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Plant function and evolutionary biology
RESEARCH ARTICLE

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

Thibault Nordey A C , Mathieu Léchaudel A and Michel Génard B
+ Author Affiliations
- Author Affiliations

A Centre de coopération internationale en recherche agronomique pour le développement (CIRAD), unité propre de recherche: fonctionnement agroécologique et performances des systèmes de culture horticoles, 97455 Saint-Pierre, La Réunion, France.

B Institut national de recherche agronomique (INRA), unité de recherche 1115: Plantes et systèmes de culture horticoles, Domaine St Paul, Site Agroparc, 84914 Avignon cedex 9, France.

C Corresponding author. Email: thibault.nordey@cirad.fr

Functional Plant Biology 42(7) 668-675 https://doi.org/10.1071/FP14306
Submitted: 4 November 2014  Accepted: 30 March 2015   Published: 4 May 2015

Abstract

The decline in xylem flow during the late growth stage in most fruits may be due either to a decrease in the water potential gradient between the stem bearing the fruit and the fruit tissues or to a decrease in the hydraulic conductivity of xylem vessels, or both. In this study, we analysed changes in xylem flows to the mango Mangifera indica L. fruit during its development to identify the sources of variation by measuring changes in the water potential gradient and in the hydraulic properties of the fruit pedicel. The variations in xylem and transpiration flows were estimated at several stages of mango fruit development from the daily changes in the fresh mass of detached and girdled fruits on branches. The water potential gradient was estimated by monitoring the diurnal water potential in the stem and fruit. The hydraulic properties of the fruit pedicel were estimated using a flow meter. The results indicated that xylem flow increased in the early stages of fruit development and decreased in the late stage. Variations in xylem flow were related to the decrease in the hydraulic conductivity of xylem vessels but not to a decrease in the water potential gradient. The hydraulic conductivity of the fruit pedicel decreased during late growth due to embolism caused by a decrease in the fruit water potential. Further studies should establish the impact of the decrease in the hydraulic conductivity of the fruit pedicel on mango growth.

Additional keywords: cavitation, hydraulic resistance, Mangifera indica, transpiration, water potential.


References

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=738f76eb7c705511ed6dda42654d8fa3CAS | 16207748PubMed |

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=8ab5d1175d8a51e57a3360ca1bd52333CAS | 18440931PubMed |

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=34ce9609e1f37b1a91c39b4bed742477CAS | 19741048PubMed |

Clearwater MJ, Luo Z, Mazzeo M, Dichio B (2009) An external heat pulse method for measurement of sap flow through fruit pedicels, leaf petioles and other small-diameter stems. Plant, Cell & Environment 32, 1652–1663.
An external heat pulse method for measurement of sap flow through fruit pedicels, leaf petioles and other small-diameter stems.Crossref | GoogleScholarGoogle Scholar |

Clearwater MJ, Luo Z, Ong SEC, Blattmann P, Thorp TG (2012) Vascular functioning and the water balance of ripening kiwifruit (Actinidia chinensis) berries. Journal of Experimental Botany 63, 1835–1847.
Vascular functioning and the water balance of ripening kiwifruit (Actinidia chinensis) berries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjslehtrk%3D&md5=d00208a0c53cfa98d8a30732c0452aa3CAS | 22155631PubMed |

Cochard H, Badel E, Herbette S, Delzon S, Choat B, Jansen S (2013) Methods for measuring plant vulnerability to cavitation: a critical review. Journal of Experimental Botany 64, 4779–4791.
Methods for measuring plant vulnerability to cavitation: a critical review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslCrsbnE&md5=f8a19b6b02443458393daeacf9860f24CAS | 23888067PubMed |

Damour G (2008) ‘Bases théoriques et approches expérimentales de la modélisation des effets de la contrainte hydrique sur les échanges gazeux foliaires du manguier et du litchi,’ (Université de la Réunion: Saint Denis)

Dichio B, Remorini D, Lang S (2002) Developmental changes in xylem functionality in kiwifruit fruit: implications for fruit calcium accumulation. Acta Horticulturae 610, 191–195.

Dražeta L, Lang A, Hall AJ, Volz RK, Jameson PE (2004) Causes and effects of changes in xylem functionality in apple fruit. Annals of Botany 93, 275–282.
Causes and effects of changes in xylem functionality in apple fruit.Crossref | GoogleScholarGoogle Scholar | 14988096PubMed |

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 function 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 function in ripening berries.Crossref | GoogleScholarGoogle Scholar |

Fishman S, Génard M (1998) A biophysical model of fruit growth: simulation of seasonal and diurnal dynamics of mass. Plant, Cell & Environment 21, 739–752.
A biophysical model of fruit growth: simulation of seasonal and diurnal dynamics of mass.Crossref | GoogleScholarGoogle Scholar |

Fishman S, Génard M, Huguet J-G (2001) Theoretical analysis of systematic errors introduced by a pedicel-girdling technique used to estimate separately the xylem and phloem flows. Journal of Theoretical Biology 213, 435–446.
Theoretical analysis of systematic errors introduced by a pedicel-girdling technique used to estimate separately the xylem and phloem flows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3Mnpt1ejuw%3D%3D&md5=b6ae9add5b50a66f9b1611c4313d9e70CAS | 11735290PubMed |

Greenspan MD, Shackel KA, Matthews MA (1994) Developmental changes in the diurnal water budget of the grape berry exposed to water deficits. Plant, Cell & Environment 17, 811–820.
Developmental changes in the diurnal water budget of the grape berry exposed to water deficits.Crossref | GoogleScholarGoogle Scholar |

Guichard S, Gary C, Leonardi C, Bertin N (2005) Analysis of growth and water relations of tomato fruits in relation to air vapor pressure deficit and plant fruit load. Journal of Plant Growth Regulation 24, 201–213.
Analysis of growth and water relations of tomato fruits in relation to air vapor pressure deficit and plant fruit load.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1KnsbjE&md5=81a616fcd1af3a5d2b115a688f67c239CAS |

Higuchi H, Sakuratani T (2006) Water dynamics in mango (Mangifera indica L.) fruit during the young and mature fruit seasons as measured by the stem heat balance method. Journal of the Japanese Society for Horticultural Science 75, 11–19.

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

Hossain MM, Nonami H (2010) Effects of water flow from the xylem on the growth-induced water potential and the growth-effective turgor associated with enlarging tomato fruit. Environment Control in Biology 48, 101–116.
Effects of water flow from the xylem on the growth-induced water potential and the growth-effective turgor associated with enlarging tomato fruit.Crossref | GoogleScholarGoogle Scholar |

Huguet J, Génard M, Laurent R, Besset J, Bussi C, Girard T (1997) Xylemic, phloemic and transpiration flows to and from a peach. Acta Horticulturae 465, 345–353.

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=959e7f4e64986f41e4ee588e0482f530CAS | 16868045PubMed |

Lang A (1990) Xylem, phloem and transpiration flows in developing apple fruits. Journal of Experimental Botany 41, 645–651.
Xylem, phloem and transpiration flows in developing apple fruits.Crossref | GoogleScholarGoogle Scholar |

Lang A, Ryan KG (1994) Vascular development and sap flow in apple pedicels. Annals of Botany 74, 381–388.
Vascular development and sap flow in apple pedicels.Crossref | GoogleScholarGoogle Scholar |

Lang A, Thorpe M (1989) Xylem, phloem and transpiration flows in a grape: application of a technique for measuring the volume of attached fruits to high resolution using Archimedes’ principle. Journal of Experimental Botany 40, 1069–1078.
Xylem, phloem and transpiration flows in a grape: application of a technique for measuring the volume of attached fruits to high resolution using Archimedes’ principle.Crossref | GoogleScholarGoogle Scholar |

Léchaudel M, Joas J (2007) An overview of preharvest factors influencing mango fruit growth, quality and postharvest behaviour. Brazilian Journal of Plant Physiology 19, 287–298.
An overview of preharvest factors influencing mango fruit growth, quality and postharvest behaviour.Crossref | GoogleScholarGoogle Scholar |

Léchaudel M, Lopez-Lauri F, Vidal V, Sallanon H, Joas J (2013) Response of the physiological parameters of mango fruit (transpiration, water relations and antioxidant system) to its light and temperature environment. Journal of Plant Physiology 170, 567–576.
Response of the physiological parameters of mango fruit (transpiration, water relations and antioxidant system) to its light and temperature environment.Crossref | GoogleScholarGoogle Scholar | 23267462PubMed |

Li S-H, Huguet J-G, Bussi C (1989) Irrigation scheduling in a mature peach orchard using tensiometers and dendrometers. Irrigation and Drainage Systems 3, 1–12.
Irrigation scheduling in a mature peach orchard using tensiometers and dendrometers.Crossref | GoogleScholarGoogle Scholar |

Mazzeo M, Dichio B, Clearwater MJ, Montanaro G, Xiloyannis C (2013) Hydraulic resistance of developing Actinidia fruit. Annals of Botany 112, 197–205.
Hydraulic resistance of developing Actinidia fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVCqu7vN&md5=f4f82f7d97a6fc9a979b04703b7b1034CAS | 23658370PubMed |

Measham PF, Wilson SJ, Gracie AJ, Bound SA (2014) Tree water relations: flow and fruit. Agricultural Water Management 137, 59–67.
Tree water relations: flow and fruit.Crossref | GoogleScholarGoogle Scholar |

Meinzer FC, McCulloh KA (2013) Xylem recovery from drought-induced embolism: where is the hydraulic point of no return? Tree Physiology 33, 331–334.
Xylem recovery from drought-induced embolism: where is the hydraulic point of no return?Crossref | GoogleScholarGoogle Scholar | 23612243PubMed |

Mendoza D, Wills RBH (1984) ‘Mango: fruit development, postharvest physiology and marketing in ASEAN.’ (ASEAN Food Handling Bureau: Kuala Lumpur, Malaysia).

Mills TM, Behboudian MH, Clothier BE (1996) Water relations, growth, and the composition of ‘Braeburn’ apple fruit under deficit irrigation. Journal of the American Society for Horticultural Science 121, 286–291.

Montanaro G, Dichio B, Xiloyannis C (2010) Significance of fruit transpiration on calcium nutrition in developing apricot fruit. Journal of Plant Nutrition and Soil Science 173, 618–622.
Significance of fruit transpiration on calcium nutrition in developing apricot fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVaqtLbF&md5=b349eae0bbdb622d65f42c8471f026bbCAS |

Morandi B, Manfrini L, Losciale P, Zibordi M, Corelli Grappadelli L (2010) Changes in vascular and transpiration flows affect the seasonal and daily growth of kiwifruit (Actinidia deliciosa) berry. Annals of Botany 105, 913–923.
Changes in vascular and transpiration flows affect the seasonal and daily growth of kiwifruit (Actinidia deliciosa) berry.Crossref | GoogleScholarGoogle Scholar | 20382641PubMed |

Morandi B, Zibordi M, Losciale P, Manfrini L, Pierpaoli E, Grappadelli LC (2011) Shading decreases the growth rate of young apple fruit by reducing their phloem import. Scientia Horticulturae 127, 347–352.
Shading decreases the growth rate of young apple fruit by reducing their phloem import.Crossref | GoogleScholarGoogle Scholar |

Nordey T, Léchaudel M, Saudreau M, Joas J, Génard M (2014) Model-assisted analysis of spatial and temporal variations in fruit temperature and transpiration highlighting the role of fruit development. PLoS One 9, e92532
Model-assisted analysis of spatial and temporal variations in fruit temperature and transpiration highlighting the role of fruit development.Crossref | GoogleScholarGoogle Scholar | 24663687PubMed |

Sangsing K, Kasemsap P, Thanisawanyangkura S, Sangkhasila K, Gohet E, Thaler P, Cochard H (2004) Xylem embolism and stomatal regulation in two rubber clones (Hevea brasiliensis Muell. Arg.). Trees 18, 109–114.
Xylem embolism and stomatal regulation in two rubber clones (Hevea brasiliensis Muell. Arg.).Crossref | GoogleScholarGoogle Scholar |

Singh Z, Malik AU, Davenport TL (2010) Fruit drop in mango. In ‘Horticultural Reviews, Volume 31’. (Ed. J Janick) pp. 111–153. (John Wiley & Sons: Oxford).

Sperry JS, Ikeda T (1997) Xylem cavitation in roots and stems of Douglas-fir and white fir. Tree Physiology 17, 275–280.
Xylem cavitation in roots and stems of Douglas-fir and white fir.Crossref | GoogleScholarGoogle Scholar | 14759867PubMed |

Trifilò P, Raimondo F, Lo Gullo MA, Nardini A, Salleo S (2010) Hydraulic connections of leaves and fruit to the parent plant in Capsicum frutescens (hot pepper) during fruit ripening. Annals of Botany 106, 333–341.
Hydraulic connections of leaves and fruit to the parent plant in Capsicum frutescens (hot pepper) during fruit ripening.Crossref | GoogleScholarGoogle Scholar | 20525746PubMed |

Turner N (1981) Techniques and experimental approaches for the measurement of plant water status. Plant and Soil 58, 339–366.
Techniques and experimental approaches for the measurement of plant water status.Crossref | GoogleScholarGoogle Scholar |

Tyerman SD, Tilbrook J, Pardo C, Kotula L, Sullivan W, Steudle E (2004) Direct measurement of hydraulic properties in developing berries of Vitis vinifera L. cv Shiraz and Chardonnay. Australian Journal of Grape and Wine Research 10, 170–181.
Direct measurement of hydraulic properties in developing berries of Vitis vinifera L. cv Shiraz and Chardonnay.Crossref | GoogleScholarGoogle Scholar |

Tyree MT, Sperry JS (1988) Do woody plants operate near the point of catastrophic xylem dysfunction caused by dynamic water stress? Answers from a model. Plant Physiology 88, 574–580.
Do woody plants operate near the point of catastrophic xylem dysfunction caused by dynamic water stress? Answers from a model.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnhvVGjtA%3D%3D&md5=12956f2259517acc37226971909b562dCAS | 16666351PubMed |

Van Ieperen W, Volkov VS, Van Meeteren U (2003) Distribution of xylem hydraulic resistance in fruiting truss of tomato influenced by water stress. Journal of Experimental Botany 54, 317–324.
Distribution of xylem hydraulic resistance in fruiting truss of tomato influenced by water stress.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s%2FksFOqsA%3D%3D&md5=dd30ffd1fc295faa4e128864e1c52a15CAS | 12493859PubMed |