Characterization of the largest effector gene cluster of Ustilago maydis

PLoS Pathog. 2014 Jul 3;10(7):e1003866. doi: 10.1371/journal.ppat.1003866. eCollection 2014 Jul.

Abstract

In the genome of the biotrophic plant pathogen Ustilago maydis, many of the genes coding for secreted protein effectors modulating virulence are arranged in gene clusters. The vast majority of these genes encode novel proteins whose expression is coupled to plant colonization. The largest of these gene clusters, cluster 19A, encodes 24 secreted effectors. Deletion of the entire cluster results in severe attenuation of virulence. Here we present the functional analysis of this genomic region. We show that a 19A deletion mutant behaves like an endophyte, i.e. is still able to colonize plants and complete the infection cycle. However, tumors, the most conspicuous symptoms of maize smut disease, are only rarely formed and fungal biomass in infected tissue is significantly reduced. The generation and analysis of strains carrying sub-deletions identified several genes significantly contributing to tumor formation after seedling infection. Another of the effectors could be linked specifically to anthocyanin induction in the infected tissue. As the individual contributions of these genes to tumor formation were small, we studied the response of maize plants to the whole cluster mutant as well as to several individual mutants by array analysis. This revealed distinct plant responses, demonstrating that the respective effectors have discrete plant targets. We propose that the analysis of plant responses to effector mutant strains that lack a strong virulence phenotype may be a general way to visualize differences in effector function.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Gene Deletion
  • Genes, Fungal / physiology*
  • Multigene Family / physiology*
  • Plant Tumors / microbiology*
  • Seedlings / microbiology*
  • Ustilago / genetics
  • Ustilago / metabolism
  • Ustilago / pathogenicity
  • Zea mays / microbiology*

Grants and funding

Our work was supported by the Max Planck Society, the Collaborative Research Center SFB593, the Alexander von Humboldt Foundation, and the LOEWE program of the state of Hesse. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.