Overexpression of the VvSWEET4 Transporter in Grapevine Hairy Roots Increases Sugar Transport and Contents and Enhances Resistance to Pythium irregulare, a Soilborne Pathogen

Abstract

Sugar transport and partitioning play key roles in the regulation of plant development and responses to biotic and abiotic factors. During plant/pathogen interactions, there is a competition for sugar that is controlled by membrane transporters and their regulation is decisive for the outcome of the interaction. SWEET sugar transporters are the targets of extracellular pathogens, which modify their expression to acquire the sugars necessary to their growth ( Chen et al., 2010 ). The regulation of carbon allocation and sugar partitioning in the interaction between grapevine ( Vitis vinifera ) and its pathogens is poorly understood. We previously characterized the SWEET family in V. vinifera and showed that SWEET4 could be involved in resistance to the necrotrophic fungus Botrytis cinerea in Arabidopsis ( Chong et al., 2014 ). To study the role of VvSWEET4 in grapevine, we produced V. vinifera cv. Syrah hairy roots overexpressing VvSWEET4 under the control of the CaMV 35S promoter ( VvSWEET4 OX ). High levels of VvSWEET4 expression in hairy roots resulted in enhanced growth on media containing glucose or sucrose and increased contents in glucose and fructose. Sugar uptake assays further showed an improved glucose absorption in VvSWEET4 overexpressors. In parallel, we observed that VvSWEET4 expression was significantly induced after infection of wild type grapevine hairy roots with Pythium irregulare , a soilborne necrotrophic pathogen. Importantly, grapevine hairy roots overexpressing VvSWEET4 exhibited an improved resistance level to P. irregulare infection. This resistance phenotype was associated with higher glucose pools in roots after infection, higher constitutive expression of several genes involved in flavonoid biosynthesis, and higher flavanol contents. We propose that high sugar levels in VvSWEET4 OX hairy roots provides a better support to the increased energy demand during pathogen infection. In addition, high sugar levels promote biosynthesis of flavonoids with antifungal properties. Overall, this work highlights the key role of sugar transport mediated by SWEET transporters for secondary metabolism regulation and pathogen resistance in grapevine.

Application of Fractions of Crop Evapotranspiration Affects Carbon Partitioning of Grapevine Differentially in a Hot Climate

“…In addition, sugars directly or indirectly control a wide range of physiological processes, including photosynthesis, sugar transport itself, nitrogen uptake, defense reactions, secondary metabolism, and hormonal balance ( Smeekens et al, 2010 ; Dai et al, 2014 ). Not only sugar transport and partitioning play key roles in the regulation of plant development, but also they influence how grapevines respond to biotic and abiotic stress factors ( Meteier et al, 2019 ). NSC storage may be altered by both abiotic factors and internal competition for carbon in grapevine, and in turn, this may modify grapevine growth, yield, and berry chemistry ( Holzapfel and Smith, 2012 ).…”

Nitrate Uptake and Transport Properties of Two Grapevine Rootstocks With Varying Vigor

“…In grapevine, abscisic acid enhances C allocation toward roots and berries ( Moreno et al, 2011 ), possibly by the regulation of sugar-related SWEET transporters ( Meteier et al, 2019 ). Although, we did not validate this hypothesis, the lower stomatal conductance and transpiration rates under HN for RG during the highest transpiration period of the day ( Supplementary Figure 3 ) suggests that a higher level of abscisic acid was present in the scion with RG, which in turn could promote the transport of sugars toward the roots as proposed by Meteier et al (2019) . A stomatal closure induced by ABA could reduce the rate of photoassimilation in leaves, which in turn would reduce the flow of carbon moving toward sinks like roots.…”

The Molecular Regulation of Carbon Sink Strength in Grapevine (Vitis vinifera L.)

“…Seventeen SWEET homologes were identified in the grape genome ( Table 1 ), VvSWEET4 is characterized as a glucose transporter localized in the plasma membrane ( Chong et al, 2014 ). Overexpression of the VvSWEET4 in grapevine hairy roots increases sugar transportation and content and enhances resistance to soilborne pathogens ( Meteier et al, 2019 ). Similarly, VvSWEET7 is a mono- and disaccharide transporter and its expression is up-regulated in response to Botrytis cinerea infection in grapes ( Breia et al, 2019 ).…”