The mitochondrial alternative oxidase Aox1 is needed to cope with respiratory stress but dispensable for pathogenic development in Ustilago maydis

PLoS One. 2017 Mar 8;12(3):e0173389. doi: 10.1371/journal.pone.0173389. eCollection 2017.

Abstract

The mitochondrial alternative oxidase is an important enzyme that allows respiratory activity and the functioning of the Krebs cycle upon disturbance of the respiration chain. It works as a security valve in transferring excessive electrons to oxygen, thereby preventing potential damage by the generation of harmful radicals. A clear biological function, besides the stress response, has so far convincingly only been shown for plants that use the alternative oxidase to generate heat to distribute volatiles. In fungi it was described that the alternative oxidase is needed for pathogenicity. Here, we investigate expression and function of the alternative oxidase at different stages of the life cycle of the corn pathogen Ustilago maydis (Aox1). Interestingly, expression of Aox1 is specifically induced during the stationary phase suggesting a role at high cell density when nutrients become limiting. Studying deletion strains as well as overexpressing strains revealed that Aox1 is dispensable for normal growth, for cell morphology, for response to temperature stress as well as for filamentous growth and plant pathogenicity. However, during conditions eliciting respiratory stress yeast-like growth as well as hyphal growth is strongly affected. We conclude that Aox1 is dispensable for the normal biology of the fungus but specifically needed to cope with respiratory stress.

MeSH terms

  • Adaptation, Biological
  • Cell Respiration*
  • Fungal Proteins / metabolism
  • Gene Expression
  • Gene Expression Regulation, Fungal
  • Mitochondria / genetics
  • Mitochondria / metabolism*
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism*
  • Oxidoreductases / genetics
  • Oxidoreductases / metabolism*
  • Oxygen Consumption
  • Plant Diseases / microbiology
  • Plant Proteins / genetics
  • Plant Proteins / metabolism*
  • Stress, Physiological*
  • Temperature
  • Ustilago / genetics
  • Ustilago / metabolism*
  • Ustilago / pathogenicity*
  • Zea mays / metabolism
  • Zea mays / microbiology

Substances

  • Fungal Proteins
  • Mitochondrial Proteins
  • Plant Proteins
  • Oxidoreductases
  • alternative oxidase

Grant support

Juan Pablo Pardo received a grant from Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT IN209614), Universidad Nacional Autónoma de México (UNAM) and Consejo Nacional de Ciencia y Tecnología (CONACyT 254904). Christian A. Cárdenas-Monroy received a doctoral fellowship grant from CONACyT, 218133, México. Guadalupe Guerra received a grant from Secretaría de Investigación y Posgrado (SIP 20150761), Instituto Politécnico Nacional (IPN). Christian A. Cárdenas-Monroy received a doctoral fellowship grant from CONACyT, México. Research in the laboratory of M Feldbrügge was supported by DFG/CONACyT FOR1334.