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Planta

, Volume 246, Issue 3, pp 525–535 | Cite as

Low source–sink ratio reduces reserve starch in grapevine woody canes and modulates sugar transport and metabolism at transcriptional and enzyme activity levels

  • Angélica Silva
  • Henrique Noronha
  • Zhanwu Dai
  • Serge Delrot
  • Hernâni Gerós
Original Article

Abstract

Main conclusion

Severe leaf removal decreases storage starch and sucrose in grapevine cv. Cabernet Sauvignon fruiting cuttings and modulates the activity of key enzymes and the expression of sugar transporter genes.

Leaf removal is an agricultural practice that has been shown to modify vineyard efficiency and grape and wine composition. In this study, we took advantage of the ability to precisely control the number of leaves to fruits in Cabernet Sauvignon fruiting cuttings to study the effect of source–sink ratios (2 (2L), 6 (6L) and 12 (12) leaves per cluster) on starch metabolism and accumulation. Starch concentration was significantly higher in canes from 6L (42.13 ± 1.44 mg g DW−1) and 12L (43.50 ± 2.85 mg g DW−1) than in 2L (22.72 ± 3.10 mg g DW−1) plants. Moreover, carbon limitation promoted a transcriptional adjustment of genes involved in starch metabolism in grapevine woody tissues, including a decrease in the expression of the plastidic glucose-6-phosphate translocator, VvGPT1. Contrarily, the transcript levels of the gene coding the catalytic subunit VvAGPB1 of the VvAGPase complex were higher in canes from 2L plants than in 6L and 12L, which positively correlated with the biochemical activity of this enzyme. Sucrose concentration increased in canes from 2L to 6L and 12L plants, and the amount of total phenolics followed the same trend. Expression studies showed that VvSusy transcripts decreased in canes from 2L to 6L and 12L plants, which correlated with the biochemical activity of insoluble invertase, while the expression of the sugar transporters VvSUC11 and VvSUC12, together with VvSPS1, which codes an enzyme involved in sucrose synthesis, increased. Thus, sucrose seems to control starch accumulation through the adjustment of the cane sink strength.

Keywords

Leaf–cluster ratio Leaf removal Starch Viticulture Vitis vinifera 

Abbreviations

Susy

Sucrose synthase

GPT

Glucose-6-phosphate/phosphate translocator

AGPase

ADP-glucose pyrophosphorylase

GBSS

Granule-bound starch synthases

SS

Starch synthases

SPS

Sucrose-phosphate synthase

SUC

Sucrose transporter

SWEET

Sugars will eventually be exported transporter

NTT

Plastidic nucleotide transporter

Notes

Compliance with ethical standards

Funding

The work was supported by European Union Funds (INTERACT-NORTE-01-0145-FEDER-000017-Linha VitalityWine-ON 0013), Portuguese national funds (FCT-Portuguese Foundation for Science and Technology) under the Project UID/AGR/04033/2013 and the Conseil Interprofessionnel du Vin de Bordeaux (CIVB, France) under the Project CANOGRAPE N°44233. HN (SFRH/BPD/115518/2016) was supported by postdoctoral grant from FCT.

Conflict of interest

No conflicts of interest were declared.

Supplementary material

425_2017_2708_MOESM1_ESM.docx (333 kb)
Supplementary material 1 (DOCX 333 kb)

References

  1. Antolín MC, Ayari M, Sánchez-Días M (2006) Effects of partial rootzone drying on yield, ripening and berry ABA in potted Tempranillo grapevines with split roots. Aust J Grape Wine Res 12:13–20CrossRefGoogle Scholar
  2. Bavaresco L, Gatti M, Pezzutto S, Fregoni M, Mattivi F (2008) Effect of leaf removal on grape yield, berry composition, and stilbene concentration. Am J Enol Vitic 59:292–298Google Scholar
  3. Bennett J, Jarvis P, Creasy GL, Trought MCT (2005) Influence of defoliation on overwintering carbohydrate reserves, return bloom, and yield of mature Chardonnay grapevines. Am J Enol Vitic 56:386–393Google Scholar
  4. Bledsoe AM, Kliewer WM, Marois JJ (1988) Effects of timing and severity of leaf removal on yield and fruit composition of Sauvignon Blanc grapevines. Am J Enol Vitic 39:49–54Google Scholar
  5. Bobeica N, Poni S, Hilbert G, Renaud C, Gomès E, Delrot S, Dai Z (2015) Differential responses of sugar, organic acids and anthocyanins to source-sink modulation in Cabernet Sauvignon and Sangiovese grapevines. Front Plant Sci 6:382. doi: 10.3389/fpls.2015.00382 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Candolfi-Vasconcelos MC, Koblet W (1990) Yield, fruit quality, bud fertility, and starch reserves of the wood as a function of leaf removal in Vitis vinifera. Evidence of compensation and stress recovering. Vitis 29:199–221Google Scholar
  7. Chong J, Piron MC, Meyer S, Merdinoglu D, Bertsch C, Mestre P (2014) The SWEET family of sugar transporters in grapevine: VvSWEET4 is involved in the interaction with Botrytis cinerea. J Exp Bot 65:6589–6601CrossRefPubMedGoogle Scholar
  8. Conde A, Regalado A, Rodrigues D, Costa JM, Blumwald E, Chaves MM, Gerós H (2015) Polyols in grape berry: transport and metabolic adjustments as a physiological strategy for water stress tolerance in grapevine. J Exp Bot 66:889–906CrossRefPubMedGoogle Scholar
  9. Coombe BG (1962) The effect of removing leaves, flowers and shoot tips on fruit-set in Vitis vinifera L. J Hortic Sci 37:1–15CrossRefGoogle Scholar
  10. Dai ZW, Léon C, Feil R, Lunn JE, Delrot S, Gomès E (2013) Metabolic profiling reveals coordinated switches in primary carbohydrate metabolism in grape berry (Vitis vinifera L.), a non-climacteric fleshy fruit. J Exp Bot 64:1345–1355CrossRefPubMedPubMedCentralGoogle Scholar
  11. Davies C, Boss PK, Gerós H, Lecourieux F, Delrot S (2012) Source/sink relationships and molecular biology of sugar accumulation in grape berries. In: Gerós H, Chaves MM, Delrot S (eds) The biochemistry of grape berry. Bentham Science Publishers, Bussum, pp 44–66CrossRefGoogle Scholar
  12. Entwistle G, ap Rees T (1990) Lack of fructose-1,6-bisphosphatase in a range of higher plants that store starch. Biochem J 271:467–472CrossRefPubMedPubMedCentralGoogle Scholar
  13. Felsenstein J (1989) PHYLIP—Phylogeny Inference Package (Version 3.2). Cladistics 5:164–166Google Scholar
  14. Fusari C, Demonte AM, Figueroa CM, Aleanzi M, Iglesias AA (2006) A colorimetric method for the assay of ADP-glucose pyrophosphorylase. Anal Biochem 352:145–147CrossRefPubMedGoogle Scholar
  15. Gainza-Cortés F, Pérez R, Pérez-Castro R, Tapia J, Casaretto JA, González S, Peña Cortés H, Ruiz-Lara S, González E (2012) Characterization of a putative grapevine Zn transporter, VvZIP3, suggests its involvement in early reproductive development in Vitis vinifera L. BMC Plant Biol 12:111CrossRefPubMedPubMedCentralGoogle Scholar
  16. Gatti M, Bernizzoni F, Civardi S, Poni S (2012) Effects of cluster thinning and preflowering leaf removal on growth and grape composition in cv Sangiovese. Am J Enol Vitic 63:325–332CrossRefGoogle Scholar
  17. Geigenberger P (2011) Regulation of starch biosynthesis in response to a fluctuating environment. Plant Physiol 155:1566–1577CrossRefPubMedPubMedCentralGoogle Scholar
  18. Geisler-Lee J, Geisler M, Coutinho PM, Segerman B, Nishikubo N, Takahashi J, Aspeborg H, Djerbi S, Master E, Andersson-Gunnerås S, Sundberg B, Karpinski S, Teeri TT, Kleczkowski LA, Henrissat B, Mellerowicz EJ (2006) Poplar carbohydrate-active enzymes. Gene identification and expression analyses. Plant Physiol 140:946–962CrossRefPubMedPubMedCentralGoogle Scholar
  19. Gilson A, Barthes L, Delpierre N, Dufrêne É, Fresneau C, Bazot S (2014) Seasonal changes in carbon and nitrogen compound concentrations in a Quercus petraea chronosequence. Tree Physiol 34:716–729CrossRefPubMedGoogle Scholar
  20. 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 Genom 10:460. doi: 10.1186/1471-2164-10-460 CrossRefGoogle Scholar
  21. Intrieri C, Filippetti I, Allegro G, Centinari M, Poni S (2008) Early defoliation (hand vs mechanical) for improved crop control and grape composition in Sangiovese (Vitis vinifera L). Aust J Grape Wine Res 14:25–32CrossRefGoogle Scholar
  22. Keller M (2015) Photosynthesis and respiration. The science of grapevines, 2nd edn. Academic Press, San Diego, pp 125–143CrossRefGoogle Scholar
  23. Keller M, Koblet W (1994) Is carbon starvation rather than excessive nitrogen supply the cause of inflorescence necrosis in Vitis vinifera L. Vitis 33:81–86Google Scholar
  24. Kliewer WM, Dokoozlian NK (2005) Leaf area/crop weight ratios of grapevines: influence on fruit composition and wine quality. Am J Enol Vitic 56:170–181Google Scholar
  25. Kühn N, Guan L, Dai ZW, Wu B, Lauvergeat V, Gomès E, Li S, Godoy F, Arce-Johnson P, Delrot S (2014) Berry ripening: recently heard through the grapevine. J Exp Bot 65(16):4543–4559CrossRefPubMedGoogle Scholar
  26. Li J, Baroja-Fernández E, Bahaji A, Muñoz FJ, Ovecka M, Montero M, Sesma MT, Alonso-Casajús N, Almagro G, Sánchez-López AM, Hidalgo M, Zamarbide M, Pozueta-Romero J (2013) Enhancing sucrose synthase activity results in increased levels of starch and ADP-glucose in maize (Zea mays L.) seed endosperms. Plant Cell Physiol 54:282–294CrossRefPubMedGoogle Scholar
  27. Livak KJ, Schimittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  28. Magnin-Robert M, Spagnolo A, Boulanger A, Joyeux C, Clément C, Abou-Mansour E, Fontaine F (2016) Changes in plant metabolism and accumulation of fungal metabolites in response to esca proper and apoplexy expression in the whole grapevine. Phytopathology 106:541–553CrossRefPubMedGoogle Scholar
  29. Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428CrossRefGoogle Scholar
  30. Mullins MG, Rajasekaran K (1981) Fruiting cuttings: revised method for producing test plants of grapevine cultivars. Am J Enol Vitic 32:35–40Google Scholar
  31. Nicholas KB, Nicholas HB Jr, Deerfield DW (1997) GeneDoc: analysis and visualization of genetic variation. EMBNEW.NEWS 4:14Google Scholar
  32. Noronha H, Conde C, Delrot S, Gerós H (2015) Identification and functional characterization of grapevine transporters that mediate glucose-6-phosphate uptake into plastids. Planta 242:909–920CrossRefPubMedGoogle Scholar
  33. Osrečak M, Karoglan M, Kozina B (2016) Influence of leaf removal and reflective mulch on phenolic composition and antioxidant activity of Merlot, Teran and Plavac mali wines (Vitis vinifera L.). Sci Hortic Amst 209:261–269CrossRefGoogle Scholar
  34. Palliotti A, Gatti M, Poni S (2011) Early leaf removal to improve vineyard efficiency: gas exchange, source-to-sink balance, and reserve storage responses. Am J Enol Vitic 62:219–228CrossRefGoogle Scholar
  35. Pastenes C, Villalobos L, Ríos N, Reyes F, Turgeon R, Franck N (2014) Carbon partitioning to berries in water stressed grapevines: the role of active transport in leaves and fruits. Environ Exp Bot 107:154–166CrossRefGoogle Scholar
  36. Pastore C, Zenoni S, Tornielli GB, Allegro G, Dal Santo S, Valentini G, Intrieri C, Pezzotti M, Filippetti I (2011) Increasing the source/sink ratio in Vitis vinifera (cv Sangiovese) induces extensive transcriptome reprogramming and modifies berry ripening. BMC Genom 12:631. doi: 10.1186/1471-2164-12-631 CrossRefGoogle Scholar
  37. Pastore C, Zenoni S, Fasoli M, Pezzotti M, Tornielli GB, Filippetti I (2013) Selective defoliation affects plant growth, fruit transcriptional ripening program and flavonoid metabolism in grapevine. BMC Plant Biol 13:30CrossRefPubMedPubMedCentralGoogle Scholar
  38. Pillet J, Egert A, Pieri P, Lecourieux F, Kappel C, Charon J, Gomès E, Keller F, Delrot S, Lecourieux D (2012) VvGOLS1 and VvHsfA2 are involved in the heat stress responses in grapevine berries. Plant Cell Physiol 53:1776–1792CrossRefPubMedGoogle Scholar
  39. Poni S, Casalini L, Bernizzoni F, Civardi S, Intrieri C (2006) Effects of early defoliation on shoot photosynthesis, yield components, and grape composition. Am J Enol Vitic 57:397–407Google Scholar
  40. Poni S, Bernizzoni F, Civardi S (2008) The effect of early leaf removal on whole canopy gas exchange and vine performance of Vitis vinifera L Sangiovese. Vitis 47:1–6Google Scholar
  41. Poni S, Bernizzoni F, Civardi S, Libelli N (2009) Effects of pre-bloom leaf removal on growth of berry tissues and must composition in two red Vitis vinifera L cultivars. Aust J Grape Wine Res 15:185–193CrossRefGoogle Scholar
  42. Reid KE, Olsson N, Schlosser J, Peng F, Lund ST (2006) An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biol 6:27CrossRefPubMedPubMedCentralGoogle Scholar
  43. Rossouw GC, Smith JP, Barril C, Deloire A, Holzapfel BP (2017) Carbohydrate distribution during berry ripening of potted grapevines: impact of water availability and leaf-to-fruit ratio. Sci Hortic Amst 216:215–225CrossRefGoogle Scholar
  44. Ruffner HP, Hurlimann M, Skrivan R (1995) Soluble invertase from grape berries: purification, deglycosylation and antibody specificity. Plant Physiol Biochem 33:25–31Google Scholar
  45. Shannon JC, Pien FM, Cao H, Liu KC (1998) Brittle-1, an adenylate translocator, facilitates transfer of extraplastidial synthesized ADP-glucose into amyloplasts of maize endosperms. Plant Physiol 117:1235–1252CrossRefPubMedPubMedCentralGoogle Scholar
  46. Smith AM, Zeeman SC (2006) Quantification of starch in plant tissues. Nat Protoc 1:1342–1345CrossRefPubMedGoogle Scholar
  47. Smith AM, Zeeman SC, Smith SM (2005) Starch degradation. Annu Rev Plant Biol 56:73–98CrossRefPubMedGoogle Scholar
  48. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599CrossRefPubMedGoogle Scholar
  49. Tang X, Rolfe SA, Scholes JD (1996) The effect of Albugo candida (white blister rust) on the photosynthetic and carbohydrate metabolism of leaves of Arabidopsis thaliana. Plant Cell Environ 19:967–975CrossRefGoogle Scholar
  50. Tiessen A, Hendriks JHM, Stitt M, Branscheid A, Gibon Y, Farré EM, Geigenberger P (2002) Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14:2191–2213CrossRefPubMedPubMedCentralGoogle Scholar
  51. Vaillant-Gaveau N, Maillard P, Wojnarowiez G, Gross P, Clément C, Fontaine F (2011) Inflorescence of grapevine (Vitis vinifera L.): a high ability to distribute its own assimilates. J Exp Bot 62:4183–4190CrossRefPubMedGoogle Scholar
  52. Wardlaw IF (1990) The control of carbon partitioning in plants. New Phytol 116:341–381CrossRefGoogle Scholar
  53. Waterhouse AL (2002) Determination of total phenolics. In: Wrolstad RE, Acree TE, An H, Decker EA, Penner MH, Reid DS, Sporns P, Schwartz SJ, Shoemaker CF (eds) Current protocols in food analytical chemistry. Wiley, New York, pp I1.1.1–I1.1.7Google Scholar
  54. Weschke W, Panitz R, Sauer N, Wang Q, Neubohn B, Weber H, Wobus U (2000) Sucrose transport into barley seeds: molecular characterization of two transporters and implications for seed development and starch accumulation. Plant J 21:455–467CrossRefPubMedGoogle Scholar
  55. Weschke W, Panitz R, Gubatz S, Wang Q, Radchuk R, Weber H, Wobus U (2003) The role of invertases and hexose transporters in controlling sugar ratios in maternal and filial tissues of barley caryopses during early development. Plant J 33:395–411CrossRefPubMedGoogle Scholar
  56. Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699CrossRefPubMedGoogle Scholar
  57. Witt W, Sauter JJ (1994) Starch metabolism in poplar wood ray cells during spring mobilization and summer deposition. Physiol Plant 92:9–16CrossRefGoogle Scholar
  58. Zapata C, Deléens E, Chaillou S, Magné C (2004) Partitioning and mobilization of starch and N reserves in grapevine (Vitis vinifera L.). J Plant Physiol 161:1031–1040CrossRefPubMedGoogle Scholar
  59. Zeeman SC, Kossmann J, Smith AM (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu Rev Plant Biol 61:209–234CrossRefPubMedGoogle Scholar
  60. Zrenner R, Salanoubat M, Willmitzer L, Sonnewald U (1995) Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.). Plant J 7:97–107CrossRefPubMedGoogle Scholar
  61. Zufferey V, Murisier F, Vivin P, Belcher S, Lorenzini F, Spring J-L, Viret O (2012) Carbohydrate reserves in grapevine (Vitis vinifera L. ‘Chasselas’): influence of leaf to fruit ratio. Vitis 51:102–110Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Centro de Investigação e de Tecnologias Agro-ambientais e Biológicas (CITAB)Vila RealPortugal
  2. 2.UMR EGFV, Bordeaux Science Agro, INRAUniversité de BordeauxVillenave D’OrnonFrance
  3. 3.Centre of Molecular and Environmental Biology (CBMA)University of MinhoBragaPortugal
  4. 4.Centre of Biological Engineering (CEB)University of MinhoBragaPortugal

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