Reduced Carbohydrate Availability Enhances the Susceptibility of Arabidopsis toward Colletotrichum higginsianum      

Abstract

Colletotrichum higginsianum is a hemibiotrophic ascomycete fungus that is adapted to Arabidopsis (Arabidopsis thaliana). After breaching the host surface, the fungus establishes an initial biotrophic phase in the penetrated epidermis cell, before necrotrophic growth is initiated upon further host colonization. We observed that partitioning of major leaf carbohydrates was shifted in favor of sucrose and at the expense of starch during necrotrophic fungal growth. Arabidopsis mutants with impaired starch turnover were more susceptible toward C. higginsianum infection, exhibiting a strong negative correlation between diurnal carbohydrate accumulation and fungal proliferation for the tested genotypes. By altering the length of the light phase and employing additional genotypes impaired in nocturnal carbon mobilization, we revealed that reduced availability of carbon enhances susceptibility in the investigated pathosystem. Systematic starvation experiments resulted in two important findings. First, we showed that carbohydrate supply by the host is dispensable during biotrophic growth of C. higginsianum, while carbon deficiency was most harmful to the host during the necrotrophic colonization phase. Compared with the wild type, the increases in the total salicylic acid pool and camalexin accumulation were reduced in starch-free mutants at late interaction stages, while an increased ratio of free to total salicylic acid did not convey elevated pathogenesis-related gene expression in starch-free mutants. These observations suggest that reduced carbon availability dampens induced defense responses. In contrast, starchfree mutants were more resistant toward the fungal biotroph Erysiphe cruciferarum, indicating that reduced carbohydrate availability influences susceptibility differently in the interaction with the investigated hemibiotrophic and biotrophic fungal pathogens.

Reduced susceptibility of tomato stem to the necrotrophic fungusBotrytis cinereais associated with a specific adjustment of fructose content in the host sugar pool

“…This observation is compatible with the hypothesis that in this necrotrophic interaction between B. cinerea and stem tissues, neither fungal growth nor plant defence was limited by soluble sugars. A negative correlation between total leaf carbohydrates and disease caused by C. hingginsianum on Arabidopsis has been observed (Engelsdorf et al , 2013). The gene encoding for the Arabidopsis sugar transport protein STP13 is induced upon infection by B. cinerea , suggesting that cellular glucose uptake might supply the energy required for defence (Lemonnier et al , 2014).…”

“…However, the host range of necrotrophic fungi such as B. cinerea and Sclerotinia sclerotiorum is known to encompass hundreds of plants species and organs (Elad et al , 2016), and the literature lacks general trends showing that plant species or plant organs containing high carbohydrate levels may be either more resistant (because of enhanced defence) or conversely susceptible (because of higher sugar availability for the pathogen) to necrotrophic fungi. Carbohydrate availability in Arabidopsis leaves during the early necrotrophic phase of the hemibiotroph Colletotrichum higginsianum influences host susceptibility (Engelsdorf et al , 2013). Indeed, low total carbohydrate availability (main sugars plus starch) was shown to promote necrotrophic fungal invasion, presumably by perturbing host defences, while a lower carbon availability per se did not affect fungal growth.…”

“…Indeed, low total carbohydrate availability (main sugars plus starch) was shown to promote necrotrophic fungal invasion, presumably by perturbing host defences, while a lower carbon availability per se did not affect fungal growth. On the contrary, some biotrophic fungi grow slower when the carbon availability in host cells is reduced (Engelsdorf et al , 2013). As mentioned above, there is much evidence that, for intact or detached source tissues such as leaves, resistance to a range of both biotrophic and necrotrophic pathogens requires the depolymerization of starch as well as the use of sucrose to produce glucose and fructose via the activity of invertases and possibly sucrose synthase.…”

The β‐amylase genes: negative regulators of disease resistance for Verticillium dahliae

“…Also, Engelsdorf et al . () showed that starch‐free mutants were more resistant toward the fungal biotroph Erysiphe cruciferarum and more susceptible toward the hemibiotroph Colletotrichum higginsianum . This might indicate that reduced carbohydrate availability influences susceptibility differently in interactions with hemibiotrophic and biotrophic fungal pathogens.…”

The Arabidopsis ROP-activated receptor-like cytoplasmic kinase RLCK VI_A3 is involved in control of basal resistance to powdery mildew and trichome branching

“…A dissociation curve analysis was finally conducted as follows: 1 min at 95°C, 30 sec at 55°C and 30 sec at 95°C. For the quantitation of gDNA, primers for a β-tubulin gene of E. cruciferarum and primers for the RbcS gene of Arabidopsis were used as it is described elsewhere (Engelsdorf et al 2013). Data were analyzed using MxPro QPCR software (Stratagene).…”