Variation in carbon content and size in developing fruit of Actinidia deliciosa genotypes
Simona Nardozza A H , Helen L. Boldingh B , Annette C. Richardson C , Guglielmo Costa D , Hinga Marsh E , Elspeth A. MacRae A F and Michael J. Clearwater E GA The New Zealand Institute for Plant & Food Research Limited, Mt Albert Research Centre, Private Bag 92 169, Auckland, New Zealand.
B The New Zealand Institute for Plant & Food Research Limited, Ruakura Research Centre, Private Bag 3123, Hamilton, New Zealand.
C The New Zealand Institute for Plant & Food Research Limited, Kerikeri Research Centre, Private Bag 23, Kerikeri, New Zealand.
D Dipartimento di Colture Arboree, Università di Bologna, Via Fanin 46, 40127 Bologna, Italy.
E The New Zealand Institute for Plant & Food Research Limited, Te Puke Research Centre, 412 No 1 Road, RD2, Te Puke, 3182, New Zealand.
F Present address: Scion, Te Papa Tipu Innovation Park, Private Bag 3020, Rotorua, New Zealand.
G Present address: University of Waikato, Department of Biological Science, Private Bag 3105, Hamilton, New Zealand.
H Corresponding author. Email: simona.nardozza@plantandfood.co.nz
Functional Plant Biology 37(6) 545-554 https://doi.org/10.1071/FP09301
Submitted: 17 December 2009 Accepted: 3 March 2010 Published: 20 May 2010
Abstract
This study identifies the developmental processes contributing to variation in green-fleshed kiwifruit (Actinidia deliciosa (A. Chev.) C.F. Liang et A.R. Ferguson var. deliciosa) fruit dry matter content (DM) and fresh weight (FW) by comparing genotypes with either high or low final DM. Results are compared with the model for fruit development, the tomato (Solanum lycopersicum L.). Differences in final composition were attributable to a higher rate of starch accumulation from 70 days after anthesis in high DM genotypes, with no other consistent differences in accumulation of soluble sugars or organic acids. High DM genotypes had 70% higher starch content and differed from low DM genotypes in the allocation of carbon between storage and other components. DM was negatively correlated with final fruit FW only in high DM genotypes, whereas starch was a constant proportion of dry weight (DW), suggesting a dilution effect rather than an interaction between fruit size and carbohydrate metabolism. Compared with tomato, the organic acids, particularly quinic acid, contributed more to estimated osmotic pressure during growth in FW than the soluble sugars, regardless of final composition or size. Seed mass per unit FW was highest in high DM genotypes, suggesting a previously unrecognised role for kiwifruit seeds in accumulation of carbohydrate by the pericarp. Anatomical comparisons also identified a role for differences in the packing of the two principal cell types, with an increased frequency of the larger cell type correlated with reduced DM. These genotypes demonstrate that kiwifruit differs from tomato in the role of starch as the principal stored carbohydrate, the reduced importance of dilution by growth in FW and the more minor role of the sugars compared with the organic acids during fruit development.
Additional keywords: citric acid, fructose, glucose, malic acid, myo-inositol, non-structural carbohydrate, quality, sucrose.
Acknowledgements
This work was funded by the Plant & Food Research Kiwifruit Royalty Investment Programme, the New Zealand Foundation for Research, Science and Technology (Contract No. C06X0706 and C06X0202), and the University of Bologna. SN is currently supported by a post-doctoral fellowship from the Agricultural and Marketing Research and Development Trust (Contract No. 22817). The authors thank Ian Hallett and Paul Sutherland for microscopy advice, Sam Ong Eng Chye and Rosannah McCartney for their technical assistance, Nihal De Silva and Mark Wohlers for statistical advice and Ross Atkinson and Peter Minchin for their critical review of the manuscript.
Baxter CJ,
Carrari F,
Bauke A,
Overy S,
Hill SA,
Quick PW,
Fernie AR, Sweetlove LJ
(2005) Fruit carbohydrate metabolism in an introgression line of tomato with increased fruit soluble solids. Plant & Cell Physiology 46, 425–437.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bertin N,
Gautier H, Rocher C
(2002) Number of cells in tomato fruit depending on fruit position and source–sink balance during plant development. Plant Growth Regulation 36, 105–112.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Bertin N,
Causse M,
Brunel B,
Tricon D, Genard M
(2009) Identification of growth processes involved in QTLs for tomato fruit size and composition. Journal of Experimental Botany 60, 237–248.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bohner J, Bangerth F
(1988) Cell number, cell size, and hormone levels in semi-isogenic mutants of Lycopersicon pimpinellifolium differing in fruit size. Physiologia Plantarum 72, 316–320.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Boldingh H,
Smith GS, Klages K
(2000) Seasonal concentrations of non-structural carbohydrates of five Actinidia species in fruit, leaf and fine root tissue. Annals of Botany 85, 469–476.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Burdon J,
McLeod D,
Lallu N,
Gamble J,
Petley M, Gunson A
(2004) Consumer evaluation of ‘Hayward’ kiwifruit of different at-harvest dry matter contents. Postharvest Biology and Technology 34, 245–255.
| Crossref | GoogleScholarGoogle Scholar |
Buxton KN, Currie MB
(2006) Pollination: its impact on fruit yield and quality. New Zealand Kiwifruit Journal 177, 26–32.
Cheng CH,
Seal AG,
Boldingh HL,
Marsh KB,
MacRae EA,
Murphy SJ, Ferguson AR
(2004) Inheritance of taste characters and fruit size and number in a diploid Actinidia chinensis (kiwifruit) population. Euphytica 138, 185–195.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Clearwater MJ,
Mezzana S,
Richardson AC,
Boldingh HL,
Marsh H,
Clarke J,
Lavrijsen A, MacRae EA
(2007) Physiological processes contributing to genotypic variation in fruit composition of Actinidia deliciosa. Acta Horticulturae 753, 375–381.
Crowhurst RN,
Gleave AP,
MacRae EA,
Ampomah-Dwamena C, Atkinson RG ,
et al
.
(2008) Analysis of expressed sequence tags from Actinidia: applications of a cross species EST database for gene discovery in the areas of flavor, health, color and ripening. BMC Genomics 9, 351.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cruz-Castillo JG,
Woolley DJ, Lawes GS
(2002) Kiwifruit size and CPPU response are influenced by the time of anthesis. Scientia Horticulturae 95, 23–30.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Davis RMJ,
Smith PG,
Schweers VH, Scheuerman RW
(1964) Independence of floral fertility and fruit-set in the tomato. Proceedings of the American Society for Horticultural Science 86, 552–556.
Eshed Y, Zamir D
(1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTLs. Genetics 141, 1147–1162.
|
CAS |
PubMed |
Ferguson AR
(2007) The need for characterisation and evaluation of germplasm: kiwifruit as an example. Euphytica 154, 371–382.
| Crossref | GoogleScholarGoogle Scholar |
Fernandez L,
Romieu C,
Moing A,
Bouquet A,
Maucourt M,
Thomas MR, Torregrosa L
(2006) The grapevine fleshless berry mutation. A unique genotype to investigate differences between fleshy and nonfleshy fruit. Plant Physiology 140, 537–547.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Fernie AR,
Tadmor Y, Zamir D
(2006) Natural genetic variation for improving crop quality. Current Opinion in Plant Biology 9, 196–202.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fraser LG,
Tsang GK,
Datson PM,
De Silva HN,
Harvey CF,
Gill GP,
Crowhurst RN, McNeilage MA
(2009) A gene-rich linkage map in the dioecious species Actinidia chinensis (kiwifruit) reveals putative X/Y sex-determining chromosomes. BMC Genomics 10, 102.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fridman E,
Carrari F,
Liu YS,
Fernie AR, Zamir D
(2004) Zooming in on a quantitative trait for tomato yield using interspecific introgressions. Science 305, 1786–1789.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Goffinet MC,
Robinson TL, Lakso AN
(1995) A comparison of ‘Empire’ apple fruit size and anatomy in unthinned and hand-thinned trees. Journal of Horticultural Science 70, 375–387.
Hallett IC,
MacRae EA, Wegrzyn TF
(1992) Changes in kiwifruit cell-wall ultrastructure and cell packing during postharvest ripening. International Journal of Plant Sciences 153, 49–60.
| Crossref | GoogleScholarGoogle Scholar |
Harker FR, Hallett IC
(1994) Physiological and mechanical properties of kiwifruit tissue associated with texture change during cool storage. Journal of the American Society for Horticultural Science 119, 987–993.
Higashi K,
Hosoya K, Ezura H
(1999) Histological analysis of fruit development between two melon (Cucumis melo L. reticulatus) genotypes setting a different size of fruit. Journal of Experimental Botany 50, 1593–1597.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Hopping ME
(1976a) Effect of exogenous auxins, gibberellins, and cytokinins on fruit development in Chinese gooseberry (Actinidia chinensis Planch.). New Zealand Journal of Botany 14, 69–75.
|
CAS |
Hopping ME
(1976b) Structure and development of fruit and seeds in Chinese gooseberry (Actinidia chinensis Planch.). New Zealand Journal of Botany 14, 63–68.
Ibarbia EA, Lamberth VN
(1971) Tomato fruit size and quality interrelationships. Journal of the American Society for Horticultural Science 96, 199–201.
Jensen RA
(1986) The shikimate/arogenate pathway: link between carbohydrate-metabolism and secondary metabolism. Physiologia Plantarum 66, 164–168.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Jordan RB,
Walton EF,
Klages KU, Seelye RJ
(2000) Postharvest fruit density as an indicator of dry matter and ripened soluble solids of kiwifruit. Postharvest Biology and Technology 20, 163–173.
| Crossref | GoogleScholarGoogle Scholar |
Jullien A,
Munier-Jolain NG,
Malézieux E,
Chillet M, Ney B
(2001) Effect of pulp cell number and assimilate availability on dry matter accumulation rate in a banana fruit [Musa sp. AAA group ‘Grande Naine’ (Cavendish subgroup)]. Annals of Botany 88, 321–330.
| Crossref | GoogleScholarGoogle Scholar |
Klages K,
Donnison H,
Boldingh H, MacRae E
(1998)
myo-Inositol is the major sugar in Actinidia arguta during early fruit development. Australian Journal of Plant Physiology 25, 61–67.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Lippman ZB,
Semel Y, Zamir D
(2007) An integrated view of quantitative trait variation using tomato interspecific introgression lines. Current Opinion in Genetics & Development 17, 545–552.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
MacRae E,
Quick WP,
Benker C, Stitt M
(1992) Carbohydrate metabolism during postharvest ripening in kiwifruit. Planta 188, 314–323.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Marsh KB,
Boldingh HL,
Shilton RS, Laing WA
(2009) Changes in quinic acid metabolism during fruit development in three kiwifruit species. Functional Plant Biology 36, 463–470.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
McKibbin RS,
Muttucumaru N,
Paul MJ,
Powers SJ,
Burrell MM,
Coates S,
Purcell PC,
Tiessen A,
Geigenberger P, Halford NG
(2006) Production of high-starch, low-glucose potatoes through over-expression of the metabolic regulator SnRK1. Plant Biotechnology Journal 4, 409–418.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
McPherson HG,
Richardson AC,
Snelgar WP,
Patterson KJ, Currie MB
(2001) Flower quality and fruit size in kiwifruit (Actinidia deliciosa). New Zealand Journal of Crop and Horticultural Science 29, 93–101.
Patterson KJ,
Mason KA, Gould KS
(1993) Effects of CPPU (N-(2-chloro-4-pyridyl)-N’-phenylurea) on fruit-growth, maturity, and storage quality of kiwifruit. New Zealand Journal of Crop and Horticultural Science 21, 253–261.
|
CAS |
Prudent M,
Causse M,
Genard M,
Tripodi P,
Grandillo S, Bertin N
(2009) Genetic and physiological analysis of tomato fruit weight and composition: influence of carbon availability on QTL detection. Journal of Experimental Botany 60, 923–937.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Richardson AC,
McAneney KJ, Dawson TE
(1997) Carbohydrate dynamics in kiwifruit. Journal of Horticultural Science 72, 907–917.
Richardson AC,
Marsh KB,
Boldingh HL,
Pickering AH,
Bulley SM,
Frearson NJ,
Ferguson AR,
Thornber SE,
Bolitho KM, MacRae EA
(2004) High growing temperatures reduce fruit carbohydrate and vitamin C in kiwifruit. Plant, Cell & Environment 27, 423–435.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Smith GS,
Clark CJ, Boldingh HL
(1992) Seasonal accumulation of starch by components of the kiwifruit vine. Annals of Botany 70, 19–25.
|
CAS |
Stevens MA
(1986) Inheritance of tomato fruit quality components. Plant Breeding Reviews 4, 273–311.
Testolin R,
Huang WG,
Lain O,
Messina R,
Vecchione A, Cipriani G
(2001) A kiwifruit (Actinidia spp.) linkage map based on microsatellites and integrated with AFLP markers. Theoretical and Applied Genetics 103, 30–36.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Walton EF, De Jong TM
(1990) Growth and compositional changes in kiwifruit berries from three californian locations. Annals of Botany 66, 285–298.
|
CAS |
Woodward TJ, Clearwater MJ
(2008) Relationships between ‘Hayward’ kiwifruit weight and dry matter content. Postharvest Biology and Technology 48, 378–382.
| Crossref | GoogleScholarGoogle Scholar |
Wu B-H,
Génard M,
Lescourret F,
Gomez L, Li S-H
(2002) Influence of assimilate and water supply on seasonal variation of acids in peach (cv. Suncrest). Journal of the Science of Food and Agriculture 82, 1829–1836.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
