Tolerance and antioxidant response to heavy metals are differentially activated in Trichoderma asperellum and...

Heavy metal pollution reduces the community of soil microorganisms, including fungi from the genus Trichoderma, which are plant growth promotors and biological control agents. Because of potential effects on crop productivity, the toxic effects of heavy metals (HMs) in Trichoderma are of interest. However, there have been few studies on the biochemical and molecular response to oxidation caused by exposure to copper (Cu), chromium (Cr), and lead (Pb) and whether this antioxidant response is species-specific. In this study, we compared the tolerance of Trichoderma asperellum and Trichoderma longibrachiatum to Cu, Pb, and Cr and evaluated the expression of genes related to the antioxidant response, including glutathione peroxidase (GPX), catalase (CAT), and cysteine synthase (CYS) as well as the activity of peroxidase and catalase. The isolates of Trichoderma were selected because we previously reported them as promotors of plant growth and agents of biological control. Our results revealed that, with exposure to the three HMs, the Trichoderma cultures formed aggregates and the culture color changed according to the metal and the Trichoderma species. The tolerance index (TI) indicated that the two Trichoderma species were tolerant of HMs (Cu > Cr > Pb). However, the TI and conidia production revealed that T. longibrachiatum was more tolerant of HMs than T. asperellum. The three HMs caused oxidative damage in both Trichoderma species, but the enzyme activity and gene expression were differentially regulated based on exposure time (72 and 144 h) to the HMs and Trichoderma species. The main changes occurred in T. asperellum; the maximum expression of the GPX gene occurred at 144 h in response to all three HMs, whereas the CAT gene was upregulated at 72 h in response to Cu but downregulated at 144 h in response to all three HMs. The CYS gene was upregulated in response to the three metals. The peroxidase activity increased with all three HMs, but the catalase activity increased with Cu and Pb at 72 h and decreased at 144 h with Pb and Cr. In T. longibrachiatum, the GPX gene was upregulated with all three HMs at 72 h, the CAT gene was upregulated only with Pb at 72 h and was downregulated at 144 h with HMs. Cr and Cu upregulated CYS gene expression, but expression did not change with Pb. The peroxidase activity increased with Cu at 144 h and with Cr at 72 h, whereas Pb decreased the enzyme activity. In contrast, catalase activity increased with the three metals at 144 h. In conclusion, T. longibrachiatum was more tolerant of Cu, Cr, and Pb than was T. asperellum, but exposure to all three HMs caused oxidative damage to both Trichoderma species. Peroxidases and catalases were activated, and the expression of the genes GPX and CYS was upregulated, whereas the CAT gene was downregulated. These findings indicate that the antioxidant response to HMs was genetically modulated in each Trichoderma species.