Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Solute transport within grape berries inferred from the paramagnetic properties of manganese

Ryan J. Dean A , Simon J. Clarke B D , Suzy Y. Rogiers B C , Timothy Stait-Gardner A and William S. Price A B E
+ Author Affiliations
- Author Affiliations

A Nanoscale Organisation and Dynamics Group, Western Sydney University, Penrith, NSW 2751, Australia.

B National Wine and Grape Industry Centre, Charles Sturt University, Locked Bag 588, Wagga Wagga, NSW 2678, Australia.

C National Wine and Grape Industry Centre, New South Wales Department of Primary Industries, Locked Bag 588, Wagga Wagga, NSW 2678, Australia.

D Queensland Alliance for Agriculture and Food Innovation, the University of Queensland, PO Box 102, Toowoomba, Qld 4350, Australia.

E Corresponding author. Email: w.price@uws.edu.au

Functional Plant Biology 44(10) 969-977 https://doi.org/10.1071/FP16406
Submitted: 13 November 2016  Accepted: 28 May 2017   Published: 14 July 2017

Abstract

Tracer compounds used for studying solute transport should ideally have identical functions and transport properties to the molecules they are designed to mimic. Unfortunately, the xylem-mobile tracer compounds currently used to infer solute transport mechanisms in botanical specimens such as the fruit of the grapevine, Vitis vinifera L., are typically xenobiotic and have difficulty exiting the xylem during berry ripening. Here it is demonstrated that the transport of paramagnetic Mn ions can be indirectly observed within the grape berry, using relaxation magnetic resonance imaging (MRI). Mn ions from a 10 mM Mn chloride solution were taken up into the grape berry via the pedicel and moved through the peripheral vasculature before exiting into surrounding pericarp tissue. Mn did not exit evenly across the berry, implying that the berry xylem influences which sites Mn exits the vasculature ‘downstream’ of the berry pedicel. It was also found that when the cellular membranes of pericarp tissues were disrupted, the distribution of Mn through the pericarp tissue became noticeably more homogenous. This indicates that the cellular membranes of extra-vascular cells affect the spatial distribution of Mn across the berry extra-vascular pericarp tissue upon exiting the grape berry vasculature.

Additional keywords: extra-vascular transport, manganese, paramagnetically enhanced magnetic resonance imaging, xylem tracer.


References

Bačić G, Schara M, Ratković S (1993) An ESR study of manganese binding in plant tissue. General Physiology and Biophysics 12, 49–54.

Bartacek J, Vergeldt FJ, Maca J, Gerkema E, Van As H, Lens PNL (2016) Iron, cobalt, and gadolinium transport in methanogenic granules measured by 3D magnetic resonance imaging. Frontiers in Environmental Science 4, 13
Iron, cobalt, and gadolinium transport in methanogenic granules measured by 3D magnetic resonance imaging.Crossref | GoogleScholarGoogle Scholar |

Bloch F (1946) Nuclear induction. Physical Review 70, 460–474.
Nuclear induction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaH2sXnsFOq&md5=eccd8f96743d3fb3e321ca363a4f193eCAS |

Bondada BR, Matthews MA, Shackel KA (2005) Functional xylem in the post-veraison grape berry. Journal of Experimental Botany 56, 2949–2957.
Functional xylem in the post-veraison grape berry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFCjt7jF&md5=04943d40680ce57b7d4db0d7a856bdc4CAS |

Buckley DL, Parker GJM (2005) Measuring contrast agent concentration in T 1-weighted dynamic contrast-enhanced MRI. In ‘Dynamic contrast-enhanced magnetic resonance imaging in oncology’. (Eds A Jackson, DL Buckley, GJM Parker) pp. 69–79. (Springer: Berlin)

Canny MJ (1990) Tansley Review No. 22. What becomes of the transpiration stream? New Phytologist 114, 341–368.
Tansley Review No. 22. What becomes of the transpiration stream?Crossref | GoogleScholarGoogle Scholar |

Chatelet DS, Rost TL, Shackel KA, Matthews MA (2008) The peripheral xylem of grapevine (Vitis vinifera). 1. Structural integrity in post-veraison berries. Journal of Experimental Botany 59, 1987–1996.
The peripheral xylem of grapevine (Vitis vinifera). 1. Structural integrity in post-veraison berries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmvFWrsL8%3D&md5=b66a023120ba8a4e357f1f76d39d7bb9CAS |

Chen C-w, Cohen JS, Myers CE, Sohn M (1984) Paramagnetic metalloporphyrins as potential contrast agents in NMR imaging. FEBS Letters 168, 70–74.
Paramagnetic metalloporphyrins as potential contrast agents in NMR imaging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXkt1SjsbY%3D&md5=df98555c6e2a4cac71db1bf413c565eaCAS |

Choat B, Gambetta GA, Shackel KA, Matthews MA (2009) Vascular function in grape berries across development and its relevance to apparent hydraulic isolation. Plant Physiology 151, 1677–1687.
Vascular function in grape berries across development and its relevance to apparent hydraulic isolation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVCjsbfJ&md5=b0db4e2b4fe46f9e884a1280db668820CAS |

Connelly A, Lohman JAB, Loughman BC, Quiquampoix H, Ratcliffe RG (1987) High resolution imaging of plant tissues by NMR. Journal of Experimental Botany 38, 1713–1723.
High resolution imaging of plant tissues by NMR.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXivFWj&md5=95ac736cef881c72238c7487425b07e5CAS |

Creasy GL, Price SF, Lombard PB (1993) Evidence for xylem discontinuity in Pinot noir and Merlot grapes: dye uptake and mineral composition during berry maturation. American Journal of Enology and Viticulture 44, 187–192.

Dean RJ, Bobek G, Stait-Gardner T, Clarke SJ, Rogiers SY, Price WS (2016) Time-course study of grape berry split using diffusion magnetic resonance imaging. Australian Journal of Grape and Wine Research 22, 240–244.
Time-course study of grape berry split using diffusion magnetic resonance imaging.Crossref | GoogleScholarGoogle Scholar |

Donahue KM, Burstein D, Manning WJ, Gray ML (1994) Studies of Gd-DTPA relaxivity and proton exchange rates in tissue. Magnetic Resonance in Medicine 32, 66–76.
Studies of Gd-DTPA relaxivity and proton exchange rates in tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlslCjurw%3D&md5=edb8eb7cbb28acc367bf8e66ddefcd6aCAS |

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.

Einstein A (1956) ‘Investigations on the theory of the Brownian movement.’ (Dover Publications: New York)

El‐Jaoual T, Cox DA (1998) Manganese toxicity in plants. Journal of Plant Nutrition 21, 353–386.
Manganese toxicity in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtlWltrg%3D&md5=33fc2e5d1fc68f8bd1880a393bfd3a71CAS |

Fick A (1855) On liquid diffusion. The London, Edinburgh, and Dublin Philosophical Magazine and Journal of Science 10, 30–39.

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. Journal of Experimental Botany 38, 668–679.
Solute accumulation by grape pericarp cells: IV. Perfusion of pericarp apoplast via the pedicel and evidence for xylem malfunction in ripening berries.Crossref | GoogleScholarGoogle Scholar |

Gonzalez ME, Barrett DM, McCarthy MJ, Vergeldt FJ, Gerkema E, Matser AM, Van As H (2010) 1H-NMR study of the impact of high pressure and thermal processing on cell membrane integrity of onions. Journal of Food Science 75, E417–E425.
1H-NMR study of the impact of high pressure and thermal processing on cell membrane integrity of onions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1GgtbzE&md5=5cd415cdcde052317543996b5cf4d080CAS |

Graf von der Schulenburg DA, Holland DJ, Paterson-Beedle M, Macaskie LE, Gladden LF, Johns ML (2008) Spatially resolved quantification of metal ion concentration in a biofilm-mediated ion exchanger. Biotechnology and Bioengineering 99, 821–829.
Spatially resolved quantification of metal ion concentration in a biofilm-mediated ion exchanger.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXit1Kru7k%3D&md5=1d132f97cdbbe668be21d506aebd35e8CAS |

Grignon N, Touraine B, Durand M (1989) 6(5)carboxyfluorescein as a tracer of phloem sap translocation. American Journal of Botany 76, 871–877.
6(5)carboxyfluorescein as a tracer of phloem sap translocation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXlslWgs7w%3D&md5=bde0b063db086a125af9d617a8c2ced9CAS |

Hennig J, Nauerth A, Friedburg H (1986) RARE imaging: a fast imaging method for clinical MR. Magnetic Resonance in Medicine 3, 823–833.
RARE imaging: a fast imaging method for clinical MR.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s7ktlKktw%3D%3D&md5=681dad431cbb6b1b5d01384163e84043CAS |

Heyes JA, Clark CJ (2003) Magnetic resonance imaging of water movement through asparagus. Functional Plant Biology 30, 1089–1095.
Magnetic resonance imaging of water movement through asparagus.Crossref | GoogleScholarGoogle Scholar |

Keller M, Smith JP, Bondada BR (2006) Ripening grape berries remain hydraulically connected to the shoot. Journal of Experimental Botany 57, 2577–2587.
Ripening grape berries remain hydraulically connected to the shoot.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xotl2mt70%3D&md5=6dd377776a92f0f13a9eb397b18e7a82CAS |

Kessissoglou DP (1995) Manganese-proteins and enzymes and relevant trinuclear synthetic complexes. In ‘Bioinorganic chemistry: An inorganic perspective of life’. (Ed. DP Kessissoglou) pp. 299–320. (Springer: Greece)

Koizumi M, Kano H (2015) Tracking manganese ion uptake and transport by the root system of broad bean plants by micro-magnetic resonance imaging. American Journal of Biology and Life Sciences 3, 102–107.

Koizumi M, Ishida N, Kano H (1992) Imaging Mn2+ uptake of a maize shoot by an NMR microscope. The Botanical Magazine 105, 667–671.
Imaging Mn2+ uptake of a maize shoot by an NMR microscope.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlsFGht78%3D&md5=1d0864085fb48b2c47f3860b405f2739CAS |

Lauterbur PC, Mendonca-Dias MH, Rudin AM (1978) Augmentation of tissue water proton spin-lattice relaxation rates by in vivo addition of paramagnetic ions. In ‘Frontiers of biological energetics’. (Eds PL Sutton, JS Leigh, A Scarpa) pp. 752–759. (Academic Press: New York)

Levitt MH (2001) ‘Spin dynamics: basics of nuclear magnetic resonance.’ (Wiley: New York)

McRobbie DW, Moore EA, Graves MJ, Prince MR (2006) ‘MRI from picture to proton.’ (Cambridge University Press: Cambridge, UK)

Mendonça-Dias MH, Gaggelli E, Lauterbur PC (1983) Paramagnetic contrast agents in nuclear magnetic resonance medical imaging. Seminars in Nuclear Medicine 13, 364–376.
Paramagnetic contrast agents in nuclear magnetic resonance medical imaging.Crossref | GoogleScholarGoogle Scholar |

Mou D, Yao Y, Yang Y, Zhang Y, Tian C, Achal V (2011) Plant high tolerance to excess manganese related with root growth, manganese distribution and antioxidative enzyme activity in three grape cultivars. Ecotoxicology and Environmental Safety 74, 776–786.
Plant high tolerance to excess manganese related with root growth, manganese distribution and antioxidative enzyme activity in three grape cultivars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlvVequr0%3D&md5=c0ffd847d7688e163595c26d88de8bb2CAS |

Mullins M, Bouquet A, Williams L (1992) ‘Biology of the grapevine.’ (Cambridge University Press: Cambridge, UK)

Muñoz-Robredo P, Robledo P, Manríquez D, Molina R, Defilippi BG (2011) Characterization of sugars and organic acids in commercial varieties of table grapes. Chilean Journal of Agricultural Research 71, 452–458.
Characterization of sugars and organic acids in commercial varieties of table grapes.Crossref | GoogleScholarGoogle Scholar |

Pykett IL, Mansfield P (1978) A line scan image study of a tumorous rat leg by NMR. Physics in Medicine and Biology 23, 961–967.
A line scan image study of a tumorous rat leg by NMR.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1M%2FlsFWrtQ%3D%3D&md5=9e6f5b2ef6322241ca7e29f24d439a63CAS |

Rogiers SY, Smith JA, White R, Keller M, Holzapfel BP, Virgona JM (2001) Vascular function in berries of Vitis vinifera (L) cv. Shiraz. Australian Journal of Grape and Wine Research 7, 47–51.
Vascular function in berries of Vitis vinifera (L) cv. Shiraz.Crossref | GoogleScholarGoogle Scholar |

Rogiers SY, Greer D, Hatfield J, Orchard B, Keller M (2006) Mineral sinks within ripening grape berries (Vitis vinifera L.). Vitis 45, 115–123.

Snaar JEM, Van As H (1992) Probing water compartments and membrane permeability in plant cells by 1H NMR relaxation measurements. Biophysical Journal 63, 1654–1658.
Probing water compartments and membrane permeability in plant cells by 1H NMR relaxation measurements.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXns1Cgug%3D%3D&md5=44b6c124552e9dff8783d33118215006CAS |

Socha AL, Guerinot ML (2014) Mn-euvering manganese: the role of transporter gene family members in manganese uptake and mobilization in plants. Frontiers in Plant Science 5, 106
Mn-euvering manganese: the role of transporter gene family members in manganese uptake and mobilization in plants.Crossref | GoogleScholarGoogle Scholar |

Springer CS, Jr (1994) Physicochemical principles influencing magnetopharmaceuticals. In ‘NMR in physiology and biomedicine’. (Ed. RJ Gillies) pp. 75–99. (Academic Press: San Diego, CA, USA)

Tarbouriech N, Charnock SJ, Davies GJ (2001) Three-dimensional structures of the Mn and Mg dTDP complexes of the family GT-2 glycosyltransferase SpsA: a comparison with related NDP-sugar glycosyltransferases. Journal of Molecular Biology 314, 655–661.
Three-dimensional structures of the Mn and Mg dTDP complexes of the family GT-2 glycosyltransferase SpsA: a comparison with related NDP-sugar glycosyltransferases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXosl2ju7o%3D&md5=1e16fdf517a595625b58d097f2585a55CAS |

Van As H (2007) Intact plant MRI for the study of cell water relations, membrane permeability, cell-to-cell and long distance water transport. Journal of Experimental Botany 58, 743–756.
Intact plant MRI for the study of cell water relations, membrane permeability, cell-to-cell and long distance water transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXislCrt70%3D&md5=ab4b3deee416ca83aa25f1593a7a16c2CAS |

van Ieperen W, van Meeteren U, van Gelder H (2000) Fluid ionic composition influences hydraulic conductance of xylem conduits. Journal of Experimental Botany 51, 769–776.
Fluid ionic composition influences hydraulic conductance of xylem conduits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtF2jsLw%3D&md5=cd4e3f48ed6b9da3d24b2e1de931cefaCAS |

Yao Y, Xu G, Mou D, Wang J, Ma J (2012) Subcellular Mn compartation, anatomic and biochemical changes of two grape varieties in response to excess manganese. Chemosphere 89, 150–157.
Subcellular Mn compartation, anatomic and biochemical changes of two grape varieties in response to excess manganese.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XosValurc%3D&md5=e00a8a745cec932acee397bdf2574cbdCAS |

Zhang X-Y, Wang X-L, Wang X-F, Xia G-H, Pan Q-H, Fan R-C, Wu F-Q, Yu X-C, Zhang D-P (2006) A shift of phloem unloading from symplasmic to apoplasmic pathway is involved in developmental onset of ripening in grape berry. Plant Physiology 142, 220–232.
A shift of phloem unloading from symplasmic to apoplasmic pathway is involved in developmental onset of ripening in grape berry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpvVKhsrc%3D&md5=52b9a9969c1e661ac760f4f20ef1e384CAS |

Zwieniecki MA, Melcher PJ, Holbrook NM (2001) Hydrogel control of xylem hydraulic resistance in plants. Science 291, 1059–1062.
Hydrogel control of xylem hydraulic resistance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtFGksLY%3D&md5=7284d8d69886e57a030ff1b5d30bc8b0CAS |