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Rootstock influences the effect of grapevine leafroll-associated viruses on berry development and metabolism via abscisic acid signalling - PubMed

. 2021 Aug;22(8):984-1005.

doi: 10.1111/mpp.13077. Epub 2021 Jun 1.

Affiliations

Rootstock influences the effect of grapevine leafroll-associated viruses on berry development and metabolism via abscisic acid signalling

Amanda M Vondras et al. Mol Plant Pathol. 2021 Aug.

Abstract

Grapevine leafroll-associated virus (GLRaV) infections are accompanied by symptoms influenced by host genotype, rootstock, environment, and which individual or combination of GLRaVs is present. Using a dedicated experimental vineyard, we studied the responses to GLRaVs in ripening berries from Cabernet Franc grapevines grafted to different rootstocks and with zero, one, or pairs of leafroll infection(s). RNA sequencing data were mapped to a high-quality Cabernet Franc genome reference assembled to carry out this study and integrated with hormone and metabolite abundance data. This study characterized conserved and condition-dependent responses to GLRaV infection(s). Common responses to GLRaVs were reproduced in two consecutive years and occurred in plants grafted to different rootstocks in more than one infection condition. Though different infections were inconsistently distinguishable from one another, the effects of infections in plants grafted to different rootstocks were distinct at each developmental stage. Conserved responses included the modulation of genes related to pathogen detection, abscisic acid (ABA) signalling, phenylpropanoid biosynthesis, and cytoskeleton remodelling. ABA, ABA glucose ester, ABA and hormone signalling-related gene expression, and the expression of genes in several transcription factor families differentiated the effects of GLRaVs in berries from Cabernet Franc grapevines grafted to different rootstocks. These results support that ABA participates in the shared responses to GLRaV infection and differentiates the responses observed in grapevines grafted to different rootstocks.

Keywords: Closteroviridae; Vitis vinifera; leafroll disease; plant-virus interaction; rootstock-scion interaction.

© 2021 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd.

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Figures

FIGURE 1
FIGURE 1

Examples of the effects of GLRaVs on Cabernet Franc leaves, canopy density, and cluster size. (a) Photographs depicting leaves from Cabernet Franc grapevines grafted to MGT 101‐14. The photographed leaves were from (left to right) GLRaV (−), GLRaV‐1 (+), GLRaV‐1,3 (+), and GLRaV‐1,2 (+). The photograph of the GLRaV (−) leaf was taken on 2018‐08‐13. The photographs of the leaves from GLRaV (+) were taken on 2018‐08‐08. The purpose of these photographs is to depict the range of leafroll disease symptoms in leaves observed in the study. The symptoms should not be construed as specific to certain infections. (b) Canopy and berry clusters from GLRaV (−) and GLRaV‐1,2 (+) in different rootstock conditions on 2017‐08‐14

FIGURE 2
FIGURE 2

Effects of GLRaV infection on (a) dormant pruning weight, 5 ≤ n ≤ 9, (b) total cluster weight, 5 ≤ n ≤ 9, and (c) tartaric acid content, 3 ≤ n ≤ 9, in 2015 and 2016. (d) Total soluble solids (TSS) at harvest in four consecutive years. 2015–2016, 5 ≤ n ≤ 9; 2017–2018, n = 6. Group differences are indicated with nonoverlapping letters (Tukey HSD, p < .05)

FIGURE 3
FIGURE 3

The conserved responses of ripening Cabernet Franc berries to GLRaV infection(s). (a) Barplots showing the number of differentially expressed (p < .05) genes up‐ and downregulated in GLRaV (+) versus GLRaV (−) in berries from Cabernet Franc grapevines grafted to different rootstocks (Kober 5BB [Kober] and MGT 101‐14 [MGT]) at each developmental stage (prevéraison [PV], véraison [Vé], mid‐ripening [MR], and harvest [Ha]) in 2017, in 2018, and in both years. (b) Heatmap showing the responses to GLRaVs (p < .05) in both rootstock conditions and in more than one GLRaV infection condition. *Differentially expressed in 1 year; **differentially expressed in both years. One or two letters “r” indicate that the effect of a particular GLRaV infection differs between rootstocks at the same developmental stage in 1 or 2 years. Any notation requires the direction (up/downregulation) of the effect to be consistent in both years, even if a significant change occurred in only 1 year

FIGURE 4
FIGURE 4

ABA metabolism and signalling pathways are sensitive to GLRaV infection. (a) Boxplots showing the abundance of abscisic acid (ABA), ABA glucose ester (ABA‐GE), and xanthoxin in 2017 and 2018 at prevéraison. Groups with nonoverlapping letters are significantly different (Tukey HSD, p < .05). (b) The effect of GLRaV infection(s) and rootstock on ABA biosynthesis and signalling genes. *Differentially expressed in 1 year; **differentially expressed in both years. One or two letters “r” indicate that the effect of a particular GLRaV infection differs between rootstocks at the same developmental stage in 1 or 2 years. Any notation requires the direction (up/downregulation) of the effect to be consistent in both years, even if a significant change occurred in only 1 year

FIGURE 5
FIGURE 5

Multiple factor analysis (MFA) of the effects of GLRaV infection. This scatterplot shows the distribution of samples along the first two MFA dimensions at each developmental stage. For each rootstock (left) and each GLRaV infection condition (right), 95% confidence ellipses are drawn

FIGURE 6
FIGURE 6

The roles of genes, hormones, and metabolites in a multiple factor analysis (MFA) of GLRaV effects. (a) Correlation between hormones and hormone‐related metabolites to rootstock‐differentiating MFA dimensions. If two variables both have either a strong positive or a strong negative correlation (|corr| > 0.5) to the same rootstock‐differentiating MFA dimension, their relationship is counted in the UpSet plots in(b) and (c), which are analogous to Venn diagrams. (b and c) The numbers of (b) genes and (c) ripening‐related metabolites with similar relationships to rootstock‐differentiating MFA dimensions as the hormone(s) and/or hormone‐related metabolites indicated below each bar. ABA, abscisic acid; ABA‐GE, ABA glucose ester; JA, jasmonic acid; SA, salicylic acid

FIGURE 7
FIGURE 7

Functional categories of genes correlated (|corr| > 0.5) to the same rootstock‐differentiating multiple factor analysis dimensions as hormones and/or hormone‐related metabolites. The counts of genes, per category, related to each hormone and metabolite are shown. ABA, abscisic acid; ABA‐GE, ABA glucose ester; JA, jasmonic acid; SA, salicylic acid

FIGURE 8
FIGURE 8

The effect of GLRaVs on hormone signalling gene expression in grape berries from plants grafted to different rootstocks. Quadrants are numbered counterclockwise from top right (I) to bottom right (IV). Individual genes are numbered 1–39. The key (left) indicates in which quadrant each gene can be found at each developmental stage. Developmental stages are abbreviated. PV, prevéraison; Vé, véraison; MR, mid‐ripening; Ha, harvest. ABA, abscisic acid; CK, cytokinin; GA, gibberellin; JA, jasmonic acid; SA, salicylic acid

FIGURE 9
FIGURE 9

Differentially expressed genes and selected metabolites produced in the shikimate, phenylpropanoid, and flavonoid pathways. (a) Pathway diagram. (b) Metabolite abundances and (c) related biosynthetic and regulatory gene expression relative to GLRaV (−) in identical rootstock and at the same developmental stage. Notation requires the direction (up/downregulation) of the effect to be consistent in both years, even if a significant change occurred in only a single year. Glycosides are abbreviated: 3‐O‐glucoside [glu], 3‐O‐glucuronide [glucur], and 3‐O‐rutinoside [rut]. *Differentially expressed/abundant in 1 year; **differentially expressed/abundant in both years. One or two letters “r” indicate that the effect of a particular GLRaV infection differs between rootstocks at the same developmental stage. Kober, Kober 5BB rootstock; MGT, MGT 101‐14 rootstock. PAL, phenylalanine ammonia‐lyase; C4H, trans‐cinnamate 4‐monooxygenase; C3H, p‐coumarate 3‐hydroxylase; F5H, ferulate‐5‐hydroxylase; 4CL, 4‐coumaroyl‐CoA ligase; CCR, cinnamoyl‐CoA reductase; CAD, cinnamyl alcohol dehydrogenase; STS, stilbene synthase; CHS, chalcone synthase; CHI, chalcone isomerase; I2′H, isoflavone 2′‐hydroxylase; IR, isoflavone reductase; F3H, flavonone 3‐hydroxylase; FLS, flavonol synthase; F3′H, flavonoid 3′‐monooxygenase; F3′5′H, flavonoid 3′,5′‐hydroxylase; OMT, O‐methyltransferase; DFR, dihydroflavanol 4‐reductase; LAR, leucoanthocyanidin reductase; LDOX, leucoanthocyanidin dioxgenase; UFGT, UDP‐glucose:anthocyanidin/flavonoid 3‐O‐glucosyltransferase; ANR, anthocyanidin reductase; GST4, glutathione S‐transferase 4; AOMT, anthocyanin O‐methyltransferase; AAT, anthocyanin acyl‐transferase; RT, UDP‐rhamnose:rhamnosyltransferase. The pathway annotation is based on KEGG pathways (

www.genome.jp/kegg/pathway.html

, accessed 13 February 2021) and Blanco‐Ulate et al. (2017)

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