Differential Response of Tomato Plants to the Application of Three Trichoderma Species When Evaluating the Control of Pseudomonas syringae Populations
Abstract
:1. Introduction
2. Results and Discussion
2.1. Bacterial Population Sizes in Tomato Plants Are Defined by Trichoderma Species Specificity
2.2. Tomato Plants Challenged with Pst Strains Proved to Be Highly Synergistic in SA and JA Signaling Defense Pathways
2.3. Tomato Plants Challenged with Pst Strains under Different Trichoderma Treatments Display A Complex Defense-Related Gene and Plant Hormone Signaling Networks
3. Materials and Methods
3.1. Microorganisms and Tomato Seeds
3.2. Experimental Design and Plant Treatments
3.3. RNA Isolation, cDNA Synthesis and Real-Time Quantitative PCR (qRT-PCR)
3.4. Determination of L-Phenylalanine Ammonia-Lyase (PAL) Activity
3.5. Data Analysis
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
- Debbi, A.; Boureghda, H.; Monte, E.; Hermosa, R. Distribution and genetic variability of Fusarium oxysporum associated with tomato diseases in Algeria and a biocontrol strategy with indigenous Trichoderma spp. Front. Microbiol. 2018, 9, 282. [Google Scholar] [CrossRef] [Green Version]
- Lorito, M.; Woo, S.L.; Harman, G.E.; Monte, E. Translational research on Trichoderma: From ‘omics to the field. Annu. Rev. Phytopathol. 2010, 48, 395–417. [Google Scholar] [CrossRef] [Green Version]
- Coppola, M.; Cascone, P.; Chiusano, M.L.; Colantuono, C.; Lorito, M.; Pennacchio, F.; Rao, R.; Woo, S.L.; Guerrieri, E.; Digilio, M.C. Trichoderma harzianum enhances tomato indirect defense against aphids. Insect Sci. 2017, 24, 1025–1033. [Google Scholar] [CrossRef]
- Elsharkawy, M.M.; Shimizu, M.; Takahashi, H.; Ozaki, K.; Hyakumachi, M. Induction of systemic resistance against cucumber mosaic virus in Arabidopsis thaliana by Trichoderma asperellum SKT-1. Plant Pathol. J. 2013, 29, 193–200. [Google Scholar] [CrossRef] [Green Version]
- Medeiros, H.A.; De Araújo Filho, J.V.; De Freitas, L.G.; Castillo, P.; Rubio, M.B.; Hermosa, R.; Monte, E. Tomato progeny inherit resistance to the nematode Meloidogyne javanica linked to plant growth induced by the biocontrol fungus Trichoderma atroviride. Sci. Rep. 2017, 7, 40216. [Google Scholar] [CrossRef] [Green Version]
- Salas-Marina, M.A.; Isordia-Jasso, M.I.; Islas-Osuna, M.A.; Delgado-Sánchez, P.; Jiménez-Bremont, J.F.; Rodríguez-Kessler, M.; Rosales-Saavedra, M.T.; Herrera-Estrella, A.; Casas-Flores, S. 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. 2015, 6, 77. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Harman, G.E.; Howell, C.R.; Viterbo, A.; Chet, I.; Lorito, M. Trichoderma species—Opportunistic, avirulent plant symbionts. Nat. Rev. Microbiol. 2004, 2, 43–56. [Google Scholar] [CrossRef]
- Mukherjee, P.K.; Horwitz, B.A.; Herrera-Estrella, A.; Schmoll, M.; Kenerley, C.M. Trichoderma research in the genome era. Annu. Rev. Phytopathol. 2013, 51, 105–129. [Google Scholar] [CrossRef] [PubMed]
- Vinale, F.; Sivasithamparam, K.; Ghisalberti, E.L.; Marra, R.; Woo, S.L.; Lorito, M. Trichoderma–plant–pathogen interactions. Soil Biol. Biochem. 2008, 40, 1–10. [Google Scholar] [CrossRef]
- Hermosa, R.; Viterbo, A.; Chet, I.; Monte, E. Plant-beneficial effects of Trichoderma and of its genes. Microbiology 2012, 158, 17–25. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shoresh, M.; Harman, G.E.; Mastouri, F. Induced systemic resistance and plant responses to fungal biocontrol agents. Annu. Rev. Phytopathol. 2010, 48, 21–43. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Carrero-Carrón, I.; Rubio, M.B.; Niño-Sánchez, J.; Navas, J.A.; Jiménez-Díaz, R.M.; Monte, E.; Hermosa, R. Interactions between Trichoderma harzianum and defoliating Verticillium dahliae in resistant and susceptible wild olive clones. Plant Pathol. 2018, 67, 1758–1767. [Google Scholar] [CrossRef] [Green Version]
- Morán-Diez, E.; Hermosa, R.; Ambrosino, P.; Cardoza, R.E.; Gutiérrez, S.; Lorito, M.; Monte, E. The ThPG1 endopolygalacturonase is required for the Trichoderma harzianum–plant beneficial interaction. Mol. Plant-Microbe Interact. 2009, 22, 1021–1031. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pieterse, C.M.; Leon-Reyes, A.; Van der Ent, S.; Van Wees, S.C. Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 2009, 5, 308–316. [Google Scholar] [CrossRef] [Green Version]
- Gaffney, T.; Friedrich, L.; Vernooij, B.; Negrotto, D.; Nye, G.; Uknes, S.; Ward, E.; Kessmann, H.; Ryals, J. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 1993, 261, 754–756. [Google Scholar] [CrossRef]
- Van Wees, S.C.; Van der Ent, S.; Pieterse, C.M. Plant immune responses triggered by beneficial microbes. Curr. Opin. Plant Biol. 2008, 11, 443–448. [Google Scholar] [CrossRef] [Green Version]
- Pieterse, C.M.; Zamioudis, C.; Berendsen, R.L.; Weller, D.M.; Van Wees, S.C.; Bakker, P.A. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 2014, 52, 347–375. [Google Scholar] [CrossRef] [Green Version]
- Xin, X.F.; Kvitko, B.; He, S.Y. Pseudomonas syringae: What it takes to be a pathogen. Nat. Rev. Microbiol. 2018, 16, 316–328. [Google Scholar] [CrossRef]
- Bender, C.L.; Alarcón-Chaidez, F.; Gross, D.C. Pseudomonas syringae phytotoxins: Mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol. Mol. Biol. Rev. 1999, 63, 266–292. [Google Scholar] [CrossRef] [Green Version]
- Chini, A.; Fonseca, S.; Fernández, G.; Adie, B.; Chico, J.M.; Lorenzo, O.; García-Casado, J.; López-Vidriero, I.; Lozano, F.M.; Ponce, M.R.; et al. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 2007, 448, 666–671. [Google Scholar] [CrossRef]
- Kazan, K.; Manners, J.M. JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci. 2012, 17, 22–31. [Google Scholar] [CrossRef] [PubMed]
- Xin, X.F.; He, S.Y. Pseudomonas syringae pv. tomato DC3000: A model pathogen for probing disease susceptibility and hormone signaling in plants. Annu. Rev. Phytopathol. 2013, 51, 473–498. [Google Scholar] [CrossRef] [PubMed]
- Kloek, A.P.; Verbsky, M.L.; Sharma, S.B.; Schoelz, J.E.; Vogel, J.; Klessig, D.F.; Kunkel, B.N. Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coi1) mutation occurs through two distinct mechanisms. Plant J. 2001, 26, 509–522. [Google Scholar] [CrossRef] [PubMed]
- De Torres Zabala, M.; Bennett, M.H.; Truman, W.H.; Grant, M.R. Antagonism between salicylic and abscisic acid reflects early host–pathogen conflict and moulds plant defence responses. Plant J. 2009, 59, 375–386. [Google Scholar] [CrossRef]
- Mur, L.A.; Kenton, P.; Atzorn, R.; Miersch, O.; Wasternack, C. The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol. 2006, 140, 249–262. [Google Scholar] [CrossRef] [Green Version]
- Truman, W.; Bennett, M.H.; Kubiqsteltig, I.; Turnbull, C.; Grant, M. Arabidopsis systemic immunity used conserved defense signaling pathways and is mediated by jasmonates. Proc. Natl. Acad. Sci. USA 2007, 16, 1075–1080. [Google Scholar] [CrossRef] [Green Version]
- De Torres Zabala, M.; Zhai, B.; Jayaraman, S.; Eleftheriadou, G.; Winsbury, R.; Yang, R.; Truman, W.; Tang, S.; Smirnoff, N.; Grant, M. Novel JAZ co-operativity and unexpected JA dynamics underpin Arabidopsis defence responses to Pseudomonas syringae infection. New Phytol. 2016, 209, 1120–1134. [Google Scholar] [CrossRef] [Green Version]
- Joardar, V.; Lindeberg, M.; Jackson, R.W.; Selengut, J.; Dodson, R.; Brinkac, L.M.; Daugherty, S.C.; DeBoy, R.; Durkin, A.S.; Giglio, M.G.; et al. Whole-genome sequence analysis of Pseudomonas syringae pv. phaseolicola 1448A reveals divergence among pathovars in genes involved in virulence and transposition. J. Bacteriol. 2005, 187, 6488–6498. [Google Scholar] [CrossRef] [Green Version]
- Mendoza-Mendoza, A.; Zaid, R.; Lawry, R.; Hermosa, R.; Monte, E.; Horwitz, B.A.; Mukherjee, P.K. Molecular dialogues between Trichoderma and roots: Role of the fungal secretome. Fungal Biol. Rev. 2018, 32, 62–85. [Google Scholar] [CrossRef]
- Shoresh, M.; Yedidia, I.; Chet, I. Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology 2005, 95, 76–84. [Google Scholar] [CrossRef] [Green Version]
- Korolev, N.; David, D.R.; Elad, Y. The role of phytohormones in basal resistance and Trichoderma-induced systemic resistance to Botrytis cinerea in Arabidopsis thaliana. BioControl 2008, 53, 667–683. [Google Scholar] [CrossRef]
- Brotman, Y.; Landau, U.; Cuadros-Inostroza, A.; Yakayuki, T.; Fernie, A.R.; Chet, I.; Viterbo, A.; Willmitzer, L. Trichoderma-plant root colonization: Escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance. PLoS Pathog. 2013, 9, 1003221. [Google Scholar] [CrossRef]
- Segarra, G.; Casanova, E.; Bellido, D.; Odena, M.A.; Oliveira, E.; Trillas, I. Proteome, salicylic acid, and jasmonic acid changes in cucumber plants inoculated with Trichoderma asperellum strain T34. Proteomics 2007, 7, 3943–3952. [Google Scholar] [CrossRef] [PubMed]
- Martínez-Medina, A.; Fernández, I.; Sánchez-Guzmán, M.J.; Jung, S.C.; Pascua, J.A.; Pozo, M.J. Deciphering the hormonal signalling network behind the systemic resistance induced by Trichoderma harzianum in tomato. Front. Plant Sci. 2013, 4, 206. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mathys, J.; De Cremer, K.; Timmermans, P.; Van Kerkhove, S.; Lievens, B.; Vanhaecke, M.; Cammue, B.; De Coninck, B. Genome-wide characterization of ISR induced in Arabidopsis thaliana by Trichoderma hamatum T382 against Botrytis cinerea infection. Front. Plant Sci. 2012, 3, 108. [Google Scholar] [CrossRef] [Green Version]
- Salas-Marina, M.A.; Silva-Flores, M.A.; Uresti-Rivera, E.E.; Castro-Longoria, E.; Herrera-Estrella, A.; Casas-Flores, S. Colonization of Arabidopsis roots by Trichoderma atroviride promotes growth and enhances systemic disease resistance through jasmonic acid/ethylene and salicylic acid pathways. Eur. J. Plant Pathol. 2011, 131, 15–26. [Google Scholar] [CrossRef]
- Tucci, M.; Ruocco, M.; De Masi, L.; De Palma, M.; Lorito, M. The beneficial effect of Trichoderma spp. on tomato is modulated by the plant genotype. Mol. Plant Pathol. 2011, 12, 341–354. [Google Scholar] [CrossRef]
- Contreras-Cornejo, H.A.; Macías-Rodríguez, L.; Cortés-Penagos, C.; López-Bucio, J. Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol. 2009, 149, 1579–1592. [Google Scholar] [CrossRef] [Green Version]
- Pérez, E.; Rubio, M.B.; Cardoza, R.E.; Gutiérrez, S.; Bettiol, W.; Monte, E.; Hermosa, R. The importance of chorismate mutase in the biocontrol potential of Trichoderma parareesei. Front. Microbiol. 2015, 6, 1181. [Google Scholar] [CrossRef] [Green Version]
- Yuan, M.; Huang, Y.; Ge, W.; Jia, Z.; Song, S.; Zhang, L.; Huang, Y. Involvement of jasmonic acid, ethylene and salicylic acid signaling pathways behind the systemic resistance induced by Trichoderma longibrachiatum H9 in cucumber. BMC Genom. 2019, 20, 144. [Google Scholar] [CrossRef] [Green Version]
- Viterbo, A.; Landau, U.; Kim, S.; Chernin, L.; Chet, I. Characterization of ACC deaminase from the biocontrol and plant growth-promoting agent Trichoderma asperellum T203. FEMS Microbiol. Lett. 2010, 305, 42–48. [Google Scholar] [CrossRef] [PubMed]
- Martínez-Medina, A.; Fernandez, I.; Lok, G.B.; Pozo, M.J.; Pieterse, C.M.; Van Wees, S. Shifting from priming of salicylic acid-to jasmonic acid-regulated defences by Trichoderma protects tomato against the root knot nematode Meloidogyne incognita. New Phytol. 2017, 213, 1363–1377. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yedidia, I.; Shoresh, M.; Kerem, Z.; Benhamou, N.; Kapulnik, Y.; Chet, I. Concomitant induction of systemic resistance to Pseudomonas syringae pv. lachrymans in cucumber by Trichoderma asperellum (T-203) and accumulation of phytoalexins. Appl. Environ. Microbiol. 2003, 69, 7343–7353. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brotman, Y.; Lisec, J.; Méret, M.; Chet, Y.; Willmitzer, L.; Viterbo, A. Transcript and metabolite analysis of the Trichoderma-induced systemic resistance response to Pseudomonas syringae in Arabidopsis thaliana. Microbiology 2012, 158, 139–146. [Google Scholar] [CrossRef] [Green Version]
- Rubio, M.B.; Quijada, N.M.; Pérez, E.; Domínguez, S.; Monte, E.; Hermosa, R. Identifying beneficial qualities of Trichoderma parareesei for plants. Appl. Environ. Microbiol. 2014, 80, 1864–1873. [Google Scholar] [CrossRef] [Green Version]
- Rubio, M.B.; Hermosa, R.; Vicente, R.; Gómez-Acosta, F.A.; Morcuende, R.; Monte, E.; Bettiol, W. The combination of Trichoderma harzianum and chemical fertilization leads to the deregulation of phytohormone networking, preventing the adaptive responses of tomato plants to salt stress. Front. Plant Sci. 2017, 8, 294. [Google Scholar] [CrossRef] [Green Version]
- Chowdappa, P.; Kumar, S.M.; Lakshmi, M.J.; Upreti, K.K. Growth stimulation and induction of systemic resistance in tomato against early and late blight by Bacillus subtilis OTPB1 or Trichoderma harzianum OTPB3. Biol. Control 2013, 65, 109–117. [Google Scholar] [CrossRef]
- Nieto-Jacobo, M.F.; Steyaert, J.M.; Salazar-Badillo, F.B.; Nguyen, D.V.; Rostás, M.; Braithwaite, M.; De Souza, J.T.; Jimenez-Bremont, J.F.; Ohkura, M.; Stewart, A.; et al. Environmental growth conditions of Trichoderma spp. affects indole acetic acid derivatives, volatile organic compounds, and plant growth promotion. Front. Plant Sci. 2017, 8, 102. [Google Scholar] [CrossRef] [Green Version]
- Shukla, N.; Awasthi, R.P.; Rawat, L.; Kumar, J. Seed biopriming with drought tolerant isolates of Trichoderma harzianum promote growth and drought tolerance in Triticum aestivum. Ann. Appl. Biol. 2015, 166, 171–182. [Google Scholar] [CrossRef]
- Singh, V.; Upadhyay, R.S.; Sarma, B.K.; Singh, H.B. Trichoderma asperellum spore dose depended modulation of plant growth in vegetable crops. Microbiol. Res. 2016, 193, 74–86. [Google Scholar] [CrossRef]
- Zhang, S.; Gan, Y.; Xu, B. Application of plant-growth-promoting fungi Trichoderma longibrachiatum T6 enhances tolerance of wheat to salt stress through improvement of antioxidative defense system and gene expression. Front. Plant Sci. 2016, 7, 1405. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brooks, D.M.; Hernández-Guzmán, G.; Kloek, A.P.; Alarcón-Chaidez, F.; Sreedharan, A.; Rangaswamy, V.; Peñaloza-Vázquez, A.; Bender, C.L.; Kunkel, B.N. Identification and characterization of a well-defined series of coronatine biosynthetic mutants of Pseudomonas syringae pv. tomato DC3000. Mol. Plant-Microbe Interact. 2004, 17, 162–174. [Google Scholar] [CrossRef] [Green Version]
- Panchal, S.; Roy, D.; Chitrakar, R.; Price, L.; Breitbach, Z.S.; Armstrong, D.W.; Melotto, M. Coronatine facilitates Pseudomonas syringae infection of Arabidopsis leaves at night. Front. Plant Sci. 2016, 7, 880. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tsai, C.H.; Singh, P.; Chen, C.W.; Thomas, J.; Weber, J.; Mauch-Mani, B.; Zimmerli, L. Priming for enhanced defence responses by specific inhibition of the Arabidopsis response to coronatine. Plant J. 2011, 65, 469–479. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Geng, X.; Jin, L.; Shimada, M.; Kim, M.G.; Mackey, D. The phytotoxin coronatine is a multifunctional component of the virulence armament of Pseudomonas syringae. Planta 2014, 240, 1149–1165. [Google Scholar] [CrossRef] [Green Version]
- Uppalapati, S.R.; Ishiga, Y.; Wangdi, T.; Kunkel, B.N.; Anand, A.; Mysore, K.S.; Bender, C.L. The phytotoxin coronatine contributes to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato inoculated with Pseudomonas syringae pv. tomato DC3000. Mol. Plant-Microbe Interact. 2007, 20, 955–965. [Google Scholar] [CrossRef] [Green Version]
- Pieterse, C.M.; Van der Does, D.; Zamioudis, C.; León-Reyes, A.; Van Wees, S.C. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 2012, 28, 489–521. [Google Scholar] [CrossRef] [Green Version]
- Moura, J.C.M.S.; Bonine, C.A.V.; Viana, J.O.F.; Dornelas, M.C.; Mazzafera, P. Abiotic and biotic stresses and changes in the lignin content and composition in plants. J. Integr. Plant Biol. 2010, 52, 360–376. [Google Scholar] [CrossRef]
- Lee, M.J.; Jeon, H.S.; Kim, S.H.; Chung, J.H.; Roppolo, D.; Lee, H.J.; Cho, H.J.; Tobimatsu, Y.; Ralph, J.; Park, O.K. Lignin-based barrier restricts pathogens to the infection site and confers resistance in plants. EMBO J. 2019, 38, e101948. [Google Scholar] [CrossRef]
- Chen, G.; Escobar-Bravo, R.; Kim, H.K.; Leiss, K.A.; Klinkhamer, P.G. Induced resistance against western flower thrips by the Pseudomonas syringae-derived defense elicitors in tomato. Front. Plant Sci. 2018, 9, 1417. [Google Scholar] [CrossRef]
- Derksen, H.; Rampitsch, C.; Daayf, F. Signaling cross-talk in plant disease resistance. Plant Sci. 2013, 207, 79–87. [Google Scholar] [CrossRef] [PubMed]
- Zheng, X.Y.; Spivey, N.W.; Zeng, W.; Liu, P.P.; Fu, Z.Q.; Klessig, D.F.; He, S.Y.; Dong, X. Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 2012, 11, 587–596. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Berrocal-Lobo, M.; Molina, A.; Solano, R. Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J. 2002, 29, 23–32. [Google Scholar] [CrossRef] [PubMed]
- Gimenez-Ibañez, S.; Solano, R. Nuclear jasmonate and salicylate signaling and crosstalk in defense against pathogens. Front. Plant Sci. 2013, 4, 72. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hermosa, M.R.; Grondona, I.; Iturriaga, E.T.; Díaz-Mínguez, J.M.; Castro, C.; Monte, E.; García-Acha, I. Molecular characterization and identification of biocontrol isolates of Trichoderma spp. Appl. Environ. Microbiol. 2000, 66, 1890–1898. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bashan, Y.; de-Bashan, L.E. Protection of tomato seedlings against infection by Pseudomonas syringae pv. tomato by using the plant growth-promoting bacterium Azospirillum brasilense. Appl. Environ. Microbiol. 2002, 68, 2637–2643. [Google Scholar] [CrossRef] [Green Version]
- Malmierca, M.G.; Barua, J.; McCormick, S.P.; Izquierdo-Bueno, I.; Cardoza, R.E.; Alexander, N.J.; Hermosa, R.; Collado, I.G.; Monte, E.; Gutiérrez, S. Novel aspinolides production by Trichoderma arundinaceum with a potential role in Botrytis cinerea antagonistic activity and plant defence priming. Environ. Microbiol. 2015, 17, 1103–1118. [Google Scholar] [CrossRef]
- Schmittgen, T.D.; Livak, K.J. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 2008, 3, 1101–1108. [Google Scholar] [CrossRef]
- Lee, J.; Lee, D.G.; Park, J.Y.; Chae, S.; Lee, S. Analysis of the trans-cinnamic acid content in Cinnamomum spp. and commercial cinnamon powder using HPLC. J. Agric. Chem. Environ. 2015, 4, 102. [Google Scholar]
- R Development Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Analysis: Vienna, Asutria, 2005. [Google Scholar]
- Ferreira, E.B.; Cavalcanti, P.P.; Nogueira, D.A. ExpDes.pt: Experimental Designs Package R Package Version (1.1.2). 2013. Available online: https://cran.r-project.org/web/packages/ExpDes/index.html (accessed on 5 May 2020).
- Warnes, G.R.; Bolker, B.; Bonebakker, L.; Gentleman, R.; Liaw, W.H.A.; Lumley, T.; Maechler, M.; Magnusson, A.; Moeller, S.; Schwartz, M.; et al. Gplots: Various R Programming Tools for Plotting Data. 2019. Available online: http://cran.r-project.org/web/packages/gplots/index.html (accessed on 5 May 2020).
Treatment | DC3000 | DC3118 | ||
---|---|---|---|---|
BP | DS b | BP | DS | |
Control a | 6.24 b * A ** | 3 a A | 5.80 a B | 2 a B |
T6 | 6.19 b A (0.8%) *** | 3 a A | 2.05 c B (64.7%) | 1 a B |
T25 | 5.65 c A (9.4%) | 3 a A | 2.11 c B (63.6%) | 1 a B |
T34 | 6.48 a A (−3.8%) | 3 a A | 4.80 b B (17.3%) | 1 a B |
Treatment | Dry Biomass (g/Plant) a | Height (cm) |
---|---|---|
Control | 0.50 a * | 13.65 a |
T6 | 0.44 a | 16.42 a |
T25 | 0.41 a | 14.61 a |
T34 | 0.45 a | 15.92 a |
Treatment | Control | DC3000 | DC3118 |
---|---|---|---|
Control | 173.55 abc * | 257.89 c | 177.35 abc |
T6 | 115.07 a | 209.59 bc | 197.28 abc |
T25 | 125.17 ab | 188.34 abc | 136.95 ab |
T34 | 160.97 abc | 213.86 bc | 259.16 c |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Morán-Diez, M.E.; Tranque, E.; Bettiol, W.; Monte, E.; Hermosa, R. Differential Response of Tomato Plants to the Application of Three Trichoderma Species When Evaluating the Control of Pseudomonas syringae Populations. Plants 2020, 9, 626. https://doi.org/10.3390/plants9050626
Morán-Diez ME, Tranque E, Bettiol W, Monte E, Hermosa R. Differential Response of Tomato Plants to the Application of Three Trichoderma Species When Evaluating the Control of Pseudomonas syringae Populations. Plants. 2020; 9(5):626. https://doi.org/10.3390/plants9050626
Chicago/Turabian StyleMorán-Diez, María E., Eduardo Tranque, Wagner Bettiol, Enrique Monte, and Rosa Hermosa. 2020. "Differential Response of Tomato Plants to the Application of Three Trichoderma Species When Evaluating the Control of Pseudomonas syringae Populations" Plants 9, no. 5: 626. https://doi.org/10.3390/plants9050626