The fungal UmSrt1 and maize ZmSUT1 sucrose transporters battle for plant sugar resources

Abstract

The biotrophic fungus Ustilago maydis causes corn smut disease, inducing tumor formation in its host Zea mays. Upon infection, the fungal hyphae invaginate the plasma membrane of infected maize cells, establishing an interface where pathogen and host are separated only by their plasma membranes. At this interface the fungal and maize sucrose transporters, UmSrt1 and ZmSUT1, compete for extracellular sucrose in the corn smut/maize pathosystem. Here we biophysically characterized ZmSUT1 and UmSrt1 in Xenopus oocytes with respect to their voltage-, pH-and substrate-dependence and determined affinities toward protons and sucrose. In contrast to ZmSUT1, UmSrt1 has a high affinity for sucrose and is relatively pH-and voltage-independent. Using these quantitative parameters, we developed a mathematical model to simulate the competition for extracellular sucrose at the contact zone between the fungus and the host plant. This approach revealed that UmSrt1 exploits the apoplastic sucrose resource, which forces the plant transporter into a sucrose export mode providing the fungus with sugar from the phloem. Importantly, the high sucrose concentration in the phloem appeared disadvantageous for the ZmSUT1, preventing sucrose recovery from the apoplastic space in the fungus/plant interface.

γ‐Aminobutyric acid and related amino acids in plant immune responses: Emerging mechanisms of action

“…Based on pathogen lifestyle, adjustments of metabolic fluxes of soluble sugars and amino acids can be decisive to sustain strategies aimed to fuel host defences or to make the environment more hostile to the pathogen (Seifi, Van Bockhaven, Angenon, & Höfte, ). On the other hand, several pathogens have developed molecular tools to hijack critical hubs of host primary metabolism, such as enzymes and transporters, to take advantage of host resources (Engelsdorf et al, ; Wittek et al, ). To date, important roles in plant defence were established for several primary metabolites, such as sucrose (Suc) and glutamate (Glu) (Seifi, Van Bockhaven, et al, ; Tauzin & Giardina, ).…”

Differential Signaling and Sugar Exchanges in Response to Avirulent Pathogen- and Symbiont-Derived Molecules in Tobacco Cells

“…Our study should be placed within a broader contextual framework of PMIs, in which hosts and microbes may develop opposite strategies to acquire carbon molecules at the apoplastic interface ( Truernit et al, 1996 ; Fotopoulos et al, 2003 ; Azevedo et al, 2005 ; Chen et al, 2010 ; Doidy et al, 2012a ; Manck-Götzenberger and Requena, 2016 ; Wittek et al, 2017 ). The present paper reports for the first time that a myc-factor can be recognized by non-root cells, showing that undifferentiated cells, whatever their origin, are able to perceive the origin of a microbial molecule.…”

Phylogenetic Relationships of Sucrose Transporters (SUTs) in Plants and Genome-wide Characterization of SUT Genes in Orchidaceae

“…Group C contained mosses, lypophytes and angiosperms including both monocots and dicots, corresponding to SUT4 clade [20]. According to previous studies, the SUT1 and SUT2 proteins mainly play roles in phloem loading and unloading, sucrose transport to sink cells, and sucrose exchanges with microbes [2,30,31,[44][45]. While SUT4 proteins are involved in various physiological processes such as circadian rhythms and responses to dehydration and photosynthesis [46][47].…”

“…SUT family genes play essential roles in phloem loading and unloading, pollen development, fruit ripening, ethylene biosynthesis and seed development and germination in many plants [10,12,26,[28][29]. Besides, the SUT genes also involved in various physiological processes and sucrose exchanges between plants and symbiotins, pathogens and fungi [2,[30][31]. For example, in Arabidopsis, AtSUC5 is predominantly expressed in seeds, whereas AtSUC1 and the mutant atsuc9 both expressed in oral organs, and facilitates anthocyanin accumulation and oral transition [28,32].…”