Flavescence dorée (FD) is a phytoplasma disease transmitted by insects, causing severe damage in vineyards across Europe. Since there is no effective treatment, infected plants must be removed to prevent further spread. There is variation in susceptibility to FD among different grapevine cultivars, and some exhibit symptom remission, known as recovery, although the mechanisms behind this are unclear. Diseased plants accumulate soluble sugars, including sucrose, which influences the concentration of trehalose-6-phosphate (T6P), a signalling molecule affecting plant growth and stress responses. It is hypothesized that sucrose-mediated signalling via T6P could trigger defence mechanisms, reducing FD pathogen load and increasing plant recovery. To test this hypothesis, two grapevine genotypes with different susceptibility to FD were compared, revealing increased sucrose level and trehalose-6-phosphate synthase (TPS) activity in the more tolerant cultivar. However, FD-infected plants showed inhibited sucrose-cleaving enzymes and no activation of TPS expression. Attempts to enhance sucrose levels through trunk infusion and girdling promoted sucrose metabolism, T6P biosynthesis, and defence gene expression, facilitating symptom recovery. Girdling particularly enhanced T6P biosynthesis and expression of defence genes above the treatment point, reducing FD pathogen presence and promoting recovery. These findings indicate that elevated sucrose levels, possibly signalling through T6P, may limit FD pathogen spread, aiding in plant recovery.

Dept of Plant and Environmental Sciences University of Copenhagen Copenhagen Denmark

Global Change Research Institute of the Czech Academy of Sciences Brno Czech Republic

Institute for Sustainable Plant Protection CNR Turin Italy

PlantStressLab Department of Agricultural Forestry and Food Sciences University of Turin Grugliasco Italy

Zobrazit více v PubMed

Afoufa-Bastien  D, Medici  A, Jeauffre  J, Coutos-Thévenot  P, Lemoine  R, Atanassova  R, Laloi  M.  2010. The PubMed DOI PMC

André  A, Maucourt  M, Moing  A, Rolin  D, Renaudin  J.  2005. Sugar import and phytopathogenicity of PubMed DOI

Berger  S, Papadopoulus  M, Schreiber  U, Kaiser  W, Roitsch  T.  2004. Complex regulation of gene expression, photosynthesis and sugar levels by pathogen infection. Physiologia Plantarum  122, 419–428. doi: 10.1111/j.1399-3054.2004.00433.x DOI

Bertaccini  A.  2007. Phytoplasmas diversity, taxonomy, and epidemiology. Frontiers in Bioscience  12, 673–689. doi: 10.2741/2092 PubMed DOI

Bosco  D, Marzachì  C.  2016. Insect transmission of phytoplasmas. In: Brown  J, ed. Vector-mediated transmission of plant pathogens. St Paul, MN, USA: APS Press, Ch. 22, 319–327. doi: 10.1094/9780890545355.022 DOI

Breia  R, Conde  A, Badim  H, Fortes  AM, Geròs  H, Granell  A.  2021. Plant SWEETs: from sugar transport to plant–pathogen interaction and more unexpected physiological roles. Plant Physiology  186, 836–852. doi: 10.1093/plphys/kiab127 PubMed DOI PMC

Cardot  C, Mappa  G, La Camera  S, Gaillard  C, Vriet  C, Lecomte  P, Ferrari  G, Coutos-Thévenot  P.  2019. Comparison of the molecular responses of tolerant, susceptible and highly susceptible grapevine cultivars during interaction with the pathogenic fungus PubMed DOI PMC

Carra  A, Gambino  G, Schubert  A.  2007. A cetyltrimethylammonium bromide-based method to extract low-molecular-weight RNA from polysaccharide-rich plant tissues. Analytical Biochemistry  360, 318–320. doi: 10.1016/j.ab.2006.09.022 PubMed DOI

Chen  J-J, Zhang  J, He  X-Q.  2014. Tissue regeneration after bark girdling: an ideal research tool to investigate plant vascular development and regeneration. Physiologia Plantarum  151, 147–155. doi: 10.1111/ppl.12112 PubMed DOI

Chitarra  W, Pagliarani  C, Abbà  S, Boccacci  P, Birello  G, Rossi  M, Palmano  S, Marzachì  C, Perrone  I, Gambino  G.  2018. miRVIT: a novel miRNA database and its application to uncover PubMed DOI PMC

Chuche  J, Thiéry  D.  2014. Biology and ecology of the Flavescence dorée vector DOI

Covington  ED, Roitsch  T, Dermasta  M.  2016. Determination of the activity signature of key carbohydrate metabolism enzymes in phenolic-rich grapevine tissues. Acta Chimica Slovenica  63, 757–762. doi: 10.17344/acsi.2016.2484 PubMed DOI

EFSA Panel on Plant Health  2014. Scientific opinion on pest categorisation of grapevine Flavescence dorée. EFSA Journal  12, 3851. https://www.efsa.europa.eu/it/efsajournal/pub/3851

Eveillard  S, Jollard  C, Labroussaa  F, et al.  2016. Contrasting susceptibilities to Flavescence dorée in PubMed DOI PMC

Figueroa  CM, Lunn  JE.  2016. A tale of two sugars: trehalose 6-phosphate and sucrose. Plant Physiology  172, 7–27. doi: 10.1104/pp.16.00417 PubMed DOI PMC

Fu  Q, Cheng  L, Guo  Y, Turgeon  R.  2011. Phloem loading strategies and water relations in trees and herbaceous plants. Plant Physiology  157, 1518–1527. doi: 10.1104/pp.111.184820 PubMed DOI PMC

Gambino  G, Boccacci  P, Margaria  P, Palmano  S, Gribaudo  I.  2013. Hydrogen peroxide accumulation and transcriptional changes in grapevines recovered from Flavescence dorée disease. Phytopathology  103, 776–784. doi: 10.1094/PHYTO-11-12-0309-R PubMed DOI

Hayes  A, Feechan  A, Dry  IB.  2010. Involvement of abscisic acid in the coordinated regulation of a stress-inducible hexose transporter (VvHT5) and a cell wall invertase in grapevine in response to biotrophic fungal infection. Plant Physiology  153, 211–221. doi: 10.1104/pp.110.154765 PubMed DOI PMC

Hayes  MA, Davies  C, Dry  IB.  2007. Isolation, functional characterization, and expression analysis of grapevine ( PubMed DOI

Hogenhout  AS, Oshima  K, Ammar  E-D, Kakizawa  S, Kingdom  HN, Namba  S.  2008. Phytoplasmas: bacteria that manipulate plants and insects. Molecular Plant Pathology  9, 403–423. doi: 10.1111/j.1364-3703.2008.00472.x PubMed DOI PMC

Horsfall  JG, Dimond  AE.  1957. Interactions of tissue sugar, growth substances, and disease susceptibility. Zeitschrift für Pflanzenkrankheiten (Pflanzenpathologie) und Pflanzenschutz  64, 415–421. https://www.jstor.org/stable/43231735

Hren  M, Nikolić  P, Rotter  A, Blejec  A, Terrier  N, Ravnikar  M, Dermastia  M, Gruden  K.  2009. ‘Bois noir’ phytoplasma induces significant reprogramming of the leaf transcriptome in the field grown grapevine. BMC Genomics  10, 460. doi: 10.1186/1471-2164-10-460 PubMed DOI PMC

Jammer  A, Akhtar  SS, Buchvaldt Amby  D, Pandey  C, Mekureyaw  MF, Bak  F, Roitsch  T.  2022. Enzyme activity profiling as an emerging tool for cell physiological phenotyping within functional phenomics to assess plant growth and stress responses. Journal of Experimental Botany  73, 5170–5198. doi: 10.1093/jxb/erac215 PubMed DOI

Jammer  A, Gasperl  A, Luschin-Ebengreuth  N, et al.  2015. Simple and robust determination of the activity signature of key carbohydrate metabolism enzymes for physiological phenotyping in model and crop plants. Journal of Experimental Botany  66, 553–5542. doi: 10.1093/jxb/erv228 PubMed DOI

Kerbler  SM-L, Armijos-Jaramillo  V, Lunn  JE, Vicente  R.  2023. The trehalose 6-phosphate phosphatase family in plants. Physiologia Plantarum  175, e14096. doi: 10.1111/ppl.14096 PubMed DOI

Kirazawa  Y, Iwabuchi  N, Maejima  K, et al.  2022. A phytoplasma effector acts as a ubiquitin-like mediator between floral MADS-box proteins and proteasome shuttle proteins. The Plant Cell  34, 1709–1723. doi: 10.1093/plcell/koac062 PubMed DOI PMC

Kuzmanović  S, Martini  M, Ermacora  P, Ferrini  F, Starović  M, Tosić  M, Carraro  L, Osler  R.  2008. Incidence and molecular characterization of flavescence dorée and stolbur phytoplasmas in grapevine cultivars from different viticultural areas of Serbia. Vitis  47, 105–111. https://hdl.handle.net/11390/882521

Lepka  P, Stitt  M, Moll  E, Seemüller  E.  1999. Effect of phytoplasmal infection on concentration and translocation of carbohydrates and amino acids in periwinkle and tobacco. Physiological and Molecular Plant Pathology  55, 59–68. doi: 10.1006/pmpp.1999.0202 DOI

Liu  YH, Song  YH, Ruan  YL.  2022. Sugar conundrum in plant–pathogen interactions: roles of invertase and sugar transporters depend on pathosystems. Journal of Experimental Botany  73, 1910–1925. doi: 10.1093/jxb/erab562 PubMed DOI PMC

Livak  KJ, Schmittgen  TD.  2001. Analysis of relative gene expression data using real-time quantitative PCR and the   method. Methods  25, 402–408. doi: 10.1006/meth.2001.1262 PubMed DOI

Margaria  P, Ferrandino  A, Caciagli  P, Kedrina  O, Schubert  A, Palmano  S.  2014. Time course metabolic and transcript analysis of the flavonoid pathway in Nebbiolo and Barbera grapevines ( PubMed DOI

McAdam  S, Brodribb  TJ, Ross  JJ.  2016. Shoot-derived abscisic acid promotes root growth. Plant, Cell & Environment  39, 652–659. doi: 10.1111/pce.12669 PubMed DOI

Morabito  C, Secchi  F, Schubert  A.  2021. Grapevine TPS (trehalose-6-phosphate synthase) family genes are differentially regulated during development, upon sugar treatment and drought stress. Plant Physiology and Biochemistry  164, 54–62. doi: 10.1016/j.plaphy.2021.04.032 PubMed DOI

Morone  C, Boveri  M, Giosuè  S, Gotta  P, Rossi  V, Scapin  I, Marzachì  C.  2007. Epidemiology of flavescence dorée in vineyards in North-western Italy. Phytopathology  97, 1422–1427. doi: 10.1094/PHYTO-97-11-1422 PubMed DOI

Musetti  R, Buxa  SV, De Marco  F, Loschi  A, Polizzotto  R, Kogel  K-H, van Bel  AJE.  2013. Phytoplasma-triggered Ca PubMed DOI

Naseem  M, Kunz  M, Dandekar  T.  2017. Plant–pathogen maneuvering over apoplastic sugars. Trends in Plant Science  22, 740–743. doi: 10.1016/j.tplants.2017.07.001 PubMed DOI

Pagliarani  C, Gambino  G, Ferrandino  A, Chitarra  W, Vrhovsek  U, Cantù  D, Palmano  S, Marzachì  C, Schubert  A.  2020. Molecular memory of PubMed DOI PMC

Pelletier  C, Salar  P, Gillet  J, Cloquemin  G, Very  P, Foissac  X, Malembic-Maher  S.  2009. Triplex real-time PCR assay for sensitive and simultaneous detection of grapevine phytoplasmas of the 16SrV and 16SrXII-A groups with an endogenous analytical control. Vitis  48, 87–95. doi: 10.5073/vitis.2009.48.87-95 DOI

Prezelj  N, Covington  E, Roitsch  T, Gruden  K, Fragner  L, Weckwerth  W, Chersicola  M, Vodopivec  M, Dermastia  M.  2016. Metabolic consequences of infection of grapevine ( PubMed DOI PMC

Prezelj  N, Nikolić  P, Gruden  K, Ravnikar  M, Dermastia  M.  2013. Spatiotemporal distribution of flavescence dorée phytoplasma in grapevine. Plant Pathology  62, 760–766. doi: 10.1111/j.1365-3059.2012.02693.x PubMed DOI PMC

Proels  RK, Hückelhoven  R.  2014. Cell-wall invertases, key enzymes in the modulation of plant metabolism during defence responses. Molecular Plant Pathology  15, 858–864. doi: 10.1111/mpp.12139 PubMed DOI PMC

Ripamonti  M, Maron  F, Cornara  D, Marzachì  C, Fereres  A, Bosco  D.  2022. Leafhopper feeding behaviour on three grapevine cultivars with different susceptibilities to Flavescence dorée. Journal of Insect Physiology  137, 104366. doi: 10.1016/j.jinsphys.2022.104366 PubMed DOI

Ripamonti  M, Pacifico  D, Roggia  C, Palmano  S, Rossi  M, Bodino  N, Marzachì  C, Bosco  D, Galetto  L.  2020. Recovery from grapevine flavescence dorée in areas of high infection pressure. Agronomy  10, 1479. doi: 10.3390/agronomy10101479 DOI

Ripamonti  M, Pegoraro  M, Morabito  C, Gribaudo  I, Schubert  A, Bosco  D, Marzachì  C.  2021. Susceptibility to flavescence dorée of different DOI

Roggia  C, Caciagli  L, Galetto  D, Pacifico  F, Veratti  F, Bosco  D, Marzachì  C.  2014. Flavescence doreée phytoplasma titre in field-infected Barbera and Nebbiolo grapevines. Plant Pathology  63, 31–41. doi: 10.1111/ppa.12068 DOI

Roitsch  T, Balibrea  ME, Hofmann  M, Proels  R, Sinha  AK.  2003. Extracellular invertase: key metabolic enzyme and PR protein. Journal of Experimental Botany  54, 513–524. doi: 10.1093/jxb/erg050 PubMed DOI

Roitsch  T, Gonzalez  M.  2004. Function and regulation of invertases in higher plants: sweet sensations. Trends in Plant Science  9, 606–613. doi: 10.1016/j.tplants.2004.10.009 PubMed DOI

Rolland  F, Baena-Gonzalez  E, Sheen  J.  2006. Sugar sensing and signaling in plants: conserved and novel mechanisms. Annual Review of Plant Biology  57, 675–709. doi: 10.1146/annurev.arplant.57.032905.105441 PubMed DOI

Ruffner  HP, Adler  S, Rast  DM.  1990. Soluble and wall associated forms of invertase in

Santi  S, De Marco  F, Polizzotto  R, Grisan  S, Musetti  R.  2013. Recovery from stolbur disease in grapevine involves changes in sugar transport and metabolism. Frontiers in Plant Science  4, 171. doi: 10.3389/fpls.2013.00171 PubMed DOI PMC

Santi  S, Grisan  S, Pierasc  A, De Marco  F, Musetti  R.  2012. Laser microdissection of grapevine leaf phloem infected by stolbur reveals site-specific gene responses associated to sucrose transport and metabolism. Plant, Cell & Environment  36, 343–355. doi: 10.1111/j.1365-3040.2012.02577.x PubMed DOI

Sugio  A, Kingdom  NK, MacLean  AM, Grieve  VM, Hogenhout  SA.  2011. Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis. Proceedings of the National Academy of Sciences, USA  108, E1254–E1263. doi: 10.1073/pnas.1105664108 PubMed DOI PMC

Teixeira  A, Martins  V, Frusciante  S, Cruz  T, Noronha  H, Diretto  G, Geros  H.  2020. Flavescence dorée-derived leaf yellowing in grapevine ( PubMed DOI PMC

Vannozzi  A, Dry  IB, Fasoli  M, Zenoni  S, Lucchin  M.  2012. Genome-wide analysis of the grapevine stilbene synthase multigenic family: genomic organization and expression profiles upon biotic and abiotic stresses. BMC Plant Biology  12, 130. doi: 10.1186/1471-2229-12-130 PubMed DOI PMC

Vitali  M, Chitarra  W, Galetto  L, Bosco  D, Marzachì  C, Gullino  ML, Spanna  F, Lovisolo  C.  2013. Flavescence dorée phytoplasma deregulates stomatal control of photosynthesis in DOI

Wu  B, Liu  H, Guan  L, Fan  P, Li  S.  2015. Carbohydrate metabolism in grape cultivars that differ in sucrose accumulation. Vitis  50, 51–57.

Zhang  Y, Primavesi  LF, Jhurreea  D, Andraloj  PJ, Mitchell  RAC, Powers  SJ, Schluepmann  H, Delatte  T, Wingler  A, Paul  MJ.  2009. Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiology  149, 1860–1861. doi: 10.1104/pp.108.133934 PubMed DOI PMC

Zhou  R, Cheng  L.. 2008. Competitive inhibition of phosphoglucose isomerase of apple leaves by sorbitol 6-phosphate. Journal of Plant Physiology  165, 903–910. doi: 10.1016/j.jplph.2007.12.002. PubMed DOI