Abstract

Flavescence dorée (FD), caused by the phytoplasma Candidatus Phytoplasma vitis, is a major threat to vineyard survival in different European grape-growing areas. It has been recorded in French vineyards since the mid-1950s, and rapidly spread to other countries. In Portugal, the phytoplasma was first detected in the DOC region of ‘Vinhos Verdes’ in 2006, and reached the central region of the country in 2009. The infection causes strong accumulation of carbohydrates and phenolics in the mesophyll cells and a simultaneous decrease of chlorophylls, events accompanied by a down regulation of genes and proteins involved in the dark and light-dependent reactions and stabilization of the photosystem II (PSII). In the present study, to better elucidate the basis of the leaf chlorosis in infected grapevine cv. Loureiro, we studied the isoprenoid transcript–metabolite correlation in leaves from healthy and FD-infected vines. Specifically, targeted metabolome revealed that twenty-one compounds (out of thirty-two), including chlorophylls, carotenoids, quinones and tocopherols, were reduced in response to FD-infection. Thereafter, and consistently with the biochemical data, qPCR analysis highlighted a severe FD-mediated repression in key genes involved in isoprenoid biosynthetic pathways. A more diverse set of changes, on the contrary, was observed in the case of ABA metabolism. Principal component analysis (PCA) of all identified metabolites clearly separated healthy from FD-infected vines, therefore confirming that the infection strongly alters the biosynthesis of grapevine isoprenoids; additionally, forty-four genes and metabolites were identified as the components mostly explaining the variance between healthy and infected samples. Finally, transcript–metabolite network correlation analyses were exploited to display the main hubs of the infection process, which highlighted a strong role of VvCHLG, VvVTE and VvZEP genes and the chlorophylls intermediates aminolevulunic acid and porphobilinogen in response to FD infection. Overall, results indicated that the FD infection impairs the synthesis of isoprenoids, through the repression of key genes involved in the biosynthesis of chlorophylls, carotenoids, quinones and tocopherols.

Highlights

  • Flavescence dorée (FD) has been recorded in French vineyards since the mid-1950s (Boudon-Padieu, 2002), and rapidly spread to other countries (Bertaccini et al, 2014)

  • We confirmed the hypothesis that leaf yellowing is associated caused by FD-mediated repression of the biosynthetic pathways of chlorophylls; an important novelty of the present study is that additional isoprenoid classes, carotenoids, tocochromanols and quinones, were strongly negatively affected. In agreement with this result, we found that in leaves from FD-infected plants key genes involved in the biosynthesis of chlorophylls, carotenoids, tocochromanols and quinones were strongly repressed

  • The results suggested that the observed strong reduction of L-glutamic, the early precursor of chlorophyll, could contribute, at least in part, for the observed reduction of chlorophyll a, but paradoxically, the polar intermediates phorphobilinogen and d-aminolevulinic acid (ALA), universal precursors of tetrapyrroles, were more abundant in leaves from FD-infected vines

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Summary

Introduction

Flavescence dorée (FD) has been recorded in French vineyards since the mid-1950s (Boudon-Padieu, 2002), and rapidly spread to other countries (Bertaccini et al, 2014). The FD has become a major threat to vineyard survival in different European grape-growing areas (Boudon-Padieu, 2002; Chuche and Thiéry, 2014; Margaria et al, 2014; Eveillard et al, 2016; Prezelj et al, 2016). FD is caused by the phytoplasma Candidatus Phytoplasma vitis, which is transmitted by the phytophagous insect Scaphoideus titanus Ball (Cicadellidae family). This vector is perfectly suited to southern European wine-growing areas, where summer is long enough for adults to lay their eggs (Bressan et al, 2005; Marzorati et al, 2006). Disease symptoms appear in early summer and increase in incidence and severity until harvest (Margaria et al, 2007; Abbà et al, 2014)

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