Sporisorium reilianum Infection Changes Inflorescence and Branching Architectures of Maize

Abstract

Sporisorium reilianum is a biotrophic maize (Zea mays) pathogen of increasing economic importance. Symptoms become obvious at flowering time, when the fungus causes spore formation and phyllody in the inflorescences. To understand how S. reilianum changes the inflorescence and floral developmental program of its host plant, we investigated the induced morphological and transcriptional alterations. S. reilianum infection promoted the outgrowth of subapical ears, suggesting that fungal presence suppressed apical dominance. Female inflorescences showed two distinct morphologies, here termed "leafy ear" and "eary ear." In leafy ears, all floral organs were replaced by vegetative organs. In eary ears, modified carpels enclosed a new female inflorescence harboring additional female inflorescences at every spikelet position. Similar changes in meristem fate and organ identity were observed in the tassel of infected plants, which formed male inflorescences at spikelet positions. Thus, S. reilianum triggered a loss of organ and meristem identity and a loss of meristem determinacy in male and female inflorescences and flowers. Microarray analysis showed that these developmental changes were accompanied by transcriptional regulation of genes proposed to regulate floral organ and meristem identity as well as meristem determinacy in maize. S. reilianum colonization also led to a 30% increase in the total auxin content of the inflorescence as well as a dramatic accumulation of reactive oxygen species. We propose a model describing the architectural changes of infected inflorescence as a consequence of transcriptional, hormonal, and redox modulation, which will be the basis for further molecular investigation of the underlying mechanism of S. reilianum-induced alteration of floral development.