ABA-Induced Sugar Transporter TaSTP6 Promotes Wheat Susceptibility to Stripe Rust

Abstract

Biotrophic pathogens, such as wheat rust fungi, survive on nutrients derived from host cells. Sugar appears to be the major carbon source transferred from host cells to various fungal pathogens; however, the molecular mechanism by which host sugar transporters are manipulated by fungal pathogens for nutrient uptake is poorly understood. TaSTP6, a sugar transporter protein in wheat (Triticum aestivum), was previously shown to exhibit enhanced expression in leaves upon infection by Puccinia striiformis f. sp. tritici (Pst), the causal agent of wheat stripe rust. In this study, we found that Pst infection caused increased accumulation of abscisic acid (ABA) and that application of exogenous ABA significantly enhanced TaSTP6 expression. Moreover, knockdown of TaSTP6 expression by barley stripe mosaic virus-induced gene silencing reduced wheat susceptibility to the Pst pathotype CYR31, suggesting that TaSTP6 expression upregulation contributes to Pst host sugar acquisition. Consistent with this, TaSTP6 overexpression in Arabidopsis (Arabidopsis thaliana) promoted plant susceptibility to powdery mildew and led to increased Glc accumulation in the leaves. Functional complementation assays in Saccharomyces cerevisiae showed that TaSTP6 has broad substrate specificity, indicating that TaSTP6 is an active sugar transporter. Subcellular localization analysis indicated that TaSTP6 localizes to the plasma membrane. Yeast two-hybrid and bimolecular fluorescence complementation experiments revealed that TaSTP6 undergoes oligomerization. Taken together, our results suggest that Pst stimulates ABA biosynthesis in host cells and thereby upregulates TaSTP6 expression, which increases sugar supply and promotes fungal infection.

Abscisic acid dynamics, signaling, and functions in plants

“…Biotic stresses such as pathogen infection can also modulate ABA homeostasis in host plants. Some biotrophic pathogens such as wheat rust fungi can promote increases in ABA that lead to elevated cytoplasmic sugar accumulation by enhancing TaSTP6 expression (Huai et al 2019). Upon infection by the necrotrophic pathogen Botrytis cinereal , the transcription factor WRKY33 promotes ABA biosynthesis by upregulating the transcription of NCED3 and NCED5 in Arabidopsis (Liu et al 2015a).…”

TaSTP13 contributes to wheat susceptibility to stripe rust possibly by increasing cytoplasmic hexose concentration

“…In addition, to further determine whether TaSTP13 forms hetero-oligomers with other STPs from wheat, interactions between TaSTP13 and TaSTP6, a STP conferring enhanced wheat susceptibility to stripe rust [20], were studied in yeast and tobacco plants as described above. The results showed that TaSTP13 could not interact with TaSTP6 (data not shown), indicating that TaSTP13 possibly functions as a homo-oligomer.…”

“…The infection sites in stained tissues were examined using an Olympus BX-51 microscope (Olympus, Tokyo, Japan) and measured with the cellSens Entry software (Olympus, Tokyo, Japan). Data of each index were obtained as described previously [20]. For the statistical analyses, standard deviations, one-way ANOVA and t-test were performed using SPSS software v17.0 based on three independent samples.…”

“…The leaves of Arabidopsis for determination of watersoluble carbohydrates were collected as described previously [20]. Water-soluble carbohydrates were extracted, and high-performance liquid chromatography was performed as described [48].…”

“…Self-interaction of TaSTP13 was assessed by monitoring cell growth on SD-Leu-Trp-Ade-His medium (SD-LTAH) and SD-LTAH containing X-Gal for 4 days. Positive controls were used as described previously [20].…”