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Trichoderma and bradyrhizobia act synergistically and enhance the growth rate, biomass and photosynthetic pigments of cowpea (Vigna unguiculata) grown in controlled conditions

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Abstract

Trichoderma exhibits great ecological and agricultural relevance because it improves plant growth, development and productivity. In this study, Trichoderma isolates (T01, T02, T04, T74, T76 and T96 of T. asperelloides; T77 of T. asperellum; or T44, T78 and T92 of T. harzianum) were evaluated in vitro for their ability to solubilize phosphate and produce indole-3-acetic acid (IAA). Afterwards, a completely randomized experimental design with 12 treatments was used to investigate physiological changes in cowpea plants inoculated with Bradyrhizobium sp. BR 3267 (bradyrhizobia) or coinoculated with bradyrhizobia and those Trichoderma isolates in the greenhouse conditions. All Trichoderma isolates showed the ability to solubilize phosphate and to produce IAA. Cowpeas were positively influenced by coinoculation with bradyrhizobia and Trichoderma, with the highlight being cowpea plants coinoculated with bradyrhizobia and T. asperelloides T02. These plants display significant increases in height; relative growth rate; stem diameter; dry weight of shoots, roots and nodules; total dry weight; and specific root length in relation to other symbiotic pairs and absolute control. In contrast, negative responses were registered in cowpea plants coinoculated with bradyrhizobia and T. asperelloides T04, bradyrhizobia and T. harzianum T44 or bradyrhizobia and T. harzianum T92. These plants, together with the absolute control, display lower values of stem diameter, total dry weight, specific root length, and total chlorophyll and carotenoids; the absence of root nodules; and a higher root length and anthocyanin content in relation to other treatments. Our hypothesis is that the increase in root length may be related to IAA produced by Trichoderma, while anthocyanin accumulation is associated with nitrogen deficiency, suggesting that these plants are under stress. To our knowledge, this is the first evidence of antagonistic relationships between bradyrhizobia and Trichoderma in the cowpea rhizosphere. Our findings demonstrated that Trichoderma promotes positive effects on cowpeas nodulated by bradyrhizobia and acts as stimulators of plant growth, but an adequate microbial consortium of bradyrhizobia-Trichoderma could represent a promising practical method for increasing the productivity of cowpea and other legumes.

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References

  • Alcántara C, Thornton CR, Pérez-de-Luque A, Le Cocq K, Pedraza V, Murray PJ (2016) The free-living rhizosphere fungus Trichoderma hamatum GD12 enhances clover productivity in clover-ryegrass mixtures. Plant Soil 398:165–180

    Google Scholar 

  • Babu S, Prasanna R, Bidyarani N, Nain L, Shivay YS (2015) Synergistic action of PGP agents and Rhizobium spp. for improved plant growth, nutrient mobilization and yields in different leguminous crops. Biocatal Agric Biotechnol 4(4):456–464

    Google Scholar 

  • Badar R, Qureshi SA (2012) Comparative effect of Trichoderma hamatum and host-specific Rhizobium species on growth of Vigna mungo. J Appl Pharm Sci 2(4):128–132

    Google Scholar 

  • Bremner JM (1965) Total nitrogen. In: black CA. Methods of soil analysis chemical and microbiological properties. Madison: American Society of Agronomy, Part 2:1149–1178

    Google Scholar 

  • Carvalho Filho MR (2013) Identification and phylogenetic relationships, potential use of Trichoderma isolates in the control of white mold and as growth promoters of common bean. PhD Thesis (Doctor in Phytopathology), University of Brasília, Brasília, Brazil, 123 p

  • Chagas LF, Chagas Junior AF, Fidelis RR, Carvalho Filho MR, Miller LO (2017) Trichoderma asperellum efficiency in soybean yield components. Com Sci 8(1):165–169

    CAS  Google Scholar 

  • Chen SC, Zhao HJ, Wang ZH, Zheng CX, Zhao PY, Guan ZH, Qin HY, Liu AR, Lin XM, Ahammed GJ (2017) Trichoderma harzianum-induced resistance against Fusarium oxysporum involves regulation of nuclear DNA content, cell viability and cell cycle-related genes expression in cucumber roots. Eur J Plant Pathol 147:43–53

    CAS  Google Scholar 

  • Das T, Mahapatra S, Das S (2017) In vitro compatibility study between the Rhizobium and native Trichoderma isolates from lentil rhizospheric soil. Int J Curr Microbiol App Sci 6(8):1757–1769

    Google Scholar 

  • Divito GA, Sadras VO (2014) How do phosphorus, potassium and Sulphur affect plant growth and biological nitrogen fixation in crop and pasture legumes? A meta-analysis. Field Crops Res 156:161–171

    Google Scholar 

  • Domínguez S, Rubio MB, Cardoza RE, Gutiérrez S, Nicolás C, Bettiol W, Hermosa R, Monte E (2016) Nitrogen metabolism and growth enhancement in tomato plants challenged with Trichoderma harzianum expressing the Aspergillus nidulans Acetamidase amdS gene. Front Microbiol 7:1182

    PubMed  PubMed Central  Google Scholar 

  • Edi-Premono M, Moawad AM, Vleck PLG (1996) Effect of phosphate solubilizing Pseudomonas putida on the growth of maize and its survival in the rhizosphere. Indones J Crop Sci 11:13–23

    Google Scholar 

  • Eissenstat DM (1991) On the relationship between specific root length and the rate of root proliferation: a field study using citrus rootstocks. New Phytol 118(1):63–68

    Google Scholar 

  • Ekundayo EA, Ekundayo FO, Osinowo IA (2015) Antifungal activities of Trichoderma viride and two fungicides in controlling diseases caused by Sclerotium rolfsii on tomato plants. Adv Appl Sci Res 6:12–19

    CAS  Google Scholar 

  • Evans JSB (1972) Interpretation and matching bias in a reasoning task. Q J Exp Psychol 24(2):193–199

    Google Scholar 

  • Ferrigo D, Raiola A, Piccolo E, Scopel C, Causin R (2014) Trichoderma harzianum T22 induces in maize systemic resistance against Fusarium verticillioides. J Plant Pathol 96:133–142

    Google Scholar 

  • Figueiredo MVB, Bonifacio A, Rodrigues AC, Araujo FF (2016) Plant growth-promoting rhizobacteria: key mechanisms of action. Choudhary DK, Varma A Microbial-mediated induced systemic resistance in plants 1 ed Singapore: Springer 1:23–37

    Google Scholar 

  • Gitelson AA, Merzlyak MN, Chivkunova OB (2011) Optical properties and nondestructive estimation of anthocyanin content in plant leaves. Photochem Photobiol 74(1):38–45

    Google Scholar 

  • Glickmann E, Dessaux Y (1995) A critical examination of the specificity of the Salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 61:793–796

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gordon SA, Weber RP (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26(1):192–195

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hermosa R, Rubio MB, Cardoza RE, Nicolás C, Monte E, Gutiérrez S (2013) The contribution of Trichoderma to balancing the costs of plant growth and defense. Int Microbiol 16(2):69–80

    CAS  PubMed  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soils. California Agricultural Experimental Station, Berkeley, 347 p

    Google Scholar 

  • Jagadeesh V, Patta S, Triveni S, Keshavulu K, Rani KJ, Raghavendra K (2017) Effect of biological seed coating on pigeon pea seedling vigour. Int J Curr Microbiol App Sci 6(8):843–854

    Google Scholar 

  • Jayaraj J, Ramabadran R (1999) Rhizobium-Trichoderma interaction in vitro and in vivo. Indian Phytopath 52(2):190–192

    Google Scholar 

  • Kitajima K, Hogan KP (2003) Increases of chlorophyll a/b ratios during acclimation of tropical woody seedlings to nitrogen limitation and high light. Plant Cell Environ 26(6):857–865

    PubMed  Google Scholar 

  • Kitson RE, Mellon MG (1944) Colorimetric determination of phosphorus as molybdivanado and phosphoric acid. Ind Eng Chem 16(6):379–383

    CAS  Google Scholar 

  • Kovinich N, Kayanja G, Chanoca A, Otegui MS, Grotewold E (2015) Abiotic stresses induce different localizations of anthocyanins in Arabidopsis. Plant Signal Behav 10(7):e1027850

    PubMed  PubMed Central  Google Scholar 

  • Kucuk C, Cevheri C (2015) In vitro antagonism of Rhizobium strains isolated from various legumes. J Pure Appl Microbio 9:503–511

    Google Scholar 

  • Li RX, Cai F, Pang G, Shen QR, Li R, Chen W (2015) Solubilization of phosphate and micronutrients by Trichoderma harzianum and its relationship with the promotion of tomato plant growth. PLoS One 10(6):e0130081

    PubMed  PubMed Central  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592

    CAS  Google Scholar 

  • López-Bucio J, Pelagio-Flores R, Herrera-Estrella A (2015) Trichoderma as biostimulants: exploiting the multilevel properties of a plant beneficial fungus. Sci Hortic 196:109–123

    Google Scholar 

  • Martins D, Macovei A, Leonetti P, Balestrazzi A, Araújo S (2017) The influence of phosphate deficiency on legume symbiotic N2 fixation. In: Sulieman S, Tran LSP. Legume nitrogen fixation in soils with low phosphorus availability: adaptation and regulatory implication. Cham: springer. Chapter 3:41–75

    Google Scholar 

  • Mishra N, Khan SS, Sundari SK (2016) Native isolate of Trichoderma: a biocontrol agent with unique stress tolerance properties. World J Microbiol Biotechnol 32:130

    CAS  PubMed  Google Scholar 

  • Mweetwa AM, Chilombo G, Gondwe BM (2016) Nodulation, nutrient uptake and yield of common bean inoculated with Bradyrhizobia and Trichoderma in an acid soil. J Agric Sci 9(12):61

    Google Scholar 

  • Nopparat C, Jatupornpipat M, Rittiboon A (2007) Isolation of phosphate solubilizing fungi in soil from Kanchanaburi, Thailand. KMITL Sci Tech J 7(S2):137–146

    Google Scholar 

  • Pereira JL, Queiroz RML, Charneau SO, Felix CR, Ricart CAO, Silva FL, Steindorff AS, Ulhoa C, Noronha EF (2014) Analysis of Phaseolus vulgaris response to its association with Trichoderma harzianum (ALL-42) in the presence or absence of the phytopathogenic Fungi Rhizoctonia solani and Fusarium solani. PLoS One 9(5):e98234

    PubMed  PubMed Central  Google Scholar 

  • Pineda MEB (2014) Phosphate solubilization as a microbial strategy for promoting plant growth. Corpoica Cienc Tecnol Agropecu 15(1):101–113

    Google Scholar 

  • Ponmurugan P, Gopi C (2006) In vitro production of growth regulators and phosphatase activity by phosphate solubilizing bacteria. Afr J Biotechnol 5(4):348–350

    CAS  Google Scholar 

  • Rego FA, Diop I, Sadio O, Sylva MC, Agbangba CE, Touré O, Wade TK (2015) Response of cowpea to symbiotic microorganisms inoculation (Arbuscular mycorrhizal fungi and Rhizobium) in cultivated soils in Senegal. Univers J Plant Sci 3(2):32–42

    Google Scholar 

  • Rodrigues AC, Vendruscolo CT, Moreira AS, Santana MVS, Oliveira JP, Bonifacio A, Figueiredo MVB (2015) Rhizobium tropici exopolysaccharides as carriers improve the symbiosis of cowpea-Bradyrhizobium-Paenibacillus. Afr J Microbiol Res 9(37):2037–2050

    CAS  Google Scholar 

  • Rubio MB, Hermosa R, Vicente R, Gómez-Acosta FA, Morcuende R, Monte E, Bettiol W (2017) 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 8:294

    CAS  PubMed  PubMed Central  Google Scholar 

  • Silva FAS, Azevedo CAV (2016) The Assistat software version 7.7 and its use in the analysis of experimental data. Afr J Agric Res 11(39):3733–3740

    Google Scholar 

  • Silveira JAG, Contado J, Rodrigues J, Oliveira JT (1998) Phosphoenolpyruvate carboxylase and glutamine synthetase activities in relation to nitrogen fixation in cowpea nodules. Braz J Plant Physiol 10:19–23

    Google Scholar 

  • Venturi V, Keel C (2016) Signaling in the rhizosphere. Trends Plant Sci 21(3):187–198

    CAS  PubMed  Google Scholar 

  • Zhao L, Zhang Y (2015) Effects of phosphate solubilization and phytohormone production of Trichoderma asperellum Q1 on promoting cucumber growth under salt stress. J Integr Agr 14(8):1588–1597

    CAS  Google Scholar 

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Acknowledgements

The authors are grateful to the National Council for Scientific and Technological Development (CNPq) and National Council for the Improvement of Higher Education (CAPES), Brazilian research-funding agencies, for financial support.

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Correspondence to Aurenivia Bonifacio.

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Highlights

• Adequate microbial consortium with Trichoderma may increase legume productivity.

T. asperelloides T02 induces positive responses on cowpea nodulated by bradyrhizobia.

• The in vivo synergism among bradyrhizobia and Trichoderma is reported.

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Mendes, J.B.S., da Costa Neto, V.P., de Sousa, C.D.A. et al. Trichoderma and bradyrhizobia act synergistically and enhance the growth rate, biomass and photosynthetic pigments of cowpea (Vigna unguiculata) grown in controlled conditions. Symbiosis 80, 133–143 (2020). https://doi.org/10.1007/s13199-019-00662-y

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  • DOI: https://doi.org/10.1007/s13199-019-00662-y

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