 2022;34(5):1666–1683. doi: 10.1093/plcell/koac015
  • Jang MK, Kong BG, Jeong YI, et al. Physicochemical characterization of α-chitin, β-chitin, and γ-chitin separated from natural resources. J Polym Sci. 2004;42:3423–3432. doi: 10.1002/pola.20176
  • Sun Y, Li L, Macho AP, et al. Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science. 2013;342(6158):624–628. doi: 10.1126/science.1243825
  • Wallenhammar AC. Prevalence of Plasmodiophora brassicae in a spring oilseed rape growing area in central Sweden and factors influencing soil infestation levels. Plant Pathol. 1996;45(4):710–719. doi: 10.1046/j.1365-3059.1996.d01-173.x
  • Hasan J, Megha S, Rahman H. Clubroot in Brassica: recent advances in genomics, breeding, and disease management. Genome. 2021;64(8):735–760. doi: 10.1139/gen-2020-0089
  • Holtz MD, Hwang SF, Strelkov SE. Genotyping of Plasmodiophora brassicae reveals the presence of distinct populations. BMC Genomics. 2018;19(1):254. doi: 10.1186/s12864-018-4658-1
  • Sedaghatkish A, Gossen BD, Yu F, et al. Whole-genome DNA similarity and population structure of Plasmodiophora brassicae strains from Canada. BMC Genomics. 2019;20(1):744. doi: 10.1186/s12864-019-6118-y
  • Strelkov SE, Hwang SF, Manolii VP, et al. Virulence and pathotype classification of Plasmodiophora brassicae populations collected from clubroot resistant canola (Brassica napus) in Canada. Can J Plant Pathol. 2018;40:284–298. doi: 10.1080/07060661.2018.1459851
  • Hirani AH, Gao F, Liu J, et al. Combinations of independent dominant loci conferring clubroot resistance in all four turnip accessions (Brassica rapa) from the European clubroot differential set. Front Plant Sci. 2018;9:1628. doi: 10.3389/fpls.2018.01628
  • Strelkov SE, Hwang SF, Manolii VP, et al. Emergence of new virulence phenotypes of Plasmodiophora brassicae on canola (Brassica napus) in Alberta, Canada. Eur J Plant Pathol. 2016;145(3):517–529. doi: 10.1007/s10658-016-0888-8
  • Cao T, Manolii VP, Zhou Q, et al. Effect of canola (Brassica napus) cultivar rotation on Plasmodiophora brassicae pathotype composition. Can J Plant Sci. 2020;100(2):218–225. doi: 10.1139/cjps-2019-0126
  • Legrand M, Kauffmann S, Geoffroy P, et al. Biological function of pathogenesis-related proteins: Four tobacco pathogenesis-related proteins are chitinases. PNAS. 1987;84(19):6750–6754. doi: 10.1073/pnas.84.19.6750
  • Dana M, Pintor-Toro T, Cubero B. Transgenic tobacco plants overexpressing chitinases of fungal origin show enhanced resistance to biotic and abiotic stress agents. Plant Physiol. 2006;142:722–730. doi: 10.1104/pp.106.086140
  • Cletus J, Balasubramanian V, Vashisht D, et al. Transgenic expression of plant chitinases to enhance disease resistance. Biotechnol Lett. 2013;35(11):1719–1732. doi: 10.1007/s10529-013-1269-4
  • Yang X, Yang J, Li H, et al. Overexpression of the chitinase gene CmCH1 from Coniothyrium minitans renders enhanced resistance to Sclerotinia sclerotiorum in soybean. Transgenic Res. 2020;29(2):187–198. doi: 10.1007/s11248-020-00190-2
  • Cao Y, Liang Y, Tanaka K, et al. The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. Elife. 2014;3:e03766. doi: 10.7554/eLife.03766
  • Sánchez-Vallet A, Mesters JR, Thomma BPHJ. The battle for chitin recognition in plant-microbe interactions. FEMS Microbiol Rev. 2015;39:171–183. doi: 10.1093/femsre/fuu003
  • Mentlak TA, Kombrink A, Shinya T, et al. Effector-mediated suppression of chitin-triggered immunity by magnaporthe oryzae is necessary for rice blast disease. Plant Cell. 2012;24(1):322–335. doi: 10.1105/tpc.111.092957
  • de Jonge R, Peter van Esse, van Esse HP A, et al. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science. 2010;329:953–955. doi: 10.1126/science.1190859
  • Marshall R, Kombrink A, Motteram J, et al. Analysis of two in planta expressed LysM effector homologs from the fungus Mycosphaerella graminicola reveals novel functional properties and varying contributions to virulence on wheat. Plant Physiol. 2011;156:756–769. doi: 10.1104/pp.111.176347