Skip to main content
SpringerLink
Log in

Grapevine leafroll disease alters leaf physiology but has little effect on plant cold hardiness

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Foliar sugar accumulation in grapevines with leafroll disease was correlated with lower photosynthesis, likely due to feedback inhibition. However, cold acclimation of dormant tissues remained unaffected by the virus status.

Grapevine leafroll-associated viruses (GLRaV) contribute to losses in fruit yield and quality worldwide. Visually, leafroll disease symptoms appear similar to those associated with an imbalance in source/sink relations and a concomitant feedback inhibition of photosynthesis, which is often caused by an impasse in sugar translocation. In order to test this potential relationship and related physiological responses, leaf water status, gas exchange, non-structural carbohydrates, and dormant tissue cold hardiness were examined over 2 years in healthy and GLRaV-3-infected, field-grown Merlot grapevines. Diurnal and seasonal changes in leaf water status and gas exchange were dominated by variations in water availability, temperature, and leaf age, while GLRaV-3 infection contributed less to the overall variation. By contrast, foliar carbohydrates increased markedly in infected plants, with starch accumulating early in the growing season, followed by soluble sugar accumulation, leaf reddening, and declining gas exchange. Photosynthesis correlated negatively with leaf sugar content. However, dormant-season cold hardiness of buds and cane vascular tissues was similar in healthy and infected vines. These findings support the idea that visible symptoms of grapevine leafroll disease are a consequence of carbohydrate accumulation which, in turn, may lead to feedback inhibition of photosynthesis. In addition, this study provided evidence that GLRaV-3 infection is unlikely to alter the susceptibility to moderate water deficit and winter damage in mature Merlot grapevines.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

GLD:

Grapevine leafroll disease

GLRaV:

Grapevine leafroll-associated virus

g s :

Stomatal conductance

K h :

Root-to-stem hydraulic conductance

LT10 :

Temperature causing 10% phloem or xylem injury

LT50 :

Lethal temperature for 50% of dormant buds

NSC:

Non-structural carbohydrates

P n :

Leaf net photosynthetic rate

Ψ pd :

Predawn leaf water potential

Ψ s :

Midday stem water potential

References

  • Alabi OJ, Casassa LF, Gutha LR, Larsen RC, Henick-Kling T, Harbertson JF, Naidu RA (2016) Impacts of grapevine leafroll disease on fruit yield and grape and wine chemistry in a wine grape (Vitis vinifera L.) cultivar. PLoS One 11:e0149666

    Article  PubMed Central  PubMed  Google Scholar 

  • Ayre BG (2011) Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Mol Plant 4:377–394

    Article  CAS  PubMed  Google Scholar 

  • Bertamini M, Muthuchelian K, Nedunchezhian N (2004) Effects of grapevine leafroll on the photosynthesis of field grown grapevine plants (Vitis vinifera L. cv. Lagrein). J Phytopathol 152:145–152

    Article  CAS  Google Scholar 

  • Cabaleiro C, Segura A, García-Berrios JJ (1999) Effects of grapevine leafroll-associated virus 3 on the physiology and must of Vitis vinifera L. cv. Albariño following contamination in the field. Am J Enol Vitic 50:40–44

    Google Scholar 

  • Castellano MA, Abou-Ghanem N, Choueiri E, Martelli GP (2000) Ultrastructure of grapevine leafroll-associated virus 2 and 7 infections. J Plant Pathol 82:9–15

    Google Scholar 

  • Choné X, van Leeuwen C, Dubourdieu D, Gaudillère JP (2001) Stem water potential is a sensitive indicator of grapevine water status. Ann Bot 87:477–483

    Article  Google Scholar 

  • Downton WJS, Grant WJR, Loveys BR (1987) Diurnal changes in the photosynthesis of field-grown grape vines. New Phytol 105:71–80

    Article  PubMed  Google Scholar 

  • El Aou-ouad H, Pou A, Tomás M, Montero R, Ribas-Carbo M, Medrano H, Bota J (2017) Combined effect of virus infection and water stress on water flow and water economy in grapevines. Physiol Plant 160:171–184

    Article  PubMed  Google Scholar 

  • Endeshaw ST, Sabbatini P, Romanazzi G, Schilder AC, Neri D (2014) Effects of grapevine leafroll associated virus 3 infection on growth, leaf gas exchange, yield and basic fruit chemistry of Vitis vinifera L. cv. Cabernet Franc. Sci Hortic 170:228–236

    Article  CAS  Google Scholar 

  • Espinoza C, Vega A, Medina C, Schlauch K, Cramer G, Arce-Johnson P (2007) Gene expression associated with compatible viral diseases in grapevine cultivars. Funct Integr Genom 7:95–110

    Article  CAS  Google Scholar 

  • Feild TS, Lee DW, Holbrook NM (2001) Why leaves turn red in autumn. The role of anthocyanins in senescing leaves of red-osier dogwood. Plant Physiol 127:566–574

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ferguson JC, Moyer MM, Mills LJ, Hoogenboom G, Keller M (2014) Modeling dormant bud cold hardiness and in twenty-three Vitis genotypes reveals variation by region of origin. Am J Enol Vitic 65:59–71

    Article  Google Scholar 

  • Goheen AC, Cook JA (1959) Leafroll (red-leaf or rougeau) and its effects on vine growth, fruit quality, and yields. Am J Enol Vitic 10:173–181

    Google Scholar 

  • Goldschmidt EE, Huber SC (1992) Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars. Plant Physiol 99:1443–1448

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gutha LR, Casassa LF, Harbertson JF, Naidu RA (2010) Modulation of flavonoid biosynthetic pathway genes and anthocyanins due to virus infection in grapevine (Vitis vinifera L.) leaves. BMC Plant Biol 10:187

    Article  PubMed Central  PubMed  Google Scholar 

  • Hoch WA, Singsaas EL, McCown BH (2003) Resorption protection. Anthocyanins facilitate nutrient recovery in autumn by shielding leaves from potentially damaging light levels. Plant Physiol 133:1296–1305

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hochberg U, Bonel AG, David-Schwartz R, Degu A, Fait A, Cochard H, Peterlunger E, Herrera JC (2017) Grapevine acclimation to water deficit: the adjustment of stomatal and hydraulic conductance differs from petiole embolism vulnerability. Planta 245:1091–1104

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jones KS, Paroschy J, McKersie BD, Bowley SR (1999) Carbohydrate composition and freezing tolerance of canes and buds in Vitis vinifera. J Plant Physiol 155:101–106

    Article  CAS  Google Scholar 

  • Keller M (2015) The science of grapevines—anatomy and physiology, 2nd edn. Elsevier Academic Press, London

    Google Scholar 

  • Keller M, Mills LJ (2007) Effect of pruning on recovery and productivity of cold-injured Merlot grapevines. Am J Enol Vitic 58:351–357

    Google Scholar 

  • Keller M, Shrestha PM (2014) Solute accumulation differs in the vacuoles and apoplast of ripening grape berries. Planta 239:633–642

    Article  CAS  PubMed  Google Scholar 

  • Keller M, Smithyman RP, Mills LJ (2008) Interactive effects of deficit irrigation and crop load on Cabernet Sauvignon in an arid climate. Am J Enol Vitic 59:221–234

    Google Scholar 

  • Keller M, Mills LJ, Olmstead MA (2014) Fruit ripening has little influence on grapevine cold acclimation. Am J Enol Vitic 65:417–423

    Article  CAS  Google Scholar 

  • Keller M, Deyermond LS, Bondada BR (2015a) Plant hydraulic conductance adapts to shoot number but limits shoot vigour in grapevines. Funct Plant Biol 42:366–375

    Article  CAS  PubMed  Google Scholar 

  • Keller M, Zhang Y, Shrestha PM, Biondi M, Bondada BR (2015b) Sugar demand of ripening grape berries leads to recycling of surplus phloem water via the xylem. Plant Cell Environ 38:1048–1059

    Article  CAS  PubMed  Google Scholar 

  • Keller M, Shrestha PM, Hall GE, Bondada BR, Davenport JR (2016) Arrested sugar accumulation and altered organic acid metabolism in grape berries affected by berry shrivel syndrome. Am J Enol Vitic 67:398–406

    Article  CAS  Google Scholar 

  • Koroleva OA, Tomos AD, Farrar J, Pollock CJ (2002) Changes in osmotic and turgor pressure in response to sugar accumulation in barley source leaves. Planta 215:210–219

    Article  CAS  PubMed  Google Scholar 

  • Lecourieux F, Kappel C, Lecourieux D, Serrano A, Torres E, Arce-Johnson P, Delrot S (2014) An update on sugar transport and signalling in grapevine. J Exp Bot 65:821–832

    Article  CAS  PubMed  Google Scholar 

  • Lovisolo C, Perrone I, Carra A, Ferrandino A, Flexas J, Medrano H, Schubert A (2010) Drought-induced changes in development and function of grapevine (Vitis spp.) organs and in their hydraulic and non-hydraulic interactions at the whole-plant level: a physiological and molecular update. Funct Plant Biol 37:98–116

    Article  CAS  Google Scholar 

  • Margaria P, Ferrandino A, Caciagli P, Kedrina O, Schubert A, Palmano S (2014) Metabolic and transcript analysis of the flavonoid pathway in diseased and recovered Nebbiolo and Barbera grapevines (Vitis vinifera L.) following infection by Flavescence dorée phytoplasma. Plant Cell Environ 37:2183–2200

    Article  CAS  PubMed  Google Scholar 

  • Martelli GP, Graniti A, Ercolani GL (1986) Nature and physiological effects of grapevine diseases. Experientia 42:933–942

    Article  CAS  Google Scholar 

  • Mills LJ, Ferguson JC, Keller M (2006) Cold-hardiness evaluation of grapevine buds and cane tissues. Am J Enol Vitic 57:194–200

    Google Scholar 

  • Montero R, Pérez-Bueno ML, Barón M, Florez-Sarasa I, Tohge T, Fernie AR, El Aou-ouad H, Flexas J, Bota J (2016) Alterations in primary and secondary metabolism in Vitis vinifera ‘Malvasía de Banyalbufar’ upon infection with Grapevine leafroll-associated virus 3. Physiol Plant 157:442–452

    Article  CAS  PubMed  Google Scholar 

  • Moutinho-Pereira J, Correia CM, Gonçalves B, Bacelar EA, Coutinho JF, Ferreira HF, Lousada JL, Cortez MI (2012) Impacts of leafroll-associated viruses (GLRaV-1 and -3) on the physiology of the Portuguese grapevine cultivar ‘Touriga Nacional’ growing under field conditions. Ann Appl Biol 160:237–249

    Article  CAS  Google Scholar 

  • Naidu R, Rowhani A, Fuchs M, Golino D, Martelli GP (2014) Grapevine leafroll: a complex viral disease affecting a high-value fruit crop. Plant Dis 98:1172–1185

    Article  CAS  PubMed  Google Scholar 

  • Oliver JE, Fuchs M (2011) Tolerance and resistance to viruses and their vectors in Vitis sp.: a virologist’s perspective of the literature. Am J Enol Vitic 62:438–451

    Article  Google Scholar 

  • Pirie A, Mullins MG (1976) Changes in anthocyanin and phenolics content of grapevine leaf and fruit tissues treated with sucrose, nitrate, and abscisic acid. Plant Physiol 58:468–472

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Quereix A, Dewar RC, Gaudillere JP, Dayau S, Valancogne C (2001) Sink feedback regulation of photosynthesis in vines: measurements and a model. J Exp Bot 52:2313–2322

    Article  CAS  PubMed  Google Scholar 

  • Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709

    Article  CAS  PubMed  Google Scholar 

  • Roper TR, Williams LE (1989) Net CO2 assimilation and carbohydrate partitioning of grapevine leaves in response to trunk girdling and gibberellic acid application. Plant Physiol 89:1136–1140

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rühl EH, Clingeleffer PR (1993) Effect of minimal pruning and virus inoculation on the carbohydrate and nitrogen accumulation in Cabernet franc vines. Am J Enol Vitic 44:81–85

    Google Scholar 

  • Sampol B, Bota J, Riera D, Medrano H, Flexas J (2003) Analysis of the virus-induced inhibition of photosynthesis in malmsey grapevines. New Phytol 160:403–412

    Article  CAS  PubMed  Google Scholar 

  • Tsai CW, Daugherty MP, Almeida RPP (2012) Seasonal dynamics and virus translocation of Grapevine leafroll-associated virus 3 in grapevine cultivars. Plant Pathol 61:977–985

    Article  Google Scholar 

  • Vega A, Gutiérrez RA, Peña-Neira A, Cramer GR, Arce-Johnson P (2011) Compatible GLRaV-3 viral infections affect berry ripening decreasing sugar accumulation and anthocyanin biosynthesis in Vitis vinifera. Plant Mol Biol 77:261–274

    Article  CAS  PubMed  Google Scholar 

  • Wingler A, Delatte TL, O’Hara LE, Primavesi LF, Jhurreea D, Paul MJ, Schluepmann H (2012) Trehalose 6-phosphate is required for the onset of leaf senescence associated with high carbon availability. Plant Physiol 158:1241–1251

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang Y, Keller M (2017) Discharge of surplus phloem water may be required for normal grape ripening. J Exp Bot 68:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank an anonymous grower and Naidu Rayapati for access to their vineyard trial, Peter Cousins for sharing his unpublished leaf disk assay, and Lynn Mills for technical assistance. This work was partly funded by the American Vineyard Foundation and Washington State University’s Department of Horticulture and Irrigated Agriculture Research and Extension Center.

Author information

Author notes

  1. Matthew M. Halldorson

    Present address: Ste. Michelle Wine Estates, Prosser, WA, 99350, USA

Authors and Affiliations

  1. Department of Horticulture, Irrigated Agriculture Research and Extension Center, Washington State University, 24106 N. Bunn Rd, Prosser, WA, 99350, USA

    Matthew M. Halldorson & Markus Keller

Authors
  1. Matthew M. Halldorson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Markus Keller
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Markus Keller.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 204 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Halldorson, M.M., Keller, M. Grapevine leafroll disease alters leaf physiology but has little effect on plant cold hardiness. Planta 248, 1201–1211 (2018). https://doi.org/10.1007/s00425-018-2967-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-018-2967-x

Keywords

Search

Navigation