Understanding Ustilago maydis Infection of Multiple Maize Organs.

Alex C Ferris,Virginia Walbot

doi:10.3390/jof7010008

Abstract

Ustilago maydis is a smut fungus that infects all aerial maize organs, namely, seedling leaves, tassels, and ears. In all organs, tumors are formed by inducing hypertrophy and hyperplasia in actively dividing cells; however, the vast differences in cell types and developmental stages for different parts of the plant requires that U. maydis have both general and organ-specific strategies for infecting maize. In this review, we summarize how the maize–U. maydis interaction can be studied using mutant U. maydis strains to better understand how individual effectors contribute to this interaction, either through general or specific expression in a cell type, tissue, or organ. We also examine how male sterile maize mutants that do not support tumor formation can be used to explore key features of the maize anthers that are required for successful infection. Finally, we discuss key unanswered questions about the maize–U. maydis interaction and how new technologies can potentially be used to answer them.

Highlights

Ustilago maydis is a biotrophic fungus that causes tumors in all aerial maize organs.After spores germinate on the epidermis, in nature two compatible strains fuse to form a dikaryotic filament that can infect maize cells; the lab-derived SG200 strain is solopathogenic and utilized in almost all experiments [1,2]
The differential interaction of the fungus and epidermal compared to interior cell types demonstrates tissue-specific interactions between host and pathogen in all organs examined
Anther lobes were traced from confocal images with different cell types filled in colors corresponding to the legend

Summary

Introduction

Ustilago maydis is a biotrophic fungus that causes tumors in all aerial maize organs. U. maydis initially grows along the epidermis of all organs before penetrating between epidermal cells to reach and spread throughout the subepidermal cells. It forms a biotrophic interface (close juxtaposition of fungal cell wall with the plant cell wall or plasma membrane) with the target interior cells, which invaginate their plasma membranes to accommodate branching fungal hyphae [1]. U. maydis infects leaf, stem, and reproductive organs (ears, tassels) of maize. The differential interaction of the fungus and epidermal compared to interior cell types demonstrates tissue-specific interactions between host and pathogen in all organs examined

Leaf Characteristics

Reproductive Organ Characteristics

Infection and Tumor Progression

Exploiting Maize Mutants to Define Requirements for Tumor Formation