Involvement of Abscisic Acid in the Coordinated Regulation of a Stress-Inducible Hexose Transporter (VvHT5) and a Cell Wall Invertase in Grapevine in Response to Biotrophic Fungal Infection

Abstract

Biotrophic fungal and oomycete pathogens alter carbohydrate metabolism in infected host tissues. Symptoms such as elevated soluble carbohydrate concentrations and increased invertase activity suggest that a pathogen-induced carbohydrate sink is established. To identify pathogen-induced regulators of carbohydrate sink strength, quantitative real-time polymerase chain reaction was used to measure transcript levels of invertase and hexose transporter genes in biotrophic pathogen-infected grapevine (Vitis vinifera) leaves. The hexose transporter VvHT5 was highly induced in coordination with the cell wall invertase gene VvcwINV by powdery and downy mildew infection. However, similar responses were also observed in response to wounding, suggesting that this is a generalized response to stress. Analysis of the VvHT5 promoter region indicated the presence of multiple abscisic acid (ABA) response elements, suggesting a role for ABA in the transition from source to sink under stress conditions. ABA treatment of grape leaves was found to reproduce the same gene-specific transcriptional changes as observed under biotic and abiotic stress conditions. Furthermore, the key regulatory ABA biosynthetic gene, VvNCED1, was activated under these same stress conditions. VvHT5 promoter::b-glucuronidase-directed expression in transgenic Arabidopsis (Arabidopsis thaliana) was activated by infection with powdery mildew and by ABA treatment, and the expression was closely associated with vascular tissue adjacent to infected regions. Unlike VvHT1 and VvHT3, which appear to be predominantly involved in hexose transport in developing leaves and berries, VvHT5 appears to have a specific role in enhancing sink strength under stress conditions, and this is controlled through ABA. Our data suggest a central role for ABA in the regulation of VvcwINV and VvHT5 expression during the transition from source to sink in response to infection by biotrophic pathogens.

The role of sugar signaling in plant defense responses against fungal pathogens

“…VvHT5 shows the highest similarity to AtSTP13 and both of them have a comparable high affinity to glucose (K m = 89 lM and K m = 74 lM, respectively) (Norholm et al 2006;Hayes et al 2007;Afoufa-Bastien et al 2010). Furthermore, the expression of these two transporters is described to be induced in response to pathogen attack (Norholm et al 2006;Hayes et al 2010). Induction of STP sugar transporters is a characteristic feature of plant response to various stresses, both biotic and abiotic.…”

“…Cell wall invertase is a sink-specific enzyme, normally found in various types of carbohydrateconsuming tissues and its activity is usually low in source leaves (Essmann et al 2008). However, when leaves are attacked by a pathogen, a rapid increase is observed in the activity of this enzyme (Chou et al 2000;Fotopoulos et al 2003;Hayes et al 2010). Apart from the induction of plant cell wall invertase activity at the infection site, the activity of fungal invertases is observed (Heisterüber et al 1994;Chou et al 2000;Voegele et al 2006), which also degrades sucrose in the apoplast.…”

“…In grapevine leaves infested by obligatory biotrophs Erysiphe necator and Plasmopara viticola numerous hexose transporters were induced, but the strongest effect was found for VvHT5, which was also induced in response to wounding. This, according to the authors, suggests their general role in plant response to stress (Hayes et al 2010). VvHT5 shows the highest similarity to AtSTP13 and both of them have a comparable high affinity to glucose (K m = 89 lM and K m = 74 lM, respectively) (Norholm et al 2006;Hayes et al 2007;Afoufa-Bastien et al 2010).…”

The Accumulation of miRNAs Differentially Modulated by Drought Stress Is Affected by Grafting in Grapevine

“…PPO enzymes play a role in the control of reactive oxygen species (Sharma et al, 2012), and inhibition of the PPO gene, putatively mediated by n_231, could counteract drought-induced oxidative stress damage. The candidate miRNA n_622 has three putative targets, including the hexose transporter HT5, which was functionally characterized in grapevine as a homolog of the Arabidopsis sugar transporter STP13 (Hayes et al, 2007(Hayes et al, , 2010. This could support an induction of sugar signaling pathways, which, in woody species, can facilitate adaptation and/or recovery in response to dehydration (Secchi et al, 2016).…”

Understanding the Role of Defective Invertases in Plants: Tobacco Nin88 Fails to Degrade Sucrose

“…Their function is most prominent in sinks with no plasmodesmatal connections between cells, such as developing seeds and pollen (Proels et al, 2006;Hirsche et al, 2009;Kang et al, 2009). The expression and activity of cwINVs are regulated by a number of stimuli that are known to affect carbohydrate requirements, such as phytohormones (Balibrea-Lara et al, 2004;Hayes et al, 2010) and pathogen infection (Benhamou et al, 1991;Siemens et al, 2011). The activity of cwINVs is not only tightly regulated at both transcriptional and posttranscription levels; at the posttranslational level as well, cwINVs can be targeted by endogenous compartment-specific inhibitor proteins (Rausch and Greiner, 2003;Ruan et al, 2009).…”