Abstract
Aim Trichoderma guizhouense
NJAU 4742 (Tgui) can serve as a promising strain for the development of novel biofertilizers and biofungicides. Plants primed with Tgui via inoculation were investigated to clarify the underlying mechanisms that promote root growth and development and activate the plant innate immune response.
Methods
The relative expression of defence-related genes and of genes involved in the auxin signalling pathway in Zea mays and Arabidopsis thaliana was quantified. Scanning electron microscopy (SEM) was performed to visualize the colonization of Tgui in maize roots, and a proteomic approach was used to identify Tgui-derived elicitors.
Results
The establishment of Tgui in the rhizosphere of maize leads to the stimulation of the auxin synthesis pathway in maize and subsequently leads to increased plant growth. And the extracellular proteins of Tgui induced systemic resistance (ISR) of maize plants to Fusarium verticillioides (Fv) (Hypocreales, Ascomycota); the ISR of maize plants may be linked to the accumulation of reactive oxygen species (ROS) and increased deposition of callose in maize tissue.
Conclusions
Activation of the maize immune response was triggered by the mixture of extracellular proteins secreted by Tgui into the rhizosphere. Our study thereby contributes to a better understanding of the interaction between T. guizhouense and plant roots.
Similar content being viewed by others
Abbreviations
- ROS:
-
reactive oxygen species
- MAMP:
-
microbe-associated molecular pattern
- SSCRP:
-
small, secreted cysteine-rich protein
- CAZymes:
-
carbohydrate active enzymes
- SEM:
-
scanning electron microscopy
- qPCR:
-
quantitative PCR
- CWI:
-
cell wall invertase
- DAPI:
-
4′,6-diamidino-2-phenylindole
- DAB:
-
3′,3′-diaminobenzidine
References
Berger D, Altmann T (2000) A subtilisin-like serine protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana. Genes Dev 14:1119–1131. https://doi.org/10.1101/gad.14.9.1119
Bindschedler LV, Dewdney J, Blee KA, Stone JM, Asai T, Plotnikov J, Denoux C, Hayes T, Gerrish C, Davies DR, Ausubel FM, Paul Bolwell G (2006) Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J 47:851–863. https://doi.org/10.1111/j.1365-313X.2006.02837.x
Camejo D, Guzmán-Cedeño Á, Moreno A (2016) Reactive oxygen species, essential molecules, during plant-pathogen interactions. Plant Physiol Biochem 103:10–23. https://doi.org/10.1016/j.plaphy.2016.02.035
Chaverri P, Branco-Rocha F, Jaklitsch W, Gazis R, Degenkolb T, Samuels GJ (2015) Systematics of the Trichoderma harzianum species complex and the re-identification of commercial biocontrol strains. Mycologia 107:558–590. https://doi.org/10.3852/14-147
Chen Y, Yordanov YS, Ma C, Strauss S, Busov VB (2013) DR5 as a reporter system to study auxin response in Populus. Plant Cell Rep 32:453–463. https://doi.org/10.1007/s00299-012-1378-x
Chen SC, Ren JJ, Zhao HJ, Wang XL, Wang TH, Jin SD, Wang ZH, Li C, Liu AR, Lin XM, Ahammed GJ (2019) Trichoderma harzianum improves defence against Fusarium oxysporum by regulating ROS and RNS metabolism, redox balance, and energy flow in cucumber roots. Phytopathology. https://doi.org/10.1094/phyto-09-18-0342-r
Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323:95–101. https://doi.org/10.1126/science.1164627
Conrath U, Beckers GJM, Langenbach CJG, Jaskiewicz MR (2015) Priming for enhanced defence. Annu Rev Phytopathol. https://doi.org/10.1146/annurev-phyto-080614-120132
Contreras-Cornejo HA, Macías-Rodríguez L, Beltrán-Peña E, Herrera-Estrella A, López-Bucio J (2011) Trichoderma-induced plant immunity likely involves both hormonal- and camalexindependent mechanisms in Arabidopsis thaliana and confers resistance against necrotrophic fungus Botrytis cinerea. Plant Signal Behav. https://doi.org/10.4161/psb.6.10.17443
Crutcher FK, Moran-diez ME, Ding S (2015) A paralog of the proteinaceous elicitor SM1 is involved in colonization of maize roots by Trichoderma virens. Fungal biol 1–11. https://doi.org/10.1016/j.funbio.2015.01.004
Daudi A, Cheng Z, O’Brien JA, Mammarella N, Khan S, Ausubel FM, Bolwell GP (2012) The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity. Plant Cell 24:275–287. https://doi.org/10.1105/tpc.111.093039
De Souza JT, Bailey BA, Pomella AWVV, Erbe EF, Murphy CA, Bae H, Hebbar PK (2008) Colonization of cacao seedlings by Trichoderma stromaticum, a mycoparasite of the witches’ broom pathogen, and its influence on plant growth and resistance. Biol Control 46:36–45. https://doi.org/10.1016/j.biocontrol.2008.01.010
Delaunois B, Farace G, Jeandet P, Clément C, Baillieul F, Dorey S, Cordelier S (2014) Elicitors as alternative strategy to pesticides in grapevine? Current knowledge on their mode of action from controlled conditions to vineyard. Environ Sci Pollut Res 21:4837–4846. https://doi.org/10.1007/s11356-013-1841-4
Djonovi S, Pozo MJ, Dangott LJ, Howell CR, Kenerley CM, Djonović S, Pozo MJ, Dangott LJ, Howell CR, Kenerley CM (2006) Sm1, a Proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant Defence responses and systemic resistance. Mol Plant-Microbe Interact 19:838–853. https://doi.org/10.1094/MPMI-19-0838
Djonovic S, Vargas WA, Kolomiets MV, Horndeski M, Wiest A, Kenerley CM (2007) A Proteinaceous elicitor Sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol 145:875–889. https://doi.org/10.1104/pp.107.103689
Druzhinina IS, Kubicek CP (2013) Ecological genomics of Trichoderma. In: the ecological genomics of fungi, 1st edn. John Wiley & Sons Inc, Hoboken, NJ, pp 89–116
Druzhinina IS, Kubicek CP, Komon-Zelazowska M, Belayneh Mulaw T, Bissett J (2010) The Trichoderma harzianum demon: complex speciation history resulting in coexistence of hypothetical biological species, recent agamospecies and numerous relict lineages. BMC Evol Biol 10:94. https://doi.org/10.1186/1471-2148-10-94
Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP (2011) Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9:749–759. https://doi.org/10.1038/nrmicro2637
Druzhinina IS, Shelest E, Kubicek CP (2012) Novel traits of Trichoderma predicted through the analysis of its secretome. FEMS Microbiol Lett 337:1–9. https://doi.org/10.1111/j.1574-6968.2012.02665.x
Druzhinina IS, Chenthamara K, Zhang J, Atanasova L, Yang D, Miao Y, Rahimi MJ, Grujic M, Cai F, Pourmehdi S, Salim KA, Pretzer C, Kopchinskiy AG, Henrissat B, Kuo A, Hundley H, Wang M, Aerts A, Salamov A, Lipzen A, LaButti K, Barry K, Grigoriev IV, Shen Q, Kubicek CP (2018) Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts. PLoS Genet 14:e1007322. https://doi.org/10.1371/journal.pgen.1007322
Duncan KE, Howard RJ (2009) Biology of maize kernel infection by Fusarium verticillioides. Mol Plant-Microbe Interact. https://doi.org/10.1094/mpmi-23-1-0006
Fan LL, Fu KH, Yu CJ, Li YY, Li YQ, Chen J (2015a) Thc6 protein, isolated from Trichoderma harzianum, can induce maize defence response against Curvularia lunata. J Basic Microbiol 55:591–600. https://doi.org/10.1002/jobm.201300814
Fan LS, Li RL, Pan JW, Ding ZJ, Lin JX (2015b) Endocytosis and its regulation in plants. Trends Plant Sci 20:388–397. https://doi.org/10.1016/j.tplants.2015.03.014
Fandohan P, Hell K, Marasas WFO, Wingfield MJ (2003) Infection of maize by Fusarium species and contamination with fumonisin in africa. African J Biotechnol 2:570–579. https://doi.org/10.5897/ajb2003.000-1110
Figueiredo A, Monteiro F, Sebastiana M (2014) Subtilisin-like proteases in plant-pathogen recognition and immune priming: a perspective. Front Plant Sci 5:1–4. https://doi.org/10.3389/fpls.2014.00739
Freitas RS, Steindorff AS, Ramada MHS, de Siqueira SJL, Noronha EF, Ulhoa CJ (2014) Cloning and characterization of a protein elicitor Sm1 gene from Trichoderma harzianum. Biotechnol Lett 36:783–788. https://doi.org/10.1007/s10529-013-1410-4
Friedl MA, Druzhinina IS (2012) Taxon-specific metagenomics of Trichoderma reveals a narrow community of opportunistic species that regulate each other’s development. Microbiology 158:69–83. https://doi.org/10.1099/mic.0.052555-0
Gaderer R, Lamdan NL, Frischmann A, Sulyok M, Krska R, Horwitz BA, Seidl-seiboth V (2015) Sm2 , a paralog of the Trichoderma cerato-platanin elicitor Sm1 , is also highly important for plant protection conferred by the fungal-root interaction of Trichoderma with maize. BMC Microbiol 15(1):2. https://doi.org/10.1186/s12866-014-0333-0
Gao X, Starr J, Göbel C, Engelberth J, Feussner I, Tumlinson J, Kolomiets M (2008) Maize 9-lipoxygenase ZmLOX3 controls development, root-specific expression of defence genes, and resistance to root-knot nematodes. Mol Plant-Microbe Interact 21:98–109. https://doi.org/10.1094/MPMI-21-1-0098
Gao X, Brodhagen M, Isakeit T, Brown SH, Göbel C, Betran J, Feussner I, Keller NP, Kolomiets M V (2009) Inactivation of the lipoxygenase ZmLOX3 increases susceptibility of maize to Aspergillus spp. Mol Plant-Microbe Interact 22:222–231. https://doi.org/10.1094/MPMI-21-1-0098
Gomes EV, Costa N, Paula, de Paula RG, de Azevedo, RR, da Silva FL, Noronha EF, Ulhoa CJ (2015) The Cerato-Platanin protein Epl-1 from Trichoderma harzianum is involved in mycoparasitism, plant resistance induction and self cell wall protection. Nat Publ Gr 1–13. https://doi.org/10.1038/srep17998
Guzmán-Guzmán P, Porras-Troncoso MD, Olmedo-Monfil V, Herrera-Estrella A (2018) Trichoderma species: versatile plant symbionts. Phytopathology 109:6–16. https://doi.org/10.1094/PHYTO-07-18-0218-RVW
Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species - opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56. https://doi.org/10.1038/nrmicro797
Jelenska J, Davern SM, Standaert RF, Mirzadeh S, Greenberg JT (2017) Flagellin peptide flg22 gains access to long-distance trafficking in Arabidopsis via its receptor, FLS2. J Exp Bot 68:1769–1783. https://doi.org/10.1093/jxb/erx060
Khan J, Ooka JJ, Miller SA, Madden LV, Hoitink HAJ (2004) Systemic resistance induced by Trichoderma hamatum 382 in cucumber against Phytophthora crown rot and leaf blight. Plant Dis 88:280–286. https://doi.org/10.1094/Pdis.2004.88.3.280
Kombrink A, Sánchez-Vallet A, Thomma BPHJ (2011) The role of chitin detection in plant-pathogen interactions. Microbes Infect 13:1168–1176. https://doi.org/10.1016/j.micinf.2011.07.010
Kong J, Wei M, Li G, Lei R, Qiu Y, Wang C, Li ZH, Zhu S (2018) The cucumber mosaic virus movement protein suppresses PAMP-triggered immune responses in Arabidopsis and tobacco. Biochem Biophys Res Commun 498:395–401. https://doi.org/10.1016/j.bbrc.2018.01.072
Kubicek CP, Steindorff AS, Chenthamara K, Manganiello G, Henrissat B, Zhang J, Cai F, Kopchinskiy AG, Kubicek EM, Kuo A, Baroncelli R, Sarrocco S, Noronha EF, Vannacci G, Shen Q, Grigoriev IV, Druzhinina IS (2019) Evolution and comparative genomics of the most common Trichoderma species. BMC Genomics 20:485. https://doi.org/10.1186/s12864-019-5680-7
Kumar V, Parkhi V, Joshi SG, Christensen S, Jayaprakasha GK, Patil BS, Kolomiets MV, Rathore KS (2012) A novel, conditional, lesion mimic phenotype in cotton cotyledons due to the expression of an endochitinase gene from Trichoderma virens. Plant Sci 183:86–95. https://doi.org/10.1016/j.plantsci.2011.11.005
Lai J, Li R, Xu X, Jin W, Xu M, Zhao H, Xiang Z, Song W, Ying K, Zhang M, Jiao Y, Ni P, Zhang J, Li D, Guo X, Ye K, Jian M, Wang B, Zheng H et al (2010) Genome-wide patterns of genetic variation among elite maize inbred lines. Nat Genet 42:1027–1030. https://doi.org/10.1038/ng.684
Levy A, Salas Gonzalez I, Mittelviefhaus M, Clingenpeel S, Herrera Paredes S, Miao J, Wang K, Devescovi G, Stillman K, Monteiro F, Rangel Alvarez B, Lundberg DS, Lu TY, Lebeis S, Jin Z, McDonald M, Klein AP, Feltcher ME, Rio TG, Grant SR, Doty SL, Ley RE, Zhao B, Venturi V, Pelletier DA, Vorholt JA, Tringe SG, Woyke T, Dangl JL (2018) Genomic features of bacterial adaptation to plants. Nat Genet 50:138–150. https://doi.org/10.1038/s41588-017-0012-9
Liu Y, Guo Y, Ma C, Zhang D, Wang C, Yang Q, Xu M (2016) Transcriptome analysis of maize resistance to Fusarium graminearum. BMC Genomics 17:1–13. https://doi.org/10.1186/s12864-016-2780-5
Lloyd SR, Schoonbeek H, Trick M, Zipfel C, Ridout CJ (2014) Methods to study PAMP-triggered immunity in Brassica species. Mol Plant-Microbe Interact 27:286–295. https://doi.org/10.1094/MPMI-05-13-0154-FI
Logrieco A, Bottalico A (1988) Fusarium species of the Liseola section associated with stalk and ear rot of maize in southern Italy, and their ability to produce moniliformin. Trans Br Mycol Soc 90:215–219. https://doi.org/10.1016/S0007-1536(88)80092-5
Marra R, Lombardi N, D’Errico G, Troisi J, Scala G, Vinale F, Woo SL, Bonanomi G, Lorito M (2019) Application of Trichoderma strains and metabolites enhances soybean productivity and nutrient content agricultural and environmental chemistry application of Trichoderma strains and metabolites enhances soybean productivity and nutrient content. J Agric Food Chem 67:1814–1822. https://doi.org/10.1021/acs.jafc.8b06503
Mendoza-Mendoza A, Zaid R, Lawry R, Hermosa R, Monte E, Horwitz BA, Mukherjee PK (2018) Molecular dialogues between Trichoderma and roots: role of the fungal secretome. Fungal Biol Rev 32:62–85. https://doi.org/10.1016/j.fbr.2017.12.001
Millet YA, Danna CH, Clay NK, Songnuan W, Simon MD, Werck-Reichhart D, Ausubel FM (2010) Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 22:973–990. https://doi.org/10.1105/tpc.109.069658
Moreno AB, Peñas G, Rufat M, Bravo JM, Estopà M, Messeguer J, San Segundo B (2005) Pathogen-induced production of the antifungal AFP protein from Aspergillus giganteus confers resistance to the blast fungus Magnaporthe grisea in transgenic rice. Mol Plant-Microbe Interact 18:960–972. https://doi.org/10.1094/MPMI-18-0960
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Nanda AK, Andrio E, Marino D, Pauly N, Dunand C (2010) Reactive oxygen species during plant-microorganism early interactions. J Integr Plant Biol 52(2):195–204. https://doi.org/10.1111/j.1744-7909.2010.00933.x
Pazzagli L, Seidl-Seiboth V, Barsottini M, Vargas WA, Scala A, Mukherjee PK (2014) Cerato-platanins: elicitors and effectors. Plant Sci 228:79–87. https://doi.org/10.1016/j.plantsci.2014.02.009
Perazzolli M, Roatti B, Bozza E, Pertot I (2011) Trichoderma harzianum T39 induces resistance against downy mildew by priming for defence without costs for grapevine. Biol Control 58:74–82. https://doi.org/10.1016/j.biocontrol.2011.04.006
Perazzolli M, Moretto M, Fontana P, Ferrarini A, Velasco R, Moser C, Delledonne M, Pertot I (2012) Downy mildew resistance induced by Trichoderma harzianum T39 in susceptible grapevines partially mimics transcriptional changes of resistant genotypes. BMC Genomics 13:1–19. https://doi.org/10.1186/1471-2164-13-660
Piel J, Atzorn R, Gäbler R, Kühnemann F, Boland W (1997) Cellulysin from the plant parasitic fungus Trichoderma viride elicits volatile biosynthesis in higher plants via the octadecanoid signalling cascade. FEBS Lett 416:143–148. https://doi.org/10.1016/S0014-5793(97)01169-1
Pilate G, Michel Boudet A, Duverger E, Grima-Pettenati J, Hawkins S (2002) The use of GUS histochemistry to visualise lignification gene expression in situ during wood formation. In: wood formation in trees-cell and molecular biology techniques, 1st edn. Taylor & Francis Inc, London, pp 271–295
Ramírez-Valdespino CA, Casas-Flores S, Olmedo-Monfil V (2019) Trichoderma as a model to study effector-like molecules. Front Microbiol 10:1030. https://doi.org/10.3389/fmicb.2019.01030
Ray S, Alves PCMSMS, Ahmad I, Gaffoor I, Acevedo FE, Peiffer M, Jin S, Han Y, Shakeel S, Felton GW, Luthe DS (2016) Turnabout is fair play: herbivory-induced plant chitinases excreted in fall armyworm frass suppress herbivore defences in maize. Plant Physiol 171:694–706. https://doi.org/10.1104/pp.15.01854
Rotblat B, Enshell-Seijffers D, Gershoni JM, Schuster S, Avni A (2002) Identification of an essential component of the elicitation active site of the EIX protein elicitor. Plant J 32:1049–1055. https://doi.org/10.1046/j.1365-313X.2002.01490.x
Salas-marina MA, Isordia-jasso MI, Islas-osuna MA, Delgado-sánchez P (2015) The Epl1 and Sm1 proteins from Trichoderma atroviride and Trichoderma virens differentially modulate systemic disease resistance against different life style pathogens in Solanum lycopersicum. Front Plant Sci 6:77. https://doi.org/10.3389/fpls.2015.00077
Segarra G, Casanova E, Avilés M, Trillas I (2010) Trichoderma asperellum strain T34 controls Fusarium wilt disease in tomato plants in soilless culture through competition for iron. Microb Ecol 59:141–149. https://doi.org/10.1007/s00248-009-9545-5
Shine MB, Xiao X, Kachroo P, Kachroo A (2019) Signaling mechanisms underlying systemic acquired resistance to microbial pathogens. Plant Sci 279:81–86. https://doi.org/10.1016/j.plantsci.2018.01.001
Shoresh M, Harman GE (2008) The molecular basis of shoot responses of maize seedlings to Trichoderma harzianum T22 inoculation of the root: a proteomic approach. Plant Physiol 147:2147–2163. https://doi.org/10.1104/pp.108.123810
Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43. https://doi.org/10.1146/annurev-phyto-073009-114450
Small CLN, Bidochka MJ (2005) Up-regulation of Pr1, a subtilisin-like protease, during conidiation in the insect pathogen Metarhizium anisopliae. Mycol Res 109:307–313. https://doi.org/10.1017/S0953756204001856
Sun Y, Li L, Macho AP, Han Z, Hu Z, Zipfel C, Zhou JM, Chai J, Complex FI, Zhifu H, Hu Z, Zhou JM (2013) Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342:624–628. https://doi.org/10.1126/science.1243825
Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194. https://doi.org/10.1046/j.1365-313X.1997.11061187.x
Torres MA, Jones JDG, Dangl JL (2006) Reactive oxygen species signalling in response to pathogens. Plant Physiol 141:373–378. https://doi.org/10.1104/pp.106.079467
Tucci M, Ruocco M, Masi LDE, Palma MDE, Lorito M (2011) The beneficial effect of Trichoderma spp. on tomato is modulated by the plant genotype. Mol Plant Pathol 12:341–354. https://doi.org/10.1111/J.1364-3703.2010.00674.X
Vinale F, Marra R, Scala F, Ghisalberti EL, Lorito M, Sivasithamparam K (2006) Major secondary metabolites produced by two commercial Trichoderma strains active against different phytopathogens. Lett Appl Microbiol 43:143–148. https://doi.org/10.1111/j.1472-765X.2006.01939.x
Viterbo A, Harel M, Chet I (2004) Isolation of two aspartyl proteases from expressed during colonization of cucumber roots.FEMS Microbiol Lett 238:151–158. https://doi.org/10.1111/j.1574-6968.2004.tb09750.x
Vitti A, Pellegrini E, Nali C, Lovelli S, Sofo A, Valerio M, Scopa A, Nuzzaci M (2016) Trichoderma harzianum T-22 induces systemic resistance in tomato infected by cucumber mosaic virus. Front Plant Sci 7:1520. https://doi.org/10.3389/fpls.2016.01520
Woloshuk CP, Shim WB (2013) Aflatoxins, fumonisins, and trichothecenes: a convergence of knowledge. FEMS Microbiol Rev 37:94–109. https://doi.org/10.1111/1574-6976.12009
Wu G, Liu Y, Xu Y, Zhang G, Shen Q, Zhang R (2018) Exploring elicitors of the beneficial rhizobacterium Bacillus amyloliquefaciens SQR9 to induce plant systemic resistance and their interactions with plant signalling pathways. Mol Plant-Microbe Interact 31:560–567. https://doi.org/10.1094/MPMI-11-17-0273-R
Zhang J, Bayram Akcapinar G, Atanasova L, Rahimi MJ, Przylucka A, Yang D, Kubicek CP, Zhang R, Shen Q, Druzhinina IS, Akcapinar GB, Atanasova L, Rahimi MJ, Przylucka A, Yang D, Kubicek CP, Zhang R, Shen Q, Druzhinina IS (2016) The neutral metallopeptidase NMP1 of Trichoderma guizhouense is required for mycotrophy and self-defence. Environ Microbiol 18:580–597. https://doi.org/10.1111/1462-2920.12966
Zhang J, Miao Y, Rahimi MJ, Zhu H, Steindorff A, Schiessler S, Cai F, Pang G, Chenthamara K, Xu Y, Kubicek CP, Shen Q, Druzhinina IS (2019) Guttation capsules containing hydrogen peroxide: an evolutionarily conserved NADPH oxidase gains a role in wars between related fungi. Environ Microbiol 21:2644–2658. https://doi.org/10.1111/1462-2920.14575
Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767. https://doi.org/10.1038/nature02485
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Luz E. de-Bashan.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Xu, Y., Zhang, J., Shao, J. et al. Extracellular proteins of Trichoderma guizhouense elicit an immune response in maize (Zea mays) plants. Plant Soil 449, 133–149 (2020). https://doi.org/10.1007/s11104-020-04435-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-020-04435-1