Mechanistic assessment of tolerance to iron deficiency mediated by Trichoderma harzianum in soybean roots

J Appl Microbiol. 2022 Nov;133(5):2760-2778. doi: 10.1111/jam.15651. Epub 2022 Jun 14.

Abstract

Aims: Iron (Fe) deficiency in soil is a continuing problem for soybean (Glycine max L.) production, partly as a result of continuing climate change. This study elucidates how Trichoderma harzianum strain T22 (TH) mitigates growth retardation associated with Fe-deficiency in a highly sensitive soybean cultivar.

Methods and results: Soil TH supplementation led to mycelial colonization and the presence of UAOX1 gene in roots that caused substantial improvement in chlorophyll score, photosynthetic efficiency and morphological parameters, indicating a positive influence on soybean health. Although rhizosphere acidification was found to be a common feature of Fe-deficient soybean, the upregulation of Fe-reductase activity (GmFRO2) and total phenol secretion were two of the mechanisms that substantially increased the Fe availability by TH. Heat-killed TH applied to soil caused no improvement in photosynthetic attributes and Fe-reductase activity, confirming the active role of TH in mitigating Fe-deficiency. Consistent increases in tissue Fe content and increased Fe-transporter (GmIRT1, GmNRAMP2a, GmNRAMP2b and GmNRAMP7) mRNA levels in roots following TH supplementation were observed only under Fe-deprivation. Root cell death, electrolyte leakage, superoxide (O2 •- ) and hydrogen peroxide (H2 O2 ) substantially declined due to TH in Fe-deprived plants. Further, the elevation of citrate and malate concentration along with the expression of citrate synthase (GmCs) and malate synthase (GmMs) caused by TH suggest improved chelation of Fe in Fe-deficient plants. Results also suggest that TH has a role in triggering antioxidant defence by increasing the activity of glutathione reductase (GR) along with elevated S-metabolites (glutathione and methionine) to stabilize redox status under Fe-deficiency.

Conclusions: TH increases the availability and mobilization of Fe by inducing Fe-uptake pathways, which appears to help provide resistance to oxidative stress associated with Fe-shortage in soybean.

Significance and impact of the study: These findings indicate that while Fe deficiency does not affect the rate or degree of TH hyphal association in soybean roots, the beneficial effects of TH alone may be Fe deficiency-dependent.

Keywords: Fe-efficiency; antioxidant enzymes; beneficial fungus; mineral deficiency; mycelial colonization.

MeSH terms

  • Antioxidants / metabolism
  • Chlorophyll / metabolism
  • Citrate (si)-Synthase / metabolism
  • Citrates
  • Glutathione / metabolism
  • Glutathione Reductase / metabolism
  • Glycine max* / metabolism
  • Hydrogen Peroxide / metabolism
  • Iron / metabolism
  • Iron Deficiencies*
  • Malate Synthase / metabolism
  • Malates / metabolism
  • Methionine / metabolism
  • Phenols / metabolism
  • Plant Roots / metabolism
  • RNA, Messenger / metabolism
  • Soil
  • Superoxides / metabolism

Substances

  • Malates
  • Antioxidants
  • Hydrogen Peroxide
  • Glutathione Reductase
  • Superoxides
  • Citrate (si)-Synthase
  • Malate Synthase
  • Chlorophyll
  • Iron
  • Glutathione
  • Phenols
  • Soil
  • Citrates
  • Methionine
  • RNA, Messenger

Supplementary concepts

  • Trichoderma harzianum