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The contribution of flowering time and seed content to uneven ripening initiation among fruits within Vitis vinifera L. cv. Pinot noir clusters

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Abstract

Main conclusion

Ripening initiation-associated hormonal changes and sugar accumulation for individual fruits differed by seed content and did not depend heavily on flowering time or duration from anthesis to clusters’ onset of ripening.

For Vitis vinifera, the ripening initiation of individual fruits in a cluster occurs unevenly. This developmental period is called véraison. Why individual fruits initiate ripening at different times is not well studied, though differences in seed content and unequal developmental durations that arise from asynchronous flowering within a cluster have been proposed. This study examined how much both variables contribute to individual fruits’ ripening progress by mid-véraison, when half of berries in a cluster have initiated ripening, and whether either or both factors affect the timing of characteristic, ripening-initiation associated changes in abscisic acid and auxin before, at, and after véraison. Overall, developmental duration and flowering time did not sufficiently explain how far berries had progressed into the ripening stage because fruits did not require a fixed amount of time to initiate ripening. Fruits from early and late flowers but of similar seed content were able to initiate ripening at the same time despite differences in chronological age. This suggests either an early developmental enhancement occurred for late-initiated fruits or that flowering time is an inappropriate “day zero”. Ultimately, only seed content was linked to the timing and magnitude of ripening-related hormone changes, supporting that seeds have a comparatively larger influence than flowering time on the ripening initiation of individual berries. More specifically, if the fraction of berry weight occupied by seed was high, then the initiation of ripening for that berry and its associated hormone changes were delayed relative to berries with less seed weight versus total berry weight.

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References

  • Aharoni A, Keizer LCP, Van Den Broeck HC, Blanco-Portales R, Muñoz-Blanco J, Bois G, Smit P, De Vos RCH, O’Connell AP (2002) Novel insight into vascular, stress, and auxin-dependent and -independent gene expression programs in strawberry, a non-climacteric fruit. Plant Physiol 129:1019–1031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ban T, Ishimaru M, Kobayashi S, Shiozaki S, Goto-Yamamoto N, Horiuchi S (2003) Abscisic acid and 2,4-dichlorophenoxyacetic acid affect the expression of anthocyanin biosynthetic pathway genes in “Kyoho” grape berries. J Horticult Science Biotechnol 78:586–589

    Article  CAS  Google Scholar 

  • Bangerth F (1990) Polar auxin transport in fruit trees in relation to fruit drop. Acta Horticulturae 275:461–468

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Model using lme4. J Stat Soft 67:1–48

    Article  Google Scholar 

  • Bertin N (1995) Competition for assimilates and fruit position affect fruit set in indeterminate greenhouse tomato. Ann Bot 75:55–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Böttcher C, Harvey K, Forde CG, Boss PK, Davies C (2010) Auxin treatment of pre-veraison grape (Vitis vinifera L.) berries both delays ripening and increases the synchronicity of sugar accumulation. Aust J Grape Wine Res 17:1–8

    Article  Google Scholar 

  • Calderon-Orellana A, Mercenaro L, Shackel KA, Willits N, Matthews MA (2014) Responses of fruit uniformity to deficit irrigation and cluster thinning in commercial winegrape production. AJEV 65:354–362

    Google Scholar 

  • Carreño J, Martínez A, Almela L, Fernández-López JA (1995) Proposal of an index for the objective evaluation of the colour of red table grapes. Food Res Int 28:373–377

    Article  Google Scholar 

  • Castellarin SD, Gambetta GA, Wada H, Schackel KA, Matthews MA (2011) Fruit ripening in Vitis vinifera: spatiotemporal relationships among turgor, sugar accumulation, and anthocyanin biosynthesis. J Exp Bot 62:4345–4354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cawthon DL, Morris JR (1982a) Relationship of seed number and maturity to berry development, fruit maturation, hormonal changes, and uneven ripening of “Concord” (Vitis labrusca L.). J Am Soc Hortic Sci 107:1097–1104

    CAS  Google Scholar 

  • Cawthon DL, Morris JR (1982b) Seed development and abscisic acid related to uneven ripening of Concord grapes. Proceedings Arkansas Sate Hort Soc. 103rd Ann. Mtg 108-113

  • Cawthon DL, Morris JR (1983) Uneven ripening of Concord grapes. Arkansas Farm Research 32:9

    Google Scholar 

  • Chiang GCK, Barua D, Kramer EM, Amasino RM, Donohue K (2009) Major flowering time gene, flowering locus C, regulates seed germination in Arabidopsis thaliana. PNAS 106:11661–11666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coombe BG (1980) Development of the grape berry. I. Effects of time of flowering and competition. Crop and Pasture Science 31:125–131

    Article  Google Scholar 

  • Coombe BG (1992) Research on development and ripening of the grape berry. AJEV 43:101–110

    Google Scholar 

  • Dai ZW, Ollat N, Gomes E, Decroocq S, Tandonnet J-P, Bordenave L, Pieri P, Hilbert G, Kappel C, van Leeuwen C, Vivin P, Delrot S (2011) Ecophysiological, genetic, and molecular causes of variation in grape berry weight and composition: a review. AJEV 62:413–425

    CAS  Google Scholar 

  • Davies C, Boss PK, Robinson SP (1997) Treatment of grape berries, a nonclimacteric fruit with a synthetic auxin, retards ripening and alters the expression of developmentally regulated genes. Plant Physiol 115:1155–1161

    CAS  PubMed  PubMed Central  Google Scholar 

  • Deluc LG, Quilici DR, Decendit A, Grimplet J, Wheatley MD, Schlauch KA, Mérillon J-M, Cushman JC, Cramer GR (2009) Water deficit alters differentially metabolic pathways affecting important flavor and quality traits in grape berries of Cabernet Sauvignon and Chardonnay. BMC Genom 10:212. doi:10.1186/1471-2164-10-212

    Article  Google Scholar 

  • Dorcey E, Urbez C, Blázquez MA, Carbonell J, Perez-Amador MA (2009) Fertilization-dependent auxin response in ovules triggers fruit development through the modulation of gibberellin metabolism in Arabidopsis. Plant J 58:318–332

    Article  CAS  PubMed  Google Scholar 

  • Dry PR, Longbottom ML, McLoughlin S, Johnson TE, Collins C (2010) Classification of reproductive performance of ten wine grape varieties. Aust J Grape Wine Res 16:47–55

    Article  Google Scholar 

  • Duchene E, Dumas V, Jaegli N, Merdinoglu D (2012) Deciphering the ability of different grapevine genotypes to accumulate sugar in berries. Aust J Grape Wine Res 18:319–328

    Article  Google Scholar 

  • Ebadi A, Sedgley M, May P, Coombe BG (1996) Seed development and abortion in Vitis vinifera L., cv. Chardonnay. Int J Plant Sci 157:703–712

    Article  Google Scholar 

  • Friend AP, Creasy GL, Trought MC, Lang A (2003) Use of tagging to trace capfall and development of individual Vitis vinifera L. cv. Pinot noir flowers. AJEV 54:313–317

    Google Scholar 

  • Friend AP, Trought MC, Creasy GL (2009) The influence of seed weight on the development and growth of berries and live green ovaries in Vitis vinifera L. cvs. Pinot Noir and Cabernet Sauvignon. Aust J Grape Wine Res 15:166–174

    Article  Google Scholar 

  • Gambetta GA, Matthews MA, Shaghasi TH, McElrone AJ, Castellarin SD (2010) Sugar and abscisic acid signaling orthologs are activated at the onset of ripening in grape. Planta 232:219–234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • García de Cortázar-Atauri I, Brisson N, Gaudillere JP (2009) Performance of several models for predicting budburst date of grapevine (Vitis vinifera L.). Int J Biometeorol 53:317–326

    Article  PubMed  Google Scholar 

  • Giribaldi M, Hartung W, Schubert A (2010) The effects of abscisic acid on grape berry ripening are affected by the timing of treatment. J Int Sci Vigne Vin 9–15

  • Given NK, Venis MA, Gierson D (1988) Hormonal regulation of ripening in the strawberry, a non-climacteric fruit. Planta 174:402–406

    Article  CAS  PubMed  Google Scholar 

  • Gorchov DL (1985) Fruit ripening asynchrony is related to variable seed number in Amelanchier and Vaccinium. Am J Bot 72:1939–1943

    Article  Google Scholar 

  • Gouthu S, Deluc LG (2015) Timing of ripening initiation in grape berries and its relationship to seed content and pericarp auxin levels. BMC Plant Biol 15:46

    Article  PubMed  PubMed Central  Google Scholar 

  • Gouthu S, Deluc LG, Maier CS, Morre J (2012) An Analytical Method to Quantify Three Plant Hormone Families in Grape Berry Using Liquid Chromatography and Multiple Reaction Monitoring Mass Spectrometry. In: Gang DR (ed) Phytochemicals, Plant Growth, and the Environment. Springer New York, 19–36

  • Gouthu S, O’Neil ST, Di Y, Ansarolia M, Megraw M, Deluc LG (2014) A comparative study of ripening among berries of the grape cluster reveals an altered transcriptional programme and enhanced ripening rate in delayed berries. J Exp Bot 65:5889–5902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gray JD, Coombe BG (2009) Variation in Shiraz berry size originates before fruitset but harvest is a point of resynchronisation for berry development after flowering. Aust J Grape Wine Res 15:156–165

    Article  Google Scholar 

  • Hollander M, Wolfe DA, Chicken E (2013) Nonparametric statistical methods. J Wiley New York

  • Jia HF, Chai YM, Li CL, Lu D, Luo JJ, Qin L, Shen Y-Y (2011) Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiol 157:188–199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jofuku KD, Omidyar PK, Gee Z, Okamuro JK (2005) Control of seed mass and seed yield by the floral homeotic gene APETALA2. PNAS 102:3117–3122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson PCD (2014) Extension of Nakagawa and Schielzeth’s R 2GLMM to random slopes models. Methods Ecol Evol 5:944–946

    Article  PubMed  PubMed Central  Google Scholar 

  • Kasimatis AN, Vilas EP, Swanson FH (1975) A Study of the Variability of Thompson Seedless’ Berries for Soluble Solids and Weight. AJEV 26:37–42

    Google Scholar 

  • Kontoudakis N, Esteruelas M, Fort F, Canals JM, De Freitas V, Zamora F (2011) Food Chem 124:767–774

    Article  CAS  Google Scholar 

  • Kühn N, Abello C, Godoy F, Delrot S, Arce-Johnson P (2014) Differential Behavior within a Grapevine Cluster: decreased Ethylene-Related Gene Expression Dependent on Auxin Transport Is Correlated with Low Abscission of First Developed Berries. PLoS One 65:4543–4559

    Google Scholar 

  • Kumar R, Khurana A, Sharma AK (2014) Role of plant hormones and their interplay in development and ripening of fleshy fruits. J Exp Bot 65:4561–4575

    Article  PubMed  Google Scholar 

  • Letcher SG, Chazdon RL (2009) Lianas and self-supporting plants during tropical forest succession. For Ecol Manage 257:2150–2156

    Article  Google Scholar 

  • Manning K (1994) Changes in gene expression during strawberry fruit ripening and their regulation by auxin. Planta 194:62–68

    Article  CAS  Google Scholar 

  • Marcelis L, Hofman-Eijer LB (1997) Effects of seed number on competition and dominance among fruits in Capsicum annuum L. Ann Bot 79:687–693

    Article  Google Scholar 

  • McAtee P, Karim S, Schaffer R, David K (2013) A dynamic interplay between phytohormones is required for fruit development, maturation, and ripening. Front Plant Sci 4:1–7

    Article  Google Scholar 

  • Milec Z, Valárik M, Bartoš J, Šafář J (2014) Can a late bloomer become and early bird? Tools for flowering time adjustment. Biotechnol Adv 32:200–214

    Article  PubMed  Google Scholar 

  • Nakagawa S, Schielzeth H (2012) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  • Nitsch JP, Pratt C, Nitsch C, Shaulis NJ (1960) Natural growth substances in Concord and Concord Seedless grapes in relation to berry development. Am J Bot 47:566–576

    Article  CAS  Google Scholar 

  • Ozga JA, van Huizen R, Reinecke DM (2002) Hormone and seed-specific regulation of pea fruit growth. Plant Physiol 128:1379–1389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pagay V, Cheng L (2010) Variability in berry maturation of Concord and Cabernet franc in a cool climate. AJEV 61:61–67

    Google Scholar 

  • Parker AK, de Cortázar-Atauri IG, van Leeuwen C, Chuine I (2011) General phenological model to characterise the timing of flowering and veraison of Vitis vinifera L. Aust J Grape Wine Res 17:206–216

    Article  Google Scholar 

  • Parker A, de Cortázar-Atauri IG, Chuine I, Barbeau G, Bois B, Boursiquot J-M, Cahurel J-Y, Claverie M, Dufourcq T, Gény L, Guimerteau G, Hofmann RW, Jacquet O, Lacombe T, Monamy C, Ojeda H, Panigai L, Payan J-C, Lovelle BR, Rouchaud E, Schneider C, Spring J-L, Storchi P, Tomasi D, Trambouze W, Trought M, van Leeuwen C (2013) Classification of varieties for their timing of flowering and veraison using a modelling approach: a case study for the grapevine species Vitis vinifera L. Agric For Meteorol 180:249–264

    Article  Google Scholar 

  • Parker AK, Hofmann RW, van Leeuwen C, McLachlan ARG, Trought MCT (2014) Leaf area to fruit mass ratio determines the time of veraison in Sauvignon Blanc and Pinot Noir grapevines. Aust J Grape Wine Res 20:422–431

    Article  CAS  Google Scholar 

  • Pattison RJ, Catalá C (2012) Evaluating auxin distribution in tomato (Solanum lycopersicum) through an analysis of the PIN and AUX/LAX gene families. Plant J 70:585–598

    Article  CAS  PubMed  Google Scholar 

  • Pattison RJ, Csukasi F, Catalá C (2014) Mechanisms regulating auxin action during fruit development. Physiol Plantarum 151:62–72

    Article  CAS  Google Scholar 

  • Pisciotta A, di Lorenzo R, Barbagallo MG (2014) Berry characterisation of cv Shiraz according to position on the Rachis. South African J Enol Viticult 34:100–107

    Google Scholar 

  • Prudent M, Dai ZW, Génard M, Bertin N (2014) Resource competition modulates the seed number—fruit size relationship in a genotype-dependent manner: a modeling approach in grape and tomato. Ecol Model 290:54–64

    Article  Google Scholar 

  • Ramsey F, Schafer D (2012) The statistical sleuth: a course in methods of data analysis. Duxbury/Thomson Learning, Australia

    Google Scholar 

  • Rapp A, Klenert M (1974) Einfluss der Samen auf die Beerenreife bei Vitis vinifera L. Vitis 13:222–232

    Google Scholar 

  • Ristic R, Iland PG (2005) Relationships between seed and berry development of Vitis vinifera L. cv Shiraz: developmental changes in seed morphology and phenolic composition. Aust J Grape Wine Res 11:43–58

    Article  CAS  Google Scholar 

  • Ruan Y-L, Patrick JW, Bouzayen M, Osorio S, Fernie AR (2012) Molecular regulation of seed and fruit set. Trends Plant Sci 17:656–665

    Article  CAS  PubMed  Google Scholar 

  • Sato S, Peet MM, Gardner RG (2001) Formation of parthenocarpic fruit, undeveloped flowers and aborted flowers in tomato under moderately elevated temperatures. Sci Hortic 90:243–254

    Article  Google Scholar 

  • Selvaraj Y, Pal DK, Singh R, Roy TK (1994) Biochemistry of uneven ripening in gulabi grape. J Food Biochem 18:325–340

    Article  Google Scholar 

  • Staudt G (1999) Opening of flowers and time of anthesis in grapevines, Vitis vinifera L. Vitis 38:15–20

    Google Scholar 

  • Stephenson AG, Devlin B, Horton JB (1988) the effects of seed number and prior fruit dominance on the pattern of fruit production in Cucurbits pepo (Zucchini Squash). Ann Bot 62:653–661

    Google Scholar 

  • Sundberg E, Ostergaard L (2009) Distinct and dynamic auxin activities during reproductive development. Cold Spring Harb Perspect Biol 1:1–14

    Article  Google Scholar 

  • Symons GM, Chua Y-J, Ross JJ, Quittenden LJ, Davies NW, Reid JB (2012) Hormonal changes during non-climacteric ripening in strawberry. J Exp Bot 63:4741–4750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tarter ME, Keuter SE (2005) Effect of rachis position on size and maturity of Cabernet Sauvignon berries. AJEV 56:86–89

    Google Scholar 

  • R Core Team (2015). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed Feb 2016

  • Tiwari A, Vivian-Smith A, Ljung K, Offringa R, Heuvelink E (2013) Physiological and morphological changes during early and later stages of fruit growth in Capsicum annuum. Physiol Plant 147:396–406

    Article  CAS  PubMed  Google Scholar 

  • Vasconcelos MC, Greven M, Winefield CS, Trought MCT, Raw V (2009) The flowering process of Vitis vinifera: a review. AJEV 60:411–434

    CAS  Google Scholar 

  • Wheeler S, Loveys B, Ford C, Davies C (2009) The relationship between the expression of abscisic acid biosynthesis genes, accumulation of abscisic acid and the promotion of Vitis vinifera L. berry ripening by abscisic acid. Aust J Grape Wine Res 15:195–204

    Article  CAS  Google Scholar 

  • Zhang X, Luo G, Wang R, Wang J (2003) Growth and developmental responses of seeded and seedless grape berries to shoot girdling

  • Ziliotto F, Corso M, Rizzini FM, Rasori A, Botton A, Bonghi C (2012) Grape berry ripening delay induced by a pre-véraison NAA treatment is paralleled by a shift in the expression pattern of auxin- and ethylene-related genes. BMC Plant Biol 12:185. doi:10.1186/1471-2229-12-185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors are grateful for ongoing support from the Oregon Wine Research Institute, the Oregon Wine Board, and Oregon State University’s College of Agriculture. We are additionally thankful to undergraduate students—Jamie Erway, Ross Henried, Matthew Moreno, Kathryn Ressler, Evan Sadlou, and Nolan Sekermestrovich, who participated in the extensive flower tagging for this study. We also are immensely grateful to Dr. Yuan Jiang for his guidance regarding our statistical methods.

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Correspondence to Laurent G. Deluc.

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Vondras, A.M., Gouthu, S., Schmidt, J.A. et al. The contribution of flowering time and seed content to uneven ripening initiation among fruits within Vitis vinifera L. cv. Pinot noir clusters. Planta 243, 1191–1202 (2016). https://doi.org/10.1007/s00425-016-2474-x

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