Copper acquisition is essential for plant colonization and virulence in a root-infecting vascular wilt fungus

PLoS Pathog. 2024 Nov 4;20(11):e1012671. doi: 10.1371/journal.ppat.1012671. eCollection 2024 Nov.

Abstract

Plant pathogenic fungi provoke devastating agricultural losses and are difficult to control. How these organisms acquire micronutrients during growth in the host environment remains poorly understood. Here we show that efficient regulation of copper acquisition mechanisms is crucial for plant colonization and virulence in the soilborne ascomycete Fusarium oxysporum, the causal agent of vascular wilt disease in more than 150 different crops. Using a combination of RNA-seq and ChIP-seq, we establish a direct role of the transcriptional regulator Mac1 in activation of copper deficiency response genes, many of which are induced during plant infection. Loss of Mac1 impaired growth of F. oxysporum under low copper conditions and abolishes pathogenicity on tomato plants and on the invertebrate animal host Galleria mellonella. Importantly, overexpression of two Mac1 target genes encoding a copper reductase and a copper transporter was sufficient to restore virulence in the mac1 mutant background. Our results establish a previously unrecognized role of copper reduction and uptake in fungal infection of plants and reveal new ways to protect crops from phytopathogens.

MeSH terms

  • Animals
  • Copper* / metabolism
  • Fungal Proteins* / genetics
  • Fungal Proteins* / metabolism
  • Fusarium* / genetics
  • Fusarium* / pathogenicity
  • Gene Expression Regulation, Fungal
  • Plant Diseases* / microbiology
  • Plant Roots* / microbiology
  • Solanum lycopersicum* / microbiology
  • Virulence

Substances

  • Copper
  • Fungal Proteins

Supplementary concepts

  • Fusarium oxysporum

Grants and funding

This work was supported by grants from Junta de Andalucía (ProyExcel_00488) to MSLB; from the Spanish Ministry of Science and Innovation (MICINN, grant PID2022-140187OB-I00) to MSLB and ADP and (MICINN, grants PLEC2021-007777, TED2021-130262B-I00 and PDC2022-133749-I00) to ADP; and from the Austrian Science Fund (FWF, grant P32790-B) to JS and (FWF, grant T 1266) to LSR. RPF was supported by Ph.D. fellowship FPU18/00028 from the Spanish Ministry of Universities and by the EMBO Scientific Exchange Grant 9756. MVAP was supported by the María Zambrano program to attract international talent 2021 from the Spanish Ministry of Universities and by an UCOLIDERA grant from University of Córdoba. GPP was supported by Ph.D. fellowship FPI PRE2020-092679 from MICINN. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.