Abstract
Unidirectional transfer of nutrients from plant host to pathogen represents a most revealing aspect of the parasitic lifestyle of plant pathogens. Whereas much effort has been focused on sugars and amino acids, the identification of other significant metabolites is equally important for comprehensive characterization of metabolic interactions between plants and biotrophic fungal pathogens. Employing a strategy of targeted gene disruption, we generated a mutant strain (gpdhDelta) defective in glycerol-3-phosphate dehydrogenase in a hemibiotrophic plant pathogen, Colletotrichum gloeosporioides f.sp. malvae. The gpdhDelta strain had severe defects in carbon utilization as it could use neither glucose nor amino acids for sustained growth. Although the mutant mycelia were able to grow on potato dextrose agar medium, they displayed arrhythmicity in growth and failure to conidiate. The metabolic defect of gpdhDelta could be entirely ameliorated by glycerol in chemically defined minimal medium. Furthermore, glycerol was the one and only metabolite that could restore rhythmic growth and conidiation of gpdhDelta. Despite the profound defects in carbon source utilization, in planta the gpdhDelta strain exhibited normal pathogenicity, proceeded normally in its life cycle, and produced abundant conidia. Analysis of plant tissues at the peripheral zone of fungal infection sites revealed a time-dependent reduction in glycerol content. This study provides strong evidence for a role of glycerol as a significant transferred metabolite from plant to fungal pathogen.
Highlights
Considerable attention has been focused on nutrient uptake in a wide variety of biotrophic associations between plants and microbes [1, 2]
The glycerol3-phosphate dehydrogenase (GPDH) reaction represents a junction of several major biochemical pathways, and plays a fundamental role in energy metabolism and biomass synthesis
In addition to phospholipid and triacylglycerol biosynthesis, GPDH is involved in the synthesis of glycerol and, in concert with a mitochondrial glycerol 3-phosphate (Gly-3-P) shuttle system, is known to be crucial for coupling glycolysis with activation of mitochondrial oxidative metabolism and ATP production [34, 35]
Summary
Considerable attention has been focused on nutrient uptake in a wide variety of biotrophic associations between plants and microbes [1, 2]. To address this topic, several experimental approaches have been pursued, most involving either the axenic culturing of fungal pathogens to examine the requirements of particular nutrients, or the feeding of the plant host. The LPH ramify throughout the apoplast of the leaf tissue, giving rise to the thin secondary hyphae This generation of thin secondary hyphae from LPH has been associated with the conversion from biotrophic growth to necrotrophic infection by C. gloeosporioides.
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