Tolerance and antioxidant response to heavy metals are differentially activated in <i>Trichoderma asperellum</i> and <i>Trichoderma longibrachiatum</i>

Heavy metal pollution reduces the community of soil microorganisms, including fungi from the genus <i>Trichoderma</i>, which are plant growth promotors and biological control agents. Because of potential effects on crop productivity, the toxic effects of heavy metals (HMs) in <i>Trichoderma</i> 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 <i>Trichoderma asperellum</i> and <i>Trichoderma longibrachiatum</i> to Cu, Pb, and Cr and evaluated the expression of genes related to the antioxidant response, including glutathione peroxidase (<i>GPX</i>), catalase (<i>CAT</i>), and cysteine synthase (<i>CYS</i>) as well as the activity of peroxidase and catalase. The isolates of <i>Trichoderma</i> 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 <i>Trichoderma</i> cultures formed aggregates and the culture color changed according to the metal and the <i>Trichoderma</i> species. The tolerance index (TI) indicated that the two <i>Trichoderma</i> species were tolerant of HMs (Cu > Cr > Pb). However, the TI and conidia production revealed that <i>T. longibrachiatum</i> was more tolerant of HMs than <i>T. asperellum</i>. The three HMs caused oxidative damage in both <i>Trichoderma</i> species, but the enzyme activity and gene expression were differentially regulated based on exposure time (72 and 144 h) to the HMs and <i>Trichoderma</i> species. The main changes occurred in <i>T. asperellum</i>; the maximum expression of the <i>GPX</i> gene occurred at 144 h in response to all three HMs, whereas the <i>CAT</i> gene was upregulated at 72 h in response to Cu but downregulated at 144 h in response to all three HMs. The <i>CYS</i> 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 <i>T. longibrachiatum</i>, the <i>GPX</i> gene was upregulated with all three HMs at 72 h, the <i>CAT</i> gene was upregulated only with Pb at 72 h and was downregulated at 144 h with HMs. Cr and Cu upregulated <i>CYS</i> 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, <i>T. longibrachiatum</i> was more tolerant of Cu, Cr, and Pb than was <i>T. asperellum</i>, but exposure to all three HMs caused oxidative damage to both <i>Trichoderma</i> species. Peroxidases and catalases were activated, and the expression of the genes <i>GPX</i> and <i>CYS</i> was upregulated, whereas the <i>CAT</i> gene was downregulated. These findings indicate that the antioxidant response to HMs was genetically modulated in each <i>Trichoderma</i> species.