Developmental and metabolic plasticity of white-skinned grape berries in response to Botrytis cinerea during noble rot

Abstract

Noble rot results from exceptional infections of ripe grape (Vitis vinifera) berries by Botrytis cinerea. Unlike bunch rot, noble rot promotes favorable changes in grape berries and the accumulation of secondary metabolites that enhance wine grape composition. Noble rot-infected berries of cv Sémillon, a white-skinned variety, were collected over 3 years from a commercial vineyard at the same time that fruit were harvested for botrytized wine production. Using an integrated transcriptomics and metabolomics approach, we demonstrate that noble rot alters the metabolism of cv Sémillon berries by inducing biotic and abiotic stress responses as well as ripening processes. During noble rot, B. cinerea induced the expression of key regulators of ripening-associated pathways, some of which are distinctive to the normal ripening of red-skinned cultivars. Enhancement of phenylpropanoid metabolism, characterized by a restricted flux in white-skinned berries, was a common outcome of noble rot and red-skinned berry ripening. Transcript and metabolite analyses together with enzymatic assays determined that the biosynthesis of anthocyanins is a consistent hallmark of noble rot in cv Sémillon berries. The biosynthesis of terpenes and fatty acid aroma precursors also increased during noble rot. We finally characterized the impact of noble rot in botrytized wines. Altogether, the results of this work demonstrated that noble rot causes a major reprogramming of berry development and metabolism. This desirable interaction between a fruit and a fungus stimulates pathways otherwise inactive in white-skinned berries, leading to a greater accumulation of compounds involved in the unique flavor and aroma of botrytized wines.

Botrytized wines – current perspectives

“…A significant accumulation of several flavonoid glycosides and flavanones was detected in noble rotted berries of Sémillon grape but the production of flavones and flavonols was suppressed during noble rot. 10 In contrast, the presence of the fungus on Chenin blanc grape seems to induce, from one side, an increase in flavonols, such as catechin, epicatechin, and epicatechin gallate, and from the other side, a decrease in caftaric acid, coutaric acid, quercetin-3 glucoside, and kaempferol-3 glucoside. 12 From the results, it seems that changes in the flavonoid composition show varietal influences and need further research.…”

“…This strain was successfully used for artificial infection in the vineyard in several subsequent years, and the noble rotted grape has been used for commercial wine production as well as for several interesting research studies on botrytization. 10,[22][23][24] The draft genome sequence of this strain (BcDW1) has recently been published. 10 Induction of Botrytis infection during postharvest withering of the grape has been increasing as a strategy in making straw (passito) wines (eg, Amarone and Recioto) in Italy.…”

“…However, the final level of stilbene derivates (trans-astringin, trans-resveratrol, trans-piceid, etc) is generally low in the botrytized juice and wine, probably because Botrytis enzymes of the laccase group, such as stilbene oxidase, are able to transform these molecules to oxidized compounds, which was more extensively reviewed by Teissedre and Donèche. 4 In a significant, comprehensive study, Blanco-Ulate et al 10 have found desirable interaction between a fruit and a fungus that stimulates pathways otherwise inactive in white-skinned berries. Using transcript and metabolite analysis of the grape tissue, they identified several genes that were upregulated due to Botrytis infection.…”

“…The evolution of these compounds depends on the grape variety and on the development of noble rot. 10 In the last stage of noble rot, viniferin and astilbin could be used by the plant against Botrytis. However, the final level of stilbene derivates (trans-astringin, trans-resveratrol, trans-piceid, etc) is generally low in the botrytized juice and wine, probably because Botrytis enzymes of the laccase group, such as stilbene oxidase, are able to transform these molecules to oxidized compounds, which was more extensively reviewed by Teissedre and Donèche.…”

“…9,10 Changes in the polyphenol composition of the berry result from a combination of the fungal PPO and GOX activity and the metabolic response of the grape to fungal infection. The total phenol content either decreases 11,12 or possibly increases in highly dehydrated berries due to concentration.…”