A model ofUstilago maydisleaf tumor metabolism

Abstract

Extensive progress has been made in the last years in unraveling molecular mechanisms of plant-pathogen interactions. Although the main research focus lies on defense and counter-defense mechanisms, some plant-pathogen interactions have been characterized on the physiological level. Only a few studies have focused on the nutrient acquisition strategies of phytopathogens. In a previous study, we analyzed how local infection of maize leaves by the tumorinducing fungus Ustilago maydis affects whole plant physiology and were able to show that carbon and nitrogen assimilates are rerouted to the tumor. While the sink strength of infected emerging young leaves increases with tumor development, systemic source leaves exhibit elevated export of assimilates and delayed senescence to compensate for the altered sink-source balance. Here we provide new experimental data on the metabolization of these assimilates in the tumor and propose a model on their utilization in the infected tissue.Biotrophic plant pathogens depend on living host tissue and need to be able to compete with host cells for the acquisition of nutrients.1 It was shown that by inducing tumors on maize (Zea mays) leaves, the biotrophic basidiomycete fungus Ustilago maydis establishes a strong sink organ for carbohydrates 2-4 and amino acids. 5 These assimilates are provided by systemic source leaves, which exhibit increased productivity and increased export rates compared to comparable leaves of non-infected maize plants. To address how assimilates are metabolized in tumors, we conducted maize transcriptomics at different time points post infection and performed additional physiological analyses on developed tumors that were inspired by the transcript profiling approach. In brief, phenylpropanoid-, AA-, cell wall biosynthesis and enzymes of the TCA cycle are transcriptionally induced in tumors, while sucrose biosynthesis is repressed.3 At the same time, tumor metabolism is characterized by reduced photosynthesis and an accumulation of soluble sugars, i.e., hexoses which are generated via cleavage of sucrose by cell wall and vacuolar invertases.2 In addition, a plasmamembrane-associated sucrose synthase (Sus1) 6 is six-fold induced in tumors. Thus, we propose that sucrose imported from systemic leaves into tumor tissue serves the following main functions in host and pathogen metabolism: (1) provision of building blocks for cell wall biosynthesis of the tumor cell, which is channeled by SUS1, (2) generation of hexoses in the tumor-cell vacuole to build up osmotic pressure for tumor cell-expansion (see Fig. 2) and (3) feeding of U. maydis, which will most likely proceed via the high affinity sucrose transporter SRT1 that can outcompete host sucrose transporters based on its low K M for sucrose and will enable the pathogen to retrieve most of the sucrose.

Maize susceptibility to Ustilago maydis is influenced by genetic and chemical perturbation of carbohydrate allocation

“…Several studies have investigated maize gene expression during infection by U. maydis (Basse, ; Doehlemann et al ., ; Gao et al ., ; Horst et al ., ; Skibbe et al ., ; Voll et al ., ). An early differential display approach revealed changes in the differentiation state of host tissue during infection, as well as altered expression of genes for secondary metabolism and defence (Basse, ).…”

A Secreted Effector Protein ofUstilago maydisGuides Maize Leaf Cells to Form Tumors

“…After successful establishment in leaves, the fungus grows in the mesophyll and the living cells of the vasculature (Ökmen and Doehlemann, 2014). Proliferation of host and fungal cells results in tumors, which are supported by the comprehensive reprogramming of both plant signaling and metabolism early in infection (Doehlemann et al, 2008;Horst et al, 2010) and alteration of the pace and pattern of host cell division.…”

Chloroplast‐associated metabolic functions influence the susceptibility of maize to Ustilago maydis

“…For example, the transcripts for functions to produce ammonia from nitrate via nitrite were down‐regulated, including three of the four nitrate reductases and two ferredoxin nitrite reductases. Similarly, transcripts for amino acid biosynthetic functions showed notable regulation in our analysis and in previous studies (Doehlemann et al ., ; Horst et al ., ). In particular, the transcripts for glutamic dehydrogenase (GRMZM2G178415) for the production of glutamate from α‐ketoglutarate were up‐regulated 2.1‐fold, as were those for four glutamine synthetases (GSs).…”

“…In addition, tumour induction results in increased transcript levels for plant defence functions and enzymes for amino acid biosynthesis, secondary metabolism and the tricarboxylic acid (TCA) cycle, among other functions (Doehlemann et al ., ; Horst et al ., ; Kretschmer et al ., ). In general, infection results in the establishment of tumour tissue as a sink for amino acids and carbohydrates with particular changes to sucrose biosynthesis and transport (Horst et al ., ).…”