Grape Sour Rot: A Four-Way Interaction Involving the Host, Yeast, Acetic Acid Bacteria, and Insects

Abstract

Sour rot, a disease affecting berries of cultivated Vitis spp. worldwide, has not been clearly defined. Reported symptoms of the disease include browning of the berry skin, oozing of disintegrated berry pulp, and the smell of acetic acid, all in the presence of fruit flies (Drosophila spp.). We determined acetic acid concentrations in multiple collections of symptomatic berries, isolated and identified microbes from them, and inoculated commonly isolated organisms into healthy berries with and without concurrent exposure to wild-type or axenic Drosophila melanogaster. Coinoculations combining one of several yeasts (Metschnikowia spp., Pichia spp., and a Saccharomyces sp.) plus an acetic acid bacterium (an Acetobacter sp. and Gluconobacter spp.) reproduced sour rot symptoms, defined here as decaying berries with a loss of turgor and containing acetic acid at a minimum of 0.83 g/liter, based on observed field levels. Symptoms developed only in the presence of D. melanogaster, either wild type or axenic, indicating a nonmicrobial contribution of these insects in addition to a previously suggested microbial role. We conclude that sour rot is the culmination of coinfection by various yeasts, which convert grape sugars to ethanol, and bacteria that oxidize the ethanol to acetic acid, and that this process is mediated by Drosophila spp.

Single and combined effects of Drosophila suzukii and Drosophila melanogaster on sour rot development in viticulture

“…The authors conclude that especially the larval development of Drosophila spp. leads to the loss of berry integrity and catalyses the decaying process (Hall, Loeb, Cadle‐Davidson, et al, ). Our experiments support a role of developing Drosophila larvae on sour rot by showing an increase in volatile acidity with increasing numbers of emerging flies (Figure ).…”

“…Instead, our study shows that the common vinegar fly D. melanogaster is able to induce sour rot as well, but in contrast to D. suzukii , it is dependent on grapes' physical conditions. Drosophila melanogaster is a well‐known amplifier of this disease and winegrowers keep an eye on it at all times (Hall, Loeb, Cadle‐Davidson, et al, ; Hall, Loeb, & Wilcox, ). Thus, it requires further investigation to determine under which circumstances D. suzukii can really increase grape damage beyond the damage levels that D. melanogaster can cause.…”

“…In viticulture, sour rot is a well‐known disease complex, which causes serious damages in years with high daytime temperatures, pre‐harvest rain and humid conditions after veraison (McFadden‐Smith & Gubler, ). Various yeasts and acetic acid bacteria contribute to its development by decomposing the juice of infected berries (Barata, Malfeito‐Ferreira, & Loureiro, ; Barata, Santos, Malfeito‐Ferreira, & Loureiro, ; Hall, Loeb, Cadle‐Davidson, Evans, & Wilcox, ). This induces the development of acetic acid in grapes, which is volatile and responsible for the typical vinegar smell.…”

“…Vinegar flies ( Drosophila spp.) are known to trigger sour rot development (Barata, Malfeito‐Ferreira, et al, ; Barata, Santos, et al, ; Hall, Loeb, Cadle‐Davidson, et al, ) and recent research showed that vinegar fly regulation with the help of insecticides can reduce disease severity (Hall, Loeb, & Wilcox, ). Different scenarios of Drosophila spp.…”

“…First, the flies are able to vector the yeasts and bacteria associated with the disease (Barata, Santos, et al, ; Ioriatti et al, ). More importantly, a recent study with axenic flies demonstrated that flies also play a non‐microbial role, presumably through the developing larvae, which themselves trigger the decomposition of berries and thereby reinforce sour rot development (Hall, Loeb, Cadle‐Davidson, et al, ).…”