Chloroplast‐associated metabolic functions influence the susceptibility of maize to <i>Ustilago maydis</i>

Kretschmer, Matthias; Croll, Daniel; Kronstad, James W.

doi:10.1111/mpp.12485

Cited by 19 publications

(22 citation statements)

References 45 publications

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“…In addition to the photosynthesis pigment decrease shown in this study, Kretschmer et al . (2016a) recently described a decrease in lutein and xanthophyll (violaxanthin, antheraxanthin, or zeaxanthin) pigments in tumours. We hypothesize that the early Chl decrease in U. maydis ‐infected tissue hinders leaf maturation from sink to source organ, resulting in impaired photosynthesis activity and increased starch storage.…”

Section: Discussionmentioning

confidence: 99%

How to make a tumour: cell type specific dissection ofUstilago maydis‐induced tumour development in maize leaves

et al. 2018

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The biotrophic fungus Ustilago maydis causes smut disease on maize (Zea mays), which is characterized by immense plant tumours. To establish disease and reprogram organ primordia to tumours, U. maydis deploys effector proteins in an organ-specific manner. However, the cellular contribution to leaf tumours remains unknown. We investigated leaf tumour formation at the tissue- and cell type-specific levels. Cytology and metabolite analysis were deployed to understand the cellular basis for tumourigenesis. Laser-capture microdissection was performed to gain a cell type-specific transcriptome of U. maydis during tumour formation. In vivo visualization of plant DNA synthesis identified bundle sheath cells as the origin of hyperplasic tumour cells, while mesophyll cells become hypertrophic tumour cells. Cell type-specific transcriptome profiling of U. maydis revealed tailored expression of fungal effector genes. Moreover, U. maydis See1 was identified as the first cell type-specific fungal effector, being required for induction of cell cycle reactivation in bundle sheath cells. Identification of distinct cellular mechanisms in two different leaf cell types and of See1 as an effector for induction of proliferation of bundle sheath cells are major steps in understanding U. maydis-induced tumour formation. Moreover, the cell type-specific U. maydis transcriptome data are a valuable resource to the scientific community.

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Section: Discussionmentioning

confidence: 99%

How to make a tumour: cell type specific dissection ofUstilago maydis‐induced tumour development in maize leaves

et al. 2018

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“…Therefore, to suppress photosynthesis is also a strategy of pathogen successful infection. For example, the biotrophic fungus Ustilago maydis ‐infected maize plants display a downregulation in CO 2 fixation, chlorophyll biosynthesis or photosystem‐related proteins (Kretschmer, Croll, & Kronstad, ). In the present study, the net photosynthetic rate (Pn) in both AMF non‐inoculated and inoculated plants was dramatically reduced upon pathogen inoculation by leaf infiltrating or spraying (Tables and ).…”

Section: Discussionmentioning

confidence: 99%

Arbuscular mycorrhiza‐mediated resistance in tomato against Cladosporium fulvum‐induced mould disease

Wang

Yin

et al. 2017

Journal of Phytopathology

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Root colonization with arbuscular mycorrhizal fungi (AMF) enhances plant resistance particularly against soil-borne pathogenic fungi. In this study, mycorrhizal inoculation with Glomus mosseae (Gm) significantly alleviated tomato mould disease caused by the air-borne fungal pathogen, Cladosporium fulvum (Cf). The disease index (DI) in local leaves (receiving pathogen inoculation) and systemic leaves (just above the local leaf without pathogen inoculation) was 36.4% and 11.7% in mycorrhizal plants, respectively, whereas DI was 59.6% and 36.4% in the corresponding leaves of AMF noninoculated plants, after 50 days of Gm inoculation, corresponding to 15 days after Cf inoculation by leaf infiltration. Foliar spray inoculation with Cf also revealed that AMF pre-inoculated plants had a higher resistance against subsequent pathogen infection, where the DI was 41.3% in mycorrhizal plants vs. 64.4% in AMF non-inoculated plants.AMF-inoculated plants showed significantly higher fresh and dry weight than noninoculated plants under both control (without pathogen) and pathogen treatments.AMF-inoculated plants exhibited significant increases in activities of superoxide dismutase and peroxidase, along with decreases in levels of H 2 O 2 and malondialdehyde, compared with non-inoculated plants after pathogen inoculation. AMF inoculation led to increases in total chlorophyll contents and net photosynthesis rate as compared with non-inoculated plants under control and pathogen infection. Pathogen infection on AMF non-inoculated plants led to decreases in chlorophyll fluorescence parameters. However, pathogen infection did not affect these parameters in mycorrhizal plants. Taken together, these results indicate that AMF colonization may play an important role in plant resistance against air-borne pathogen infection by maintaining redox poise and photosynthetic activity. K E Y W O R D Santioxidative defence, arbuscular mycorrhiza, Cladosporium fulvum, disease index, Glomus mosseae, photosynthesis, tomato | INTRODUCTIONThe biotrophic pathogen fungus Cladosporium fulvum Cooke infects its only host tomato causing leaf mould disease, which is one of the most severe diseases threatening tomato yield and quality, especially in protected cultivation. For example, a yield loss of 10%-25% in normal years and even over 50% in bad years occurred in China (Sun, 2006). In conventional agricultural management, a large amount of synthetic fungicide is applied to control mould disease, which could cause serious environmental contamination and harm human health.In addition, new races of C. fulvum frequently emerge raising a problem of fungicide tolerance.*These authors contributed equally to this work. Control plants were sprayed with sterile distilled water. | MATERIALS AND METHODS | Plant culture and fungal treatment | Analyses of disease index and mycorrhizal colonizationThe DI was analysed after 15 days of pathogen inoculation accord- | Determination of plant growthThe effect of AMF colonization, pathogen infection, alone or in combinat...

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“…These studies provide insights into the role of metabolic changes related to carbohydrate availability in the plant–fungus interaction. We also examined the influence of chloroplast‐associated metabolic functions in an accompanying paper (Kretschmer et al ).…”

Section: Introductionmentioning

confidence: 99%

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

Kretschmer

Croll

Kronstad

2016

Molecular Plant Pathology

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The ability of biotrophic fungi to metabolically adapt to the host environment is a critical factor in fungal diseases of crop plants. In this study, we analysed the transcriptome of maize tumours induced by Ustilago maydis to identify key features underlying metabolic shifts during disease. Among other metabolic changes, this analysis highlighted modifications during infection in the transcriptional regulation of carbohydrate allocation and starch metabolism. We confirmed the relevance of these changes by establishing that symptom development was altered in an id1 (indeterminate1) mutant that showed increased accumulation of sucrose as well as being defective in the vegetative to reproductive transition. We further established the relevance of specific metabolic functions related to carbohydrate allocation by assaying disease in su1 (sugary1) mutant plants with altered starch metabolism and in plants treated with glucose, sucrose and silver nitrate during infection. We propose that specific regulatory and metabolic changes influence the balance between susceptibility and resistance by altering carbon allocation to promote fungal growth or to influence plant defence. Taken together, these studies reveal key aspects of metabolism that are critical for biotrophic adaptation during the maize-U. maydis interaction.

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

Cited by 19 publications

References 45 publications

How to make a tumour: cell type specific dissection ofUstilago maydis‐induced tumour development in maize leaves

How to make a tumour: cell type specific dissection ofUstilago maydis‐induced tumour development in maize leaves

Arbuscular mycorrhiza‐mediated resistance in tomato against Cladosporium fulvum‐induced mould disease

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

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