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Physical rupture of the xylem in developing sweet cherry fruit causes progressive decline in xylem sap inflow rate

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Abstract

Main conclusion

Xylem flow is progressively shut down during maturation beginning with minor veins at the stylar end and progressing to major veins and finally to bundles at the stem end.

This study investigates the functionality of the xylem vascular system in developing sweet cherry fruit (Prunus avium L.). The tracers acid fuchsin and gadoteric acid were fed to the pedicel of detached fruit. The tracer distribution was studied using light microscopy and magnetic resonance imaging. The vasculature of the sweet cherry comprises five major bundles. Three of these supply the flesh; two enter the pit to supply the ovules. All vascular bundles branch into major and minor veins that interconnect via numerous anastomoses. The flow in the xylem as indexed by the tracer distribution decreases continuously during development. The decrease is first evident at the stylar (distal) end of the fruit during pit hardening and progresses basipetally towards the pedicel (proximal) end of the fruit at maturity. That growth strains are the cause of the decreased conductance is indicated by: elastic strain relaxation after tissue excision, the presence of ruptured vessels in vivo, the presence of intrafascicular cavities, and the absence of tyloses.

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Abbreviations

Gd DOTA:

Gadoteric acid

MRI:

Magnetic resonance imaging

RH:

Relative humidity

References

  • Bernstein Z, Lustig I (1981) A new method of firmness measurement of grape berries and other juicy fruit. Vitis 20:15–21

    Google Scholar 

  • Bernstein Z, Lustig I (1985) Hydrostatic methods of measurement of firmness and turgor pressure of grape berries (Vitis vinifera L.). Sci Hortic 25:129–136

    Article  Google Scholar 

  • Bondada BR, Matthews MA, Shackel KA (2005) Functional xylem in the post-veraison grape berry. J Exp Bot 56:2949–2957

    Article  CAS  PubMed  Google Scholar 

  • Brüggenwirth M, Knoche M (2015) Xylem conductance of sweet cherry pedicels. Trees 29:1851–1860. doi:10.1007/s00468-015-1266-4

    Article  Google Scholar 

  • Brüggenwirth M, Winkler A, Knoche M (2016) Xylem, phloem, and transpiration flows in developing sweet cherry fruit. Trees 30:1821–1830. doi:10.1007/s00468-016-1415-4

    Article  Google Scholar 

  • Bukovac MJ (1971) The nature and chemical promotion of abscission in maturing cherry fruit. HortScience 6:385–388

    CAS  Google Scholar 

  • Chatelet DS, Rost TL, Shackel KA, Matthews MA (2008a) The peripheral xylem of grapevine (Vitis vinifera). 1. Structural integrity in post-veraison berries. J Exp Bot 59:1987–1996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chatelet DS, Rost TL, Matthews MA, Shackel KA (2008b) The peripheral xylem of grapevine (Vitis vinifera) berries. 2. Anatomy and development. J Exp Bot 59:1997–2007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choat B, Gambetta GA, Shackel KA, Matthews MA (2009) Vascular function in grape berries across development and its relevance to apparent hydraulic isolation. Plant Physiol 151:1677–1687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christensen JV (1996) Rain-induced cracking of sweet cherries: Its causes and prevention. In: Webster AD, Looney NE (eds) Cherries: crop physiology, production and uses. CAB Intl, Wallingford, pp 297–327

    Google Scholar 

  • Dean RJ, Stait-Gardener T, Clarke SJ, Rogiers SY, Bobek G, Price WS (2014) Use of diffusion magnetic resonance imaging to correlate the developmental changes in grape berry tissue structure with water diffusion pattern. Plant Methods 10:35. doi:10.1186/1746-4811-10-35

    Article  PubMed  Google Scholar 

  • Dichio B, Remorini D, Lang S (2003) Developmental changes in xylem functionality in kiwifruit fruit: implications for fruit calcium accumulation. Acta Hortic 610:191–195

    Article  Google Scholar 

  • Dichio B, Montanaro G, Mazzeo M, Lang A (2011) Does dye infusion indicate xylem functionality in kiwifruit? Acta Hortic 913:353–355

    Article  Google Scholar 

  • Drazeta L, Lang A, Morgan L, Volz R, Jameson PE (2001) Bitter pit and vascular function in apples. Acta Hortic 564:387–392

    Article  Google Scholar 

  • Dražeta L, Lang A, Hall AJ, Volz RK, Jameson PE (2004) Causes and effects of changes in xylem functionality in apple fruit. Ann Bot 93:275–282

    Article  PubMed  PubMed Central  Google Scholar 

  • Düring H, Lang A, Oggionni F (1987) Patterns of water flow in Riesling berries in relation to developmental changes in their xylem morphology. Vitis 26:123–131

    Google Scholar 

  • Findlay N, Oliver KJ, Nil N, Coombe BG (1987) Solute accumulation by grape pericarp cells. IV. Perfusion of pericarp apoplast via the pedicel and evidence for xylem malfunction in ripening berries. J Exp Bot 38:668–679

    Article  Google Scholar 

  • Geyer U, Schönherr J (1988) In vitro test for effects of surfactants and formulations on permeability of plant cuticles. In: Cross B, Scher HB (eds) Pesticide formulations: innovations and developments. American Chemical Society, Washington, pp 22–33

    Chapter  Google Scholar 

  • Grimm E, Peschel S, Becker T, Knoche M (2012) Stress and strain in the sweet cherry skin. J Am Soc Hortic Sci 137:383–390

    Google Scholar 

  • Ho LC, Grange RI, Picken AJ (1987) An analysis of the accumulation of water and dry matter in tomato fruit. Plant Cell Environ 10:157–162

    Google Scholar 

  • Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137A–138A

    Google Scholar 

  • Keller M, Smith JP, Bondada BR (2006) Ripening grape berries remain hydraulically connected to the shoot. J Exp Bot 57:2577–2587

    Article  CAS  PubMed  Google Scholar 

  • Kenouche S, Perrier M, Bertin N, Larionova J, Ayadi A, Zanca M, Long J, Bezzi N, Stein PC, Guari Y, Cieslak M, Godin C, Goze-Bac C (2014) In vivo quantitative NMR imaging of fruit tissue during growth using spoiled gradient echo sequence. Magn Reson Imaging 32:1418–1427

    Article  CAS  PubMed  Google Scholar 

  • Knipfer T, Fei J, Gambetta GA, McElrone AJ, Shackel KA, Matthews MA (2015) Water transport properties of the grape pedicel during fruit development: insights into xylem anatomy and function using microtomography. Plant Physiol 168:1590–1602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knoche M, Peschel S, Hinz M, Bukovac MJ (2001) Studies on water transport through the sweet cherry surface: II. Conductance of the cuticle in relation to fruit development. Planta 213:927–936

    Article  CAS  PubMed  Google Scholar 

  • Knoche M, Beyer M, Peschel S, Oparlakov B, Bukovac MJ (2004) Changes in strain and deposition of cuticle in developing sweet cherry fruit. Physiol Plant 120:667–677

    Article  CAS  PubMed  Google Scholar 

  • Knoche M, Grimm E, Schlegel HJ (2014) Mature sweet cherries have low turgor. J Am Soc Hortic Sci 139:3–12

    Google Scholar 

  • Kumar K, Sukumaran K, Taylor S, Chang AC, Nunn AD, Tweedle MF (1994) Partition coefficients (log P) and some capacity factors (k′) of some Gd(III) complexes of linear and macrocyclic polyamino carboxylates. J Liq Chromatogr 17:3735–3746

    Article  CAS  Google Scholar 

  • Lai X, Khanal BP, Knoche M (2016) Mismatch between cuticle deposition and area expansion in fruit skins allows potentially catastrophic buildup of elastic strain. Planta 244:1145–1156

    Article  CAS  PubMed  Google Scholar 

  • Lang A (1990) Xylem, phloem and transpiration flows in developing apple fruits. J Exp Bot 41:645–651

    Article  Google Scholar 

  • Lang A, Düring H (1990) Grape berry splitting and some mechanical properties of the skin. Vitis 29:61–70

    Google Scholar 

  • Lang A, Ryan KG (1994) Vascular development and sap flow in apple pedicels. Ann Bot 74:381–388

    Article  Google Scholar 

  • Lang A, Volz RK (1993) Leaf area, xylem cycling and Ca status in apples. Acta Hortic 343:89–92

    Article  Google Scholar 

  • Lang A, Volz RK (1998) Spur leaves increase calcium in young apples by promoting xylem inflow and outflow. J Am Soc Hortic Sci 123:956–960

    Google Scholar 

  • Lindner U, Lingott J, Richter S, Jakubowski N, Panne U (2013) Speciation of gadolinium in surface water samples and plants by hydrophilic interaction chromatography hyphenated with inductively coupled plasma mass spectrometry. Anal Bioanal Chem 405:1865–1873

    Article  CAS  PubMed  Google Scholar 

  • Mazzeo M, Dichio B, Clearwater MJ, Montanaro G, Xiloyannis C (2013) Hydraulic resistance of developing Actinidia fruit. Ann Bot 112:197–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morandi B, Manfrini L, Losciale P, Zibordi M, Grappadelli LC (2010) Changes in vascular and transpiration flows affect the seasonal and daily growth of kiwifruit (Actinidia deliciosa) berry. Ann Bot 105:913–923

    Article  PubMed  PubMed Central  Google Scholar 

  • Moriwaki S, Terada Y, Kose K, Haishi T, Sekozawa Y (2014) Visualization and quantification of vascular structure of fruit using magnetic resonance microimaging. Appl Magn Reson 45:517–525

    Article  Google Scholar 

  • Nordey T, Léchaudel M, Génard M (2015) The decline in xylem flow to mango fruit at the end of its development is related to the appearance of embolism in the fruit pedicel. Funct Plant Biol 42:668–675

    Article  CAS  Google Scholar 

  • Opara LU, Studman CJ, Banks NH (1997) Fruit skin splitting and cracking. Hortic Rev 19:217–262

    Google Scholar 

  • Pope JM, Jonas D, Walker RR (1993) Applications of NMR micro-imaging to the study of water, lipid, and carbohydrate distribution in grape berries. Protoplasma 173:177–186

    Article  CAS  Google Scholar 

  • Rančić D, Quarrie SP, Radošević R, Terzić M, Pećinar I, Stikić R, Jansen S (2010) The application of various anatomical techniques for studying the hydraulic network in tomato fruit pedicels. Protoplasma 246:25–31

    Article  PubMed  Google Scholar 

  • Redgwell RJ, MacRae E, Hallett I, Fischer M, Perry J, Harker R (1997) In vivo and in vitro swelling of cell walls during fruit ripening. Planta 203:162–173

    Article  CAS  Google Scholar 

  • Rogiers SY, Smith JA, White R, Keller M, Holzapfel BP, Virgona JM (2001) Vascular function in berries of Vitis vinifera (L) cv. Shiraz. Aust J Grape Wine Res 7:46–51

    Article  Google Scholar 

  • Schumann C, Schlegel HJ, Grimm E, Knoche M, Lang A (2014) Water potential and its components in developing sweet cherry. J Am Soc Hortic Sci 139:349–355

    Google Scholar 

  • Sterling C (1953) Developmental anatomy of the fruit of Prunus domestica L. Bull Torrey Bot Club 80:457–477

    Article  Google Scholar 

  • Sterling C (1964) Comparative morphology of the carpel in the Rosaceae. I. Prunoidae: Prunus. Am J Bot 51:36–44

    Article  Google Scholar 

  • Stösser R, Rasmussen HP, Bukovac MJ (1969) A histological study of abscission layer formation in cherry fruits during maturation. J Am Soc Hortic Sci 94:239–243

    Google Scholar 

  • Thomas TR, Matthews MA, Shackel KA (2006) Direct in situ measurement of cell turgor in grape (Vitis vinifera L.) berries during development and in response to plant water deficits. Plant Cell Environ 29:993–1001

    Article  PubMed  Google Scholar 

  • Thomas TR, Shackel KA, Matthews MA (2008) Mesocarp cell turgor in Vitis vinifera L. berries throughout development and its relation to firmness, growth, and the onset of ripening. Planta 228:1067–1076

    Article  CAS  PubMed  Google Scholar 

  • Tukey HB, Young JO (1939) Histological study of the developing fruit of the sour cherry. Bot Gaz 100:723–749

    Article  Google Scholar 

  • Van Dusschoten D, Metzner R, Kochs J, Postma JA, Pflugfelder D, Bühler J, Schurr U, Jahnke S (2016) Quantitative 3D analysis of plant roots growing in soil using magnetic resonance imaging. Plant Physiol 170:1176–1188

    PubMed  PubMed Central  Google Scholar 

  • Winkler A, Brüggenwirth M, Ngo NS, Knoche M (2016) Fruit apoplast tension draws xylem water into mature sweet cherries. Sci Hortic 209:270–278

    Article  Google Scholar 

  • Wittenbach VA, Bukovac MJ (1972) An anatomical and histochemical study of abscission in maturing sweet cherry fruit. J Am Soc Hortic Sci 97:214–219

    Google Scholar 

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Acknowledgements

We thank Mr. Dieter Reese (Martin-Luther-University Halle-Wittenberg) for building the sample holder for MRI, and Dr. Alexander Lang (Sandy Lang Ltd, Eastbourne, NZ) and Dr. Siegfried Jahnke (Forschungszentrum Jülich, IBG-2, Germany) for thoughtful comments on this manuscript.

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Authors and Affiliations

  1. Abteilung Obstbau, Institut für Gartenbauliche Produktionssysteme, Leibniz Universität Hannover, Herrenhäuser Straße 2, 30419, Hannover, Germany

    Eckhard Grimm, Andreas Winkler & Moritz Knoche

  2. IBG-2: Pflanzenwissenschaften, Forschungszentrum Jülich, Wilhelm-Johnen-Straße, 52428, Jülich, Germany

    Daniel Pflugfelder & Dagmar van Dusschoten

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  1. Eckhard Grimm
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  5. Moritz Knoche
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Correspondence to Moritz Knoche.

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Grimm, E., Pflugfelder, D., van Dusschoten, D. et al. Physical rupture of the xylem in developing sweet cherry fruit causes progressive decline in xylem sap inflow rate. Planta 246, 659–672 (2017). https://doi.org/10.1007/s00425-017-2719-3

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  • DOI: https://doi.org/10.1007/s00425-017-2719-3

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