Muscodor spp.: promotes tomato growth, protects against bacterial wilt and produces bioactive volatile compounds

Abstract

Several endophytic fungi are producers of metabolites with antimicrobial activity. In addition, they interact with higher plants and can perform several indispensable functions in nature, such as growth promotion and protection against diseases. Of these, fungi of the genus Muscodor have been reported as producers of a mixture of lethal volatile organic compounds (VOCs) against a wide amount of microorganisms, in addition to improving the development of some plants. However, the application of fungi of this genus in agriculture has the challenge of non-sporulation. Therefore, aimed to explore the potential of nine isolates of three species of Muscodor (M. vitigenus, M. coffeanum and M. yucatanensis) we evaluated the in vitro activity of their VOCs against the phytobacteria Ralstonia solanacearum race 3, Xanthomas vesicatoria and Pseudomonas syringae pv. tomato, with subsequent characterization of the volatiles produced by gas chromatography-mass spectrometry (GCMS). Allelopathy of volatiles on tomato radicles was also evaluated. Two methods of inoculation were tested in tomato, in seedling, in two independent experiments, with mycelium suspension, and seed, through adaptations in the water restriction technique, in which growth promotion was evaluated, as well as plant resistance, inoculated in seed, to bacterial wilt caused by R. solanacearum race 3, respectively. Several isolates of different species produced volatiles with antibacterial and allelopathic activity, especially the VOCs of the fungus M. coffeanum COAD1900, with a lethal effect against all phytobacteria, except P. syringae that grew partially, and phytoinhibition from the second day of growth. After eight days of growth, 18 VOCs were characterized, among them: acids; esters; alcohols; terpenes; aldehyde and amide. The inoculation with mycelial suspension of five fungi increased the yield of fresh fruits of tomato in the two experiments, with the highest gains promoted by the fungi M. coffeanum COAD1842 (20%), M. vitigenus CML4015 (19%) and M. vitigenus CML4014 (15%). Dry biomass gains of root and shoot were observed only in the second experiment, carried out in winter. Osmoconditioning proved to be an effective inoculation technique for Muscodor fungi, promoting effective seed colonization without damage to fungus growth. However, some isolates affected negatively the germination, height and the shoot/root ratio of the seedlings. On the other hand, M. coffeanum COAD1842 and M. yucatanensis CML4016 significantly increased the dry biomass of the roots, in addition to the seedlings presented lower shoot/root ratio than the control. Tomato for industry inoculated with M. coffeanum COAD1900 showed moderate resistance to bacterial wilt, besides an increase in fresh fruit yield and total soluble solids content. The observation of radicle colonization suggests the ability of colonization of Muscodor fungi in tomato roots. In addition, the fungi M. coffeanum COAD1842 and M. yucatanensis CML416 showed compatibility with the seed treatment (metalaxyl+deltamethrin). Our results reinforce the potential of using Muscodor fungi in the tomato crop, with the development of application strategies in seedling and seed aiming the plant development and control of bacterial wilt.