Transcriptomic Analyses of Grapevine Leafroll-Associated Virus 3 Infection in Leaves and Berries of ‘Cabernet Franc’

Abstract

Grapevine leafroll-associated virus 3 (GLRaV-3) is one of the most important viruses affecting global grape and wine production. GLRaV-3 is the chief agent associated with grapevine leafroll disease (GLRD), the most prevalent and economically destructive grapevine viral disease complex. Response of grapevine to GLRaV-3 infection at the gene expression level is poorly characterized, limiting the understanding of GLRaV-3 pathogenesis and viral-associated symptom development. In this research, we used RNA-Seq to profile the changes in global gene expression of Cabernet franc, a premium red wine grape, analyzing leaf and berry tissues at three key different developmental stages. We have identified 1457 differentially expressed genes (DEGs) in leaves and 1181 DEGs in berries. The expression profiles of a subset of DEGs were validated through RT-qPCR, including those involved in photosynthesis (VvPSBP1), carbohydrate partitioning (VvSUT2, VvHT5, VvGBSS1, and VvSUS), flavonoid biosynthesis (VvUFGT, VvLAR1, and VvFLS), defense response (VvPR-10.3, and VvPR-10.7), and mitochondrial activities (ETFB, TIM13, and NDUFA1). GLRaV-3 infection altered source–sink relationship between leaves and berries. Photosynthesis and photosynthate assimilation were inhibited in mature leaves while increased in young berries. The expression of genes involved in anthocyanin biosynthesis increased in GLRaV-3-infected leaves, correlating with interveinal tissue reddening, a hallmark of GLRD symptoms. Notably, we identified changes in gene expression that suggest a compromised sugar export and increased sugar retrieval in GLRaV-3-infected leaves. Genes associated with mitochondria were down-regulated in both leaves and berries of Cabernet franc infected with GLRaV-3. Results of the present study suggest that GLRaV-3 infection may disrupt mitochondrial function in grapevine leaves, leading to repressed sugar export and accumulation of sugar in mature leaf tissues. The excessive sugar accumulation in GLRaV-3-infected leaves may trigger downstream GLRD symptom development and negatively impact berry quality. We propose a working model to account for the molecular events underlying the pathogenesis of GLRaV-3 and symptom development.

From Asymptomatic to Symptomatic: Multiomics profiling of the temporal response of grapevine viral-mixed infection

“…Regardless of the grapevine cultivar, a very diverse virome was detected at both the asymptomatic and symptomatic stages and a large majority (83.33%) of the plants expressed virus-like symptoms in autumn. This is consistent with the findings of several studies 18,19 that observed that virus-like symptoms were more prevalent in grapevine in autumn than in summer.…”

“…These results are in line with previous studies that found that the genes involved in cell-wall softening and expansion in GLRaV3-infected grapevine leaves were downregulated, suggesting that the presence of other symptomatic viruses (e.g. GAMaV and GPGV) was not interfering with GLRaV3 symptomatology 14,19 . In addition, polyketide (e.g.…”

“…and are not known GPGV 25 . Furthermore, symptom expression may also be a consequence of leaf malfunction and metabolic compound accumulation in response to viral infections, as shown in the recent model proposed by Song et al 19 .…”

Grapevine Virome of the Don Ampelographic Collection in Russia Has Concealed Five Novel Viruses

“…GLRaV-3 (genus Ampelovirus) is one of the most widespread and harmful grapevine viruses [45,46]. It is known as the main pathogen of grapevine leafroll disease (GLD) [47].…”

Identification of Interactions between Proteins Encoded by Grapevine Leafroll-Associated Virus 3

“…Moreover, with advances in the field of high throughput sequencing (HTS), research focus has shifted to sequencing-based strategies [ 23 ]. Limited functional studies have been conducted on grapevine virus encoded proteins, and the majority of current research focuses on identifying differentially expressed genes and elucidating the aetiology of grapevine diseases [ 24 , 25 , 26 , 27 , 28 ]. In this study, two complementary techniques were employed to identify interactions between proteins encoded by GLRaV-3 with the aim to gain a better understanding of the role of virus-encoded proteins in virion assembly and movement of members of the genus Ampelovirus .…”