Abstract
Main conclusion
Carbohydrates are hydrolyzed by a family of carbohydrate-active enzymes (CAZymes) called glycosidases or glycosyl hydrolases. Here, we have summarized the roles of various plant defense glycosidases that possess different substrate specificities. We have also highlighted the open questions in this research field.
Abstract
Glycosidases or glycosyl hydrolases (GHs) are a family of carbohydrate-active enzymes (CAZymes) that hydrolyze glycosidic bonds in carbohydrates and glycoconjugates. Compared to those of all other sequenced organisms, plant genomes contain a remarkable diversity of glycosidases. Plant glycosidases exhibit activities on various substrates and have been shown to play important roles during pathogen infections. Plant glycosidases from different GH families have been shown to act upon pathogen components, host cell walls, host apoplastic sugars, host secondary metabolites, and host N-glycans to mediate immunity against invading pathogens. We could classify the activities of these plant defense GHs under eleven different mechanisms through which they operate during pathogen infections. Here, we have provided comprehensive information on the catalytic activities, GH family classification, subcellular localization, domain structure, functional roles, and microbial strategies to regulate the activities of defense-related plant GHs. We have also emphasized the research gaps and potential investigations needed to advance this topic of research.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data in the review article are available from the corresponding author upon request.
References
Ahn YO, Shimizu B, Sakata K et al (2010) Scopolin-hydrolyzing β-glucosidases in roots of Arabidopsis. Plant Cell Physiol 51:132–143. https://doi.org/10.1093/pcp/pcp174
Albersheim P, Valent BS (1974) Host-pathogen interactions: VII. Plant pathogens secrete proteins which inhibit enzymes of the host capable of attacking the pathogen. Plant Physiol 53:684–687. https://doi.org/10.1104/pp.53.5.684
Ali M, Li Q-H, Zou T et al (2020) Chitinase gene positively regulates hypersensitive and defense responses of pepper to Colletotrichum acutatum infection. Int J Mol Sci 21:E6624. https://doi.org/10.3390/ijms21186624
Anderson JP, Badruzsaufari E, Schenk PM et al (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479. https://doi.org/10.1105/tpc.104.025833
Andersson MX, Nilsson AK, Johansson ON et al (2015) Involvement of the electrophilic isothiocyanate sulforaphane in Arabidopsis local defense responses. Plant Physiol 167:251–261. https://doi.org/10.1104/pp.114.251892
Bakhat N, Vielba-Fernández A, Padilla-Roji I et al (2023) Suppression of chitin-triggered immunity by plant fungal pathogens: a case study of the cucurbit powdery mildew fungus Podosphaera xanthii. J Fungi 9:771. https://doi.org/10.3390/jof9070771
Bauer K, Nayem S, Lehmann M et al (2023) β-d-XYLOSIDASE 4 modulates systemic immune signaling in Arabidopsis thaliana. Front Plant Sci 13:1096800. https://doi.org/10.3389/fpls.2022.1096800
Bednarek P, Pislewska-Bednarek M, Svatos A et al (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323:101–106. https://doi.org/10.1126/science.1163732
Beers EP, Duke SH, Henson CA (1990) Partial characterization and subcellular localization of three alpha-glucosidase isoforms in pea (Pisum sativum L.) seedlings. Plant Physiol 94:738–744. https://doi.org/10.1104/pp.94.2.738
Berger S, Sinha AK, Roitsch T (2007) Plant physiology meets phytopathology: plant primary metabolism and plant–pathogen interactions. J Exp Bot 58:4019–4026. https://doi.org/10.1093/jxb/erm298
Boller T, Gehri A, Mauch F, Vögeli U (1983) Chitinase in bean leaves: induction by ethylene, purification, properties, and possible function. Planta 157:22–31. https://doi.org/10.1007/BF00394536
Breitenbach HH, Wenig M, Wittek F et al (2014) Contrasting roles of the apoplastic aspartyl protease APOPLASTIC, ENHANCED DISEASE SUSCEPTIBILITY1-DEPENDENT1 and LEGUME LECTIN-LIKE PROTEIN1 in Arabidopsis systemic acquired resistance. Plant Physiol 165:791–809. https://doi.org/10.1104/pp.114.239665
Brito N, Espino JJ, González C (2006) The endo-β-1,4-xylanase xyn11a is required for virulence in Botrytis cinerea. Mol Plant Microbe Interact 19:25–32. https://doi.org/10.1094/MPMI-19-0025
Brunner F, Stintzi A, Fritig B, Legrand M (1998) Substrate specificities of tobacco chitinases. Plant J 14:225–234. https://doi.org/10.1046/j.1365-313X.1998.00112.x
Brutus A, Reca IB, Herga S et al (2005) A family 11 xylanase from the pathogen Botrytis cinerea is inhibited by plant endoxylanase inhibitors XIP-I and TAXI-I. Biochem Biophys Res Commun 337:160–166. https://doi.org/10.1016/j.bbrc.2005.09.030
Bueno TV, Fontes PP, Abe VY et al (2022) A Phakopsora pachyrhizi effector suppresses PAMP-triggered immunity and interacts with a soybean glucan endo-1,3-β-glucosidase to promote virulence. Mol Plant Microbe Interact 35:779–790. https://doi.org/10.1094/MPMI-12-21-0301-R
Burn JE, Hurley UA, Birch RJ et al (2002) The cellulose-deficient Arabidopsis mutant rsw3 is defective in a gene encoding a putative glucosidase II, an enzyme processing N-glycans during ER quality control. Plant J 32:949–960. https://doi.org/10.1046/j.1365-313X.2002.01483.x
Buscaill P, Chandrasekar B, Sanguankiattichai N et al (2019) Glycosidase and glycan polymorphism control hydrolytic release of immunogenic flagellin peptides. Science 364:eaav0748. https://doi.org/10.1126/science.aav0748
Buscaill P, Sanguankiattichai N, Lee YJ et al (2021) Agromonas: a rapid disease assay for Pseudomonas syringae growth in agroinfiltrated leaves. Plant J 105:831–840. https://doi.org/10.1111/tpj.15056
Cantu D, Vicente AR, Greve LC et al (2008) The intersection between cell wall disassembly, ripening, and fruit susceptibility to Botrytis cinerea. Proc Natl Acad Sci 105:859–864. https://doi.org/10.1073/pnas.0709813105
Cantu D, Greve LC, Labavitch JM, Powell ALT (2009) Characterization of the cell wall of the ubiquitous plant pathogen Botrytis cinerea. Mycol Res 113:1396–1403. https://doi.org/10.1016/j.mycres.2009.09.006
Cao Y, Liang Y, Tanaka K et al (2014) The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. Elife 3:e03766. https://doi.org/10.7554/eLife.03766
Cao Y, Zhang Y, Chen Y et al (2021) OsPG1 encodes a polygalacturonase that determines cell wall architecture and affects resistance to bacterial blight pathogen in rice. Rice 14:36. https://doi.org/10.1186/s12284-021-00478-9
Carey AT, Smith DL, Harrison E et al (2001) Down-regulation of a ripening-related beta-galactosidase gene (TBG1) in transgenic tomato fruits. J Exp Bot 52:663–668. https://doi.org/10.1093/jexbot/52.357.663
Chandrasekar B, van der Hoorn RAL (2016) Beta galactosidases in Arabidopsis and tomato—a mini review. Biochem Soc Trans 44:150–158. https://doi.org/10.1042/BST20150217
Chandrasekar B, Colby T, Emran Khan Emon A et al (2014) Broad-range glycosidase activity profiling. Mol Cell Proteomics 13:2787–2800. https://doi.org/10.1074/mcp.O114.041616
Chandrasekar B, Hong TN, van der Hoorn RAL (2017) Inhibitor discovery by convolution ABPP. Methods Mol Biol 1491:47–56. https://doi.org/10.1007/978-1-4939-6439-0_4
Chandrasekar B, Wanke A, Wawra S et al (2022) Fungi hijack a ubiquitous plant apoplastic endoglucanase to release a ROS scavenging β-glucan decasaccharide to subvert immune responses. Plant Cell 34:2765–2784. https://doi.org/10.1093/plcell/koac114
Cheong JJ, Alba R, Cote F et al (1993) Solubilization of functional plasma membrane-localized hepta-[beta]-glucoside elicitor-binding proteins from soybean. Plant Physiol 103:1173–1182. https://doi.org/10.1104/pp.103.4.1173
Chuenchor W, Pengthaisong S, Robinson RC et al (2008) Structural insights into rice BGlu1 beta-glucosidase oligosaccharide hydrolysis and transglycosylation. J Mol Biol 377:1200–1215. https://doi.org/10.1016/j.jmb.2008.01.076
Clay NK, Adio AM, Denoux C et al (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323:95–101. https://doi.org/10.1126/science.1164627
Cooper W, Bouzayen M, Hamilton A et al (1998) Use of transgenic plants to study the role of ethylene and polygalacturonase during infection of tomato fruit by Colletotrichum gloeosporioides. Plant Pathol 47:308–316. https://doi.org/10.1046/j.1365-3059.1998.00228.x
Cosgrove DJ (2015) Plant expansins: diversity and interactions with plant cell walls. Curr Opin Plant Biol 25:162–172. https://doi.org/10.1016/j.pbi.2015.05.014
Coutinho PM, Stam M, Blanc E, Henrissat B (2003) Why are there so many carbohydrate-active enzyme-related genes in plants? Trends Plant Sci 8:563–565. https://doi.org/10.1016/j.tplants.2003.10.002
Davies G, Henrissat B (1995) Structures and mechanisms of glycosyl hydrolases. Structure 3:853–859. https://doi.org/10.1016/S0969-2126(01)00220-9
de Jonge R, Peter van Esse H, Kombrink A et al (2010) Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953–955. https://doi.org/10.1126/science.1190859
de Oliveira NF, Santos GRC, Xisto MIDS et al (2019) β-1,6-linked galactofuranose- rich peptidogalactomannan of Fusarium oxysporum is important in the activation of macrophage mechanisms and as a potential diagnostic antigen. Med Mycol 57:234–245. https://doi.org/10.1093/mmy/myx167
Dean GH, Zheng H, Tewari J et al (2007) The Arabidopsis MUM2 gene encodes a beta-galactosidase required for the production of seed coat mucilage with correct hydration properties. Plant Cell 19:4007–4021. https://doi.org/10.1105/tpc.107.050609
den Ende WV (2018) Novel fructan exohydrolase: unique properties and applications for human health. J Exp Bot 69:4227. https://doi.org/10.1093/jxb/ery268
Drula E, Garron M-L, Dogan S et al (2022) The carbohydrate-active enzyme database: functions and literature. Nucleic Acids Res 50:D571–D577. https://doi.org/10.1093/nar/gkab1045
Essmann J, Schmitz-Thom I, Schön H et al (2008) RNA interference-mediated repression of cell wall invertase impairs defense in source leaves of tobacco. Plant Physiol 147:1288–1299. https://doi.org/10.1104/pp.108.121418
Felix G, Regenass M, Boller T (1993) Specific perception of subnanomolar concentrations of chitin fragments by tomato cells: induction of extracellular alkalinization, changes in protein phosphorylation, and establishment of a refractory state. Plant J 4:307–316. https://doi.org/10.1046/j.1365-313X.1993.04020307.x
Finiti I, Leyva MO, López-Cruz J et al (2013) Functional analysis of endo-1,4-β-glucanases in response to Botrytis cinerea and Pseudomonas syringae reveals their involvement in plant–pathogen interactions. Plant Biol 15:819–831. https://doi.org/10.1111/j.1438-8677.2012.00701.x
Fiorin GL, Sanchéz-Vallet A, Thomazella DPT et al (2018) Suppression of plant immunity by fungal chitinase-like effectors. Curr Biol 28:3023-3030.e5. https://doi.org/10.1016/j.cub.2018.07.055
Fliegmann J, Mithofer A, Wanner G, Ebel J (2004) An ancient enzyme domain hidden in the putative beta-glucan elicitor receptor of soybean may play an active part in the perception of pathogen-associated molecular patterns during broad host resistance. J Biol Chem 279:1132–1140. https://doi.org/10.1074/jbc.M308552200
Fliegmann J, Montel E, Djulić A et al (2005) Catalytic properties of the bifunctional soybean β-glucan-binding protein, a member of family 81 glycoside hydrolases. FEBS Lett 579:6647–6652. https://doi.org/10.1016/j.febslet.2005.10.060
Flors V, Leyva MO, Vicedo B et al (2007) Absence of the endo-beta-1,4-glucanases Cel1 and Cel2 reduces susceptibility to Botrytis cinerea in tomato. Plant J Cell Mol Biol 52:1027–1040. https://doi.org/10.1111/j.1365-313X.2007.03299.x
Fotopoulos V, Gilbert MJ, Pittman JK et al (2003) The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atβfruct1, are induced in arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiol 132:821–829. https://doi.org/10.1104/pp.103.021428
Fuchs R, Kopischke M, Klapprodt C et al (2016) Immobilized subpopulations of leaf epidermal mitochondria mediate PENETRATION2-dependent pathogen entry control in Arabidopsis. Plant Cell 28:130–145. https://doi.org/10.1105/tpc.15.00887
Gao F, Zhang B-S, Zhao J-H et al (2019) Deacetylation of chitin oligomers increases virulence in soil-borne fungal pathogens. Nat Plants 5:1167–1176. https://doi.org/10.1038/s41477-019-0527-4
Geoghegan I, Steinberg G, Gurr S (2017) The role of the fungal cell wall in the infection of plants. Trends Microbiol 25:957–967. https://doi.org/10.1016/j.tim.2017.05.015
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227. https://doi.org/10.1146/annurev.phyto.43.040204.135923
Gloster TM, Turkenburg JP, Potts JR et al (2008) Divergence of catalytic mechanism within a glycosidase family provides insight into evolution of carbohydrate metabolism by human gut flora. Chem Biol 15:1058–1067. https://doi.org/10.1016/j.chembiol.2008.09.005
Goujon T, Minic Z, El Amrani A et al (2003) AtBXL1, a novel higher plant (Arabidopsis thaliana) putative beta-xylosidase gene, is involved in secondary cell wall metabolism and plant development. Plant J 33:677–690. https://doi.org/10.1046/j.1365-313X.2003.01654.x
Gross M, Geier G, Rudolph K, Geider K (1992) Levan and levansucrase synthesized by the fireblight pathogen Erwinia amylovora. Physiol Mol Plant Pathol 40:371–381. https://doi.org/10.1016/0885-5765(92)90029-U
Guzha A, McGee R, Scholz P et al (2022) Cell wall-localized BETA-XYLOSIDASE4 contributes to immunity of Arabidopsis against Botrytis cinerea. Plant Physiol 189:1794–1813. https://doi.org/10.1093/plphys/kiac165
Hadfield KA, Bennett AB (1998) Polygalacturonases: many genes in search of a function. Plant Physiol 117:337–343. https://doi.org/10.1104/pp.117.2.337
Ham K-S, Wu S-C, Darvill AG, Albersheim P (1997) Fungal pathogens secrete an inhibitor protein that distinguishes isoforms of plant pathogenesis-related endo-β-1,3-glucanases. Plant J 11:169–179. https://doi.org/10.1046/j.1365-313X.1997.11020169.x
Han L-B, Li Y-B, Wang F-X et al (2019) The cotton apoplastic protein CRR1 stabilizes chitinase 28 to facilitate defense against the fungal pathogen Verticillium dahliae. Plant Cell 31:520–536. https://doi.org/10.1105/tpc.18.00390
He Y, Karre S, Johal GS et al (2019) A maize polygalacturonase functions as a suppressor of programmed cell death in plants. BMC Plant Biol 19:310. https://doi.org/10.1186/s12870-019-1897-5
He J, Kong M, Qian Y et al (2023) Cellobiose elicits immunity in lettuce conferring resistance to Botrytis cinerea. J Exp Bot 74:1022–1038. https://doi.org/10.1093/jxb/erac448
Hennig J, Malamy J, Grynkiewicz G et al (1993) Interconversion of the salicylic acid signal and its glucoside in tobacco. Plant J 4:593–600. https://doi.org/10.1046/j.1365-313X.1993.04040593.x
Henrissat B, Davies G (1997) Structural and sequence-based classification of glycoside hydrolases. Curr Opin Struct Biol 7:637–644. https://doi.org/10.1016/S0959-440X(97)80072-3
Himeno N, Saburi W, Wakuta S et al (2013) Identification of rice β-glucosidase with high hydrolytic activity towards salicylic acid β-d-glucoside. Biosci Biotechnol Biochem 77:934–939. https://doi.org/10.1271/bbb.120889
Homma F, Huang J, van der Hoorn RA (2023) Alphafold-multimer predicts cross-kingdom interactions at the plant-pathogen interface. bioRxiv. https://doi.org/10.1101/2023.04.03.535425
Hu X, Cui Y, Lu X et al (2020) Maize WI5 encodes an endo-1,4-β-xylanase required for secondary cell wall synthesis and water transport in xylem. J Integr Plant Biol 62:1607–1624. https://doi.org/10.1111/jipb.12923
Hua Y, Ekkhara W, Sansenya S et al (2015) Identification of rice Os4BGlu13 as a β-glucosidase which hydrolyzes gibberellin A4 1-O-β-d-glucosyl ester, in addition to tuberonic acid glucoside and salicylic acid derivative glucosides. Arch Biochem Biophys 583:36–46. https://doi.org/10.1016/j.abb.2015.07.021
Huang X, Luo W, Wu S et al (2020) Apoplastic maize fructan exohydrolase Zm-6-FEH displays substrate specificity for levan and is induced by exposure to levan-producing bacteria. Int J Biol Macromol 163:630–639. https://doi.org/10.1016/j.ijbiomac.2020.06.254
Igawa T, Tokai T, Kudo T et al (2005) A wheat xylanase inhibitor gene, Xip-I, but not Taxi-I, is significantly induced by biotic and abiotic signals that trigger plant defense. Biosci Biotechnol Biochem 69:1058–1063. https://doi.org/10.1271/bbb.69.1058
Iqbal MM, Nazir F, Ali S et al (2012) Over expression of rice chitinase gene in transgenic peanut (Arachis hypogaea L.) improves resistance against leaf spot. Mol Biotechnol 50:129–136. https://doi.org/10.1007/s12033-011-9426-2
Islam MM, Tani C, Watanabe-Sugimoto M et al (2009) Myrosinases, TGG1 and TGG2, redundantly function in ABA and MeJA signaling in Arabidopsis guard cells. Plant Cell Physiol 50:1171–1175. https://doi.org/10.1093/pcp/pcp066
Jia H, Wang C, Zhang C et al (2016) Functional analysis of VvBG1 during fruit development and ripening of grape. J Plant Growth Regul 35:987–999. https://doi.org/10.1007/s00344-016-9597-y
Jiang C-J, Shimono M, Sugano S et al (2010) Abscisic acid interacts antagonistically with salicylic acid signaling pathway in rice-Magnaporthe grisea interaction. Mol Plant Microbe Interact 23:791–798. https://doi.org/10.1094/MPMI-23-6-0791
Johansson ON, Fantozzi E, Fahlberg P et al (2014) Role of the penetration-resistance genes PEN1, PEN2 and PEN3 in the hypersensitive response and race-specific resistance in Arabidopsis thaliana. Plant J 79:466–476. https://doi.org/10.1111/tpj.12571
Johnson JM, Thürich J, Petutschnig EK et al (2018) A poly(A) ribonuclease controls the cellotriose-based interaction between Piriformospora indica and its host Arabidopsis. Plant Physiol 176:2496–2514. https://doi.org/10.1104/pp.17.01423
Juge N, Payan F, Williamson G (2004) XIP-I, a xylanase inhibitor protein from wheat: a novel protein function. Biochim Biophys Acta 1696:203–211. https://doi.org/10.1016/j.bbapap.2003.08.014
Kaku H, Shibuya N, Xu P et al (1997) N-acetylchitooligosaccharides elicit expression of a single (1 → 3)-β-glucanase gene in suspension-cultured cells from barley (Hordeum vulgare). Physiol Plant 100:111–118. https://doi.org/10.1111/j.1399-3054.1997.tb03460.x
Kaku H, Nishizawa Y, Ishii-Minami N et al (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci USA 103:11086–11091. https://doi.org/10.1073/pnas.0508882103
Kawano T, Tanaka S, Kadono T, Muto S (2004) Salicylic acid glucoside acts as a slow inducer of oxidative burst in tobacco suspension culture. Z Naturforsch C J Biosci 59:684–692. https://doi.org/10.1515/znc-2004-9-1013
Keen NT, Yoshikawa M (1983) β-1,3-Endoglucanase from soybean releases elicitor-active carbohydrates from fungus cell walls. Plant Physiol 71:460–465. https://doi.org/10.1104/pp.71.3.460
Keen NT, Yoshikawa M, Wang MC (1983) Phytoalexin elicitor activity of carbohydrates from Phytophthora megasperma f. sp. glycinea and other sources. Plant Physiol 71(3):466–471. https://doi.org/10.1104/pp.71.3.466
Ketudat Cairns JR, Mahong B, Baiya S, Jeon J-S (2015) β-glucosidases: multitasking, moonlighting or simply misunderstood? Plant Sci 241:246–259. https://doi.org/10.1016/j.plantsci.2015.10.014
Kim DS, Kim NH, Hwang BK (2015) The Capsicum annuum class IV chitinase ChitIV interacts with receptor-like cytoplasmic protein kinase PIK1 to accelerate PIK1-triggered cell death and defence responses. J Exp Bot 66:1987–1999. https://doi.org/10.1093/jxb/erv001
Kim S-J, Chandrasekar B, Rea AC et al (2020) The synthesis of xyloglucan, an abundant plant cell wall polysaccharide, requires CSLC function. Proc Natl Acad Sci 117:20316–20324. https://doi.org/10.1073/pnas.2007245117
Kim C-Y, Park J-Y, Choi G et al (2022) A rice gene encoding glycosyl hydrolase plays contrasting roles in immunity depending on the type of pathogens. Mol Plant Pathol 23:400–416. https://doi.org/10.1111/mpp.13167
Kirubakaran SI, Sakthivel N (2007) Cloning and overexpression of antifungal barley chitinase gene in Escherichia coli. Protein Expr Purif 52:159–166. https://doi.org/10.1016/j.pep.2006.08.012
Klarzynski O, Plesse B, Joubert J-M et al (2000) Linear β-1,3 glucans are elicitors of defense responses in tobacco. Plant Physiol 124:1027–1038. https://doi.org/10.1104/pp.124.3.1027
Kocal N, Sonnewald U, Sonnewald S (2008) Cell wall-bound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pv. vesicatoria. Plant Physiol 148:1523–1536. https://doi.org/10.1104/pp.108.127977
Kötzler MP, Hancock SM, Withers SG (2014) Glycosidases: functions, families and folds. In: Encyclopedia of life sciences. Wiley, New York
Kramer M, Sanders R, Bolkan H et al (1992) Postharvest evaluation of transgenic tomatoes with reduced levels of polygalacturonase: processing, firmness and disease resistance. Postharvest Biol Technol 1:241–255. https://doi.org/10.1016/0925-5214(92)90007-C
Lacchini E, Erffelinck M-L, Mertens J et al (2023) The saponin bomb: a nucleolar-localized β-glucosidase hydrolyzes triterpene saponins in Medicago truncatula. New Phytol 239:705–719. https://doi.org/10.1111/nph.18763
Leah R, Kigel J, Svendsen I, Mundy J (1995) Biochemical and molecular characterization of a barley seed β-glucosidase. J Biol Chem 270:15789–15797. https://doi.org/10.1074/jbc.270.26.15789
Leclercq J, Fliegmann J, Tellström V et al (2008) Identification of a multigene family encoding putative β-glucan-binding proteins in Medicago truncatula. J Plant Physiol 165:766–776. https://doi.org/10.1016/j.jplph.2007.02.008
Li Q, Ji K, Sun Y et al (2013) The role of FaBG3 in fruit ripening and B. cinerea fungal infection of strawberry. Plant J 76:24–35. https://doi.org/10.1111/tpj.12272
Li B, Liu Y, Wu T et al (2019) OsBGLU19 and OsBGLU23 regulate disease resistance to bacterial leaf streak in rice. J Integr Agric 18:1199–1210. https://doi.org/10.1016/S2095-3119(18)62117-3
Liu X, Grabherr HM, Willmann R et al (2014) Host-induced bacterial cell wall decomposition mediates pattern-triggered immunity in Arabidopsis. Elife 3:e01990. https://doi.org/10.7554/eLife.01990
Liu Y-H, Song Y-H, Ruan Y-L (2022) Sugar conundrum in plant–pathogen interactions: roles of invertase and sugar transporters depend on pathosystems. J Exp Bot 73:1910–1925. https://doi.org/10.1093/jxb/erab562
Livingston DP, Hincha DK, Heyer AG (2009) Fructan and its relationship to abiotic stress tolerance in plants. Cell Mol Life Sci 66:2007–2023. https://doi.org/10.1007/s00018-009-0002-x
López-Cruz J, Finiti I, Fernández-Crespo E et al (2014) Absence of endo-1,4-β-glucanase KOR1 alters the jasmonate-dependent defence response to Pseudomonas syringae in Arabidopsis. J Plant Physiol 171:1524–1532. https://doi.org/10.1016/j.jplph.2014.07.006
Lu X, Tintor N, Mentzel T et al (2009) Uncoupling of sustained MAMP receptor signaling from early outputs in an Arabidopsis endoplasmic reticulum glucosidase II allele. Proc Natl Acad Sci 106:22522–22527. https://doi.org/10.1073/pnas.0907711106
Lv G, Zhang Y, Ma L et al (2023) A cell wall invertase modulates resistance to fusarium crown rot and sharp eyespot in common wheat. J Integr Plant Biol. https://doi.org/10.1111/jipb.13478
Maximova SN, Marelli J-P, Young A et al (2006) Over-expression of a cacao class I chitinase gene in Theobroma cacao L. enhances resistance against the pathogen, Colletotrichum gloeosporioides. Planta 224:740–749. https://doi.org/10.1007/s00425-005-0188-6
Minic Z (2008) Physiological roles of plant glycoside hydrolases. Planta 227:723–740. https://doi.org/10.1007/s00425-007-0668-y
Minic Z, Jouanin L (2006) Plant glycoside hydrolases involved in cell wall polysaccharide degradation. Plant Physiol Biochem 44:435–449. https://doi.org/10.1016/j.plaphy.2006.08.001
Minic Z, Rihouey C, Do CT et al (2004) Purification and characterization of enzymes exhibiting β-d-xylosidase activities in stem tissues of Arabidopsis. Plant Physiol 135:867–878. https://doi.org/10.1104/pp.104.041269
Mithöfer A, Lottspeich F, Ebel J (1996) One-step purification of the β-glucan elicitor-binding protein from soybean (Glycine max L.) roots and characterization of an anti-peptide antiserum. FEBS Lett 381:203–207. https://doi.org/10.1016/0014-5793(96)00126-3
Miya A, Albert P, Shinya T et al (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci 104:19613–19618. https://doi.org/10.1073/pnas.0705147104
Nakano RT, Piślewska-Bednarek M, Yamada K et al (2017) PYK10 myrosinase reveals a functional coordination between endoplasmic reticulum bodies and glucosinolates in Arabidopsis thaliana. Plant J Cell Mol Biol 89:204–220. https://doi.org/10.1111/tpj.13377
Nicol F, His I, Jauneau A et al (1998) A plasma membrane-bound putative endo-1,4-β-d-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J 17:5563–5576. https://doi.org/10.1093/emboj/17.19.5563
Okinaka Y, Mimori K, Takeo K, Kitamura S, Takeuchi Y, Yamaoka N, Yoshikawa M (1995) A structural model for the mechanisms of elicitor release from fungal cell walls by plant beta-1,3-endoglucanase. Plant Physiol 109(3):839–845. https://doi.org/10.1104/pp.109.3.839
Opassiri R, Maneesan J, Akiyama T et al (2010) Rice Os4BGlu12 is a wound-induced β-glucosidase that hydrolyzes cell wall-β-glucan-derived oligosaccharides and glycosides. Plant Sci 179:273–280. https://doi.org/10.1016/j.plantsci.2010.05.013
Passarinho PA, de Vries SC (2002) Arabidopsis chitinases: a genomic survey. Arab Book Am Soc Plant Biol 1:e0023. https://doi.org/10.1199/tab.0023
Pattathil S, Ingwers MW, Aubrey DP et al (2017) A quantitative method for analyzing glycome profiles of plant cell walls. Carbohydr Res 448:128–135. https://doi.org/10.1016/j.carres.2017.06.009
Phillips DC (1967) The hen egg-white lysozyme molecule. Proc Natl Acad Sci 57:483–495. https://doi.org/10.1073/pnas.57.3.483
Prasad K, Bhatnagar-Mathur P, Waliyar F, Sharma KK (2013) Overexpression of a chitinase gene in transgenic peanut confers enhanced resistance to major soil borne and foliar fungal pathogens. J Plant Biochem Biotechnol 22:222–233. https://doi.org/10.1007/s13562-012-0155-9
Proels RK, Hückelhoven R (2014) Cell-wall invertases, key enzymes in the modulation of plant metabolism during defence responses. Mol Plant Pathol 15:858–864. https://doi.org/10.1111/mpp.12139
Pusztahelyi T (2018) Chitin and chitin-related compounds in plant–fungal interactions. Mycology 9:189–201. https://doi.org/10.1080/21501203.2018.1473299
Rajninec M, Jopcik M, Danchenko M, Libantova J (2020) Biochemical and antifungal characteristics of recombinant class I chitinase from Drosera rotundifolia. Int J Biol Macromol 161:854–863. https://doi.org/10.1016/j.ijbiomac.2020.06.123
Ren Y-Y, West CA (1992) Elicitation of diterpene biosynthesis in rice (Oryza sativa L.) by chitin 1. Plant Physiol 99:1169–1178. https://doi.org/10.1104/pp.99.3.1169
Roby D, Gadelle A, Toppan A (1987) Chitin oligosaccharides as elicitors of chitinase activity in melon plants. Biochem Biophys Res Commun 143:885–892. https://doi.org/10.1016/0006-291X(87)90332-9
Roulin S, Xu P, Brown AHD, Fincher GB (1997) Expression of specific (1→3)-β-glucanase genes in leaves of near-isogenic resistant and susceptible barley lines infected with the leaf scald fungus (Rhynchosporium secalis). Physiol Mol Plant Pathol 50:245–261. https://doi.org/10.1006/pmpp.1997.0084
Sampedro J, Gianzo C, Iglesias N et al (2012) AtBGAL10 is the main xyloglucan β-galactosidase in Arabidopsis, and its absence results in unusual xyloglucan subunits and growth defects. Plant Physiol 158:1146–1157. https://doi.org/10.1104/pp.111.192195
Sánchez-Vallet A, Mesters JR, Thomma BPHJ (2015) The battle for chitin recognition in plant-microbe interactions. FEMS Microbiol Rev 39:171–183. https://doi.org/10.1093/femsre/fuu003
Scharte J, Schön H, Weis E (2005) Photosynthesis and carbohydrate metabolism in tobacco leaves during an incompatible interaction with Phytophthora nicotianae. Plant Cell Environ 28:1421–1435. https://doi.org/10.1111/j.1365-3040.2005.01380.x
Schmidt K, Pflugmacher M, Klages S et al (2008) Accumulation of the hormone abscisic acid (ABA) at the infection site of the fungus Cercospora beticola supports the role of ABA as a repressor of plant defence in sugar beet. Mol Plant Pathol 9:661–673. https://doi.org/10.1111/j.1364-3703.2008.00491.x
Schoffelmeer EAM, Klis FM, Sietsma JH, Cornelissen BJC (1999) The cell wall of Fusarium oxysporum. Fungal Genet Biol 27:275–282. https://doi.org/10.1006/fgbi.1999.1153
Seo S, Ishizuka K, Ohashi Y (1995) Induction of salicylic acid β-glucosidase in tobacco leaves by exogenous salicylic acid. Plant Cell Physiol 36:447–453. https://doi.org/10.1093/oxfordjournals.pcp.a078779
Seshadri S, Akiyama T, Opassiri R et al (2009) Structural and enzymatic characterization of Os3BGlu6, a rice β-glucosidase hydrolyzing hydrophobic glycosides and (1→3)- and (1→2)-linked disaccharides. Plant Physiol 151:47–58. https://doi.org/10.1104/pp.109.139436
Sherameti I, Venus Y, Drzewiecki C et al (2008) PYK10, a β-glucosidase located in the endoplasmatic reticulum, is crucial for the beneficial interaction between Arabidopsis thaliana and the endophytic fungus Piriformospora indica. Plant J 54:428–439. https://doi.org/10.1111/j.1365-313X.2008.03424.x
Shetty N, Jensen J, Knudsen A et al (2009) Effects of beta-1,3-glucan from Septoria tritici on structural defence responses in wheat. J Exp Bot 60:4287–4300. https://doi.org/10.1093/jxb/erp269
Sidar A, Albuquerque ED, Voshol GP et al (2020) Carbohydrate binding modules: diversity of domain architecture in amylases and cellulases from filamentous microorganisms. Front Bioeng Biotechnol 8:871. https://doi.org/10.3389/fbioe.2020.00871
Silva CJ, van den Abeele C, Ortega-Salazar I et al (2021) Host susceptibility factors render ripe tomato fruit vulnerable to fungal disease despite active immune responses. J Exp Bot 72:2696–2709. https://doi.org/10.1093/jxb/eraa601
Simpson PJ, Jamieson SJ, Abou-Hachem M et al (2002) The solution structure of the CBM4-2 carbohydrate binding module from a thermostable Rhodothermus marinus xylanase. Biochemistry 41:5712–5719. https://doi.org/10.1021/bi012093i
Sueldo DJ, Godson A, Kaschani F et al (2024) Activity-based proteomics uncovers suppressed hydrolases and a neo-functionalised antibacterial enzyme at the plant–pathogen interface. New Phytol 24:394–448. https://doi.org/10.1111/nph.18857
Suen DF, Huang AHC (2007) Maize pollen coat xylanase facilitates pollen tube penetration into silk during sexual reproduction. J Biol Chem 282:625–636. https://doi.org/10.1074/jbc.M608567200
Sugiyama R, Hirai MY (2019) Atypical myrosinase as a mediator of glucosinolate functions in plants. Front Plant Sci 10:1008. https://doi.org/10.3389/fpls.2019.01008
Sun L, Yang D, Kong Y et al (2014) Sugar homeostasis mediated by cell wall invertase GRAIN INCOMPLETE FILLING 1 (GIF1) plays a role in pre-existing and induced defence in rice. Mol Plant Pathol 15:161–173. https://doi.org/10.1111/mpp.12078
Swarbrick PJ, Schulze-Lefert P, Scholes JD (2006) Metabolic consequences of susceptibility and resistance (race-specific and broad-spectrum) in barley leaves challenged with powdery mildew. Plant Cell Environ 29:1061–1076. https://doi.org/10.1111/j.1365-3040.2005.01472.x
Szeja W, Grynkiewicz G, Rusin A (2017) Isoflavones, their glycosides and glycoconjugates. Synthesis and biological activity. Curr Org Chem 21:218–235. https://doi.org/10.2174/1385272820666160928120822
Takahashi H, Kanayama Y, Zheng MS et al (2004) Antagonistic interactions between the SA and JA signaling pathways in arabidopsis modulate expression of defense genes and gene-for-gene resistance to cucumber mosaic virus. Plant Cell Physiol 45:803–809. https://doi.org/10.1093/pcp/pch085
Takeuchi Y, Yoshikawa M, Takeba G et al (1990) Molecular cloning and ethylene induction of mRNA Encoding a phytoalexin elicitor-releasing factor, β-1,3-endoglucanase, in soybean 1. Plant Physiol 93:673–682. https://doi.org/10.1104/pp.93.2.673
Tauzin AS, Giardina T (2014) Sucrose and invertases, a part of the plant defense response to the biotic stresses. Front Plant Sci 5:293. https://doi.org/10.3389/fpls.2014.00293
Tu B, Zhang T, Wang Y et al (2020) Membrane-associated xylanase-like protein OsXYN1 is required for normal cell wall deposition and plant development in rice. J Exp Bot 71:4797–4811. https://doi.org/10.1093/jxb/eraa200
Umemoto N, Kakitani M, Iwamatsu A et al (1997) The structure and function of a soybean β-glucan-elicitor-binding protein. Proc Natl Acad Sci 94:1029–1034. https://doi.org/10.1073/pnas.94.3.1029
Valluru R, Van den Ende W (2008) Plant fructans in stress environments: emerging concepts and future prospects. J Exp Bot 59:2905–2916. https://doi.org/10.1093/jxb/ern164
van den Burg HA, Harrison SJ, Joosten MHAJ et al (2006) Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol Plant Microbe Interact 19:1420–1430. https://doi.org/10.1094/MPMI-19-1420
Van den Ende W (2022) Different evolutionary pathways to generate plant fructan exohydrolases. J Exp Bot 73:4620–4623. https://doi.org/10.1093/jxb/erac305
Van den Ende W, De Coninck B, Van Laere A (2004) Plant fructan exohydrolases: a role in signaling and defense? Trends Plant Sci 9:523–528. https://doi.org/10.1016/j.tplants.2004.09.008
van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162. https://doi.org/10.1146/annurev.phyto.44.070505.143425
Vasconcelos EA, Santana CG, Godoy CV et al (2011) A new chitinase-like xylanase inhibitor protein (XIP) from coffee (Coffea arabica) affects Soybean Asian rust (Phakopsora pachyrhizi) spore germination. BMC Biotechnol 11:14. https://doi.org/10.1186/1472-6750-11-14
Versluys M, Porras-Domínguez JR, De Coninck T et al (2022) A novel chicory fructanase can degrade common microbial fructan product profiles and displays positive cooperativity. J Exp Bot 73:1602–1622. https://doi.org/10.1093/jxb/erab488
von Numers N, Survila M, Aalto M et al (2010) Requirement of a homolog of glucosidase II beta-subunit for EFR-mediated defense signaling in Arabidopsis thaliana. Mol Plant 3:740–750. https://doi.org/10.1093/mp/ssq017
Wang E, Wang J, Zhu X et al (2008) Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat Genet 40:1370–1374. https://doi.org/10.1038/ng.220
Wanke A, van Boerdonk S, Mahdi LK et al (2023) A GH81-type β-glucan-binding protein facilitates colonization by mutualistic fungi in barley. bioRxiv. https://doi.org/10.1101/2023.04.12.536646
Wu L, Armstrong Z, Schröder SP et al (2019) An overview of activity-based probes for glycosidases. Curr Opin Chem Biol 53:25–36. https://doi.org/10.1016/j.cbpa.2019.05.030
Xayphakatsa K, Tsukiyama T, Inouye K et al (2008) Gene cloning, expression, purification and characterization of rice (Oryza sativa L.) class II chitinase CHT11. Enzyme Microb Technol 43:19–24. https://doi.org/10.1016/j.enzmictec.2008.03.012
Xu Q, Wang J, Zhao J et al (2020) A polysaccharide deacetylase from Puccinia striiformis f. sp. tritici is an important pathogenicity gene that suppresses plant immunity. Plant Biotechnol J 18:1830–1842. https://doi.org/10.1111/pbi.13345
Xu P, Wu T, Ali A et al (2022) Rice β-glucosidase 4 (Os1βGlu4) regulates the hull pigmentation via accumulation of salicylic acid. Int J Mol Sci 23:10646. https://doi.org/10.3390/ijms231810646
Yamada A, Shibuya N, Kodama O, Akatsuka T (1993) Induction of phytoalexin formation in suspension-cultured rice cells by N-Acetyl-chitooligosaccharides. Biosci Biotechnol Biochem 57:405–409. https://doi.org/10.1271/bbb.57.405
Yamaguchi T, Yamada A, Hong N et al (2000) Differences in the recognition of glucan elicitor signals between rice and soybean: β-glucan fragments from the rice blast disease fungus Pyricularia oryzae that elicit phytoalexin biosynthesis in suspension-cultured rice cells. Plant Cell 12:817–826. https://doi.org/10.1105/tpc.12.5.817
Yip VLY, Thompson J, Withers SG (2007) Mechanism of GlvA from Bacillus subtilis: a detailed kinetic analysis of a 6-phospho-α-glucosidase from glycoside hydrolase family 4. Biochemistry 46:9840–9852. https://doi.org/10.1021/bi700536p
Yoshikawa M, Matama M, Masago H (1981) Release of a soluble phytoalexin elicitor from mycelial walls of Phytophthora megasperma var. sojae by soybean tissues. Plant Physiol 67:1032–1035. https://doi.org/10.1104/pp.67.5.1032
Yuan X, Eldred LI, Sundin GW (2022) Exopolysaccharides amylovoran and levan contribute to sliding motility in the fire blight pathogen Erwinia amylovora. Environ Microbiol 24:4738–4754. https://doi.org/10.1111/1462-2920.16193
Zhang K, Su H, Zhou J et al (2019) Overexpressing the myrosinase gene TGG1 enhances stomatal defense against Pseudomonas syringae and delays flowering in Arabidopsis. Front Plant Sci 10:1230. https://doi.org/10.3389/fpls.2019.01230
Zhao Y, Wang J, Liu Y et al (2015) Classic myrosinase-dependent degradation of indole glucosinolate attenuates fumonisin B1-induced programmed cell death in Arabidopsis. Plant J Cell Mol Biol 81:920–933. https://doi.org/10.1111/tpj.12778
Acknowledgements
The authors thank the Science and Engineering Research Board (SERB) India for the SRG grant (SRG/2022/000528) and the Birla Institute of Technology and Science—Pilani, Pilani (BITS Pilani) campus for the ACRG grant to Balakumaran Chandrasekar. Muthusaravanan Sivaramakrishnan and Chetan Veeraganti Naveen Prakash are supported by the Institute Fellowship from Birla Institute of Technology and Science, Pilani (BITS Pilani), India. The authors would like to thank Ms. Sakshi Goel for contributing to initial literature searches and discussions.
Author information
Authors and Affiliations
Contributions
BC helped in idea and conceptualization and performed supervision, project administration, funding acquisition, and writing—original draft preparation; MS, CVNP, and BC were involved in literature review and writing—review and editing. CVNP and BC prepared table; MS and BC prepared figures. MS performed bioinformatic analysis.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Gerhard Leubner.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Sivaramakrishnan, M., Veeraganti Naveen Prakash, C. & Chandrasekar, B. Multifaceted roles of plant glycosyl hydrolases during pathogen infections: more to discover. Planta 259, 113 (2024). https://doi.org/10.1007/s00425-024-04391-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-024-04391-5