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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Changes in quinic acid metabolism during fruit development in three kiwifruit species

Ken B. Marsh A C , Helen L. Boldingh B , Rebecca S. Shilton A and William A. Laing A
+ Author Affiliations
- Author Affiliations

A Plant and Food Research, Private Bag 92169, Auckland, New Zealand.

B Plant and Food Research, Private Bag 3123, Hamilton, New Zealand.

C Corresponding author. Email: kmarsh@hortresearch.co.nz

Functional Plant Biology 36(5) 463-470 https://doi.org/10.1071/FP08240
Submitted: 12 September 2008  Accepted: 20 February 2009   Published: 6 May 2009

Abstract

Kiwifruit are novel in that they contain high levels of quinic acid (1–2% w/w), which contributes to the flavour, sugar/acid balance and health-giving properties of the fruit. In a study of quinic acid storage and metabolism in three kiwifruit species (Actinidia chinensis Planch. var. chinensis, Actinidia deliciosa (A. Chev.) C.F. Liang et A.R. Ferguson var. deliciosa and Actinidia arguta (Sieb. et Zucc.) Planch. ex Miq. var. arguta) quinic acid accumulation occurred principally in the early stages (<60 days after anthesis; (DAA)) of fruit development. The present study established that there are separate quinate dehydrogenase (QDH) and shikimate dehydrogenase (SDH) activities in kiwifruit, probably representing different proteins. Quinate dehydrogenase activity was at a maximum around the time of greatest quinic acid accumulation and declined markedly in late fruit development, and was also higher in the species that accumulated the largest amounts of quinic acid (A. chinensis and A. deliciosa). In contrast, SDH activity was highest in the early stages of fruit development and only declined to 30–50% at later stages of fruit development in all three species. Dehydroquinate synthase gene expression levels measured by quantitative real-time PCR showed a high level in the early season, which was sustained through the mid-season. The quantitative real-time PCR results for a kiwifruit EST that had homology to chloroplastic isoforms of SDH showed an induction in the middle to late season; therefore, the high level of SDH activity in the early season (<30 DAA) may have resulted from the expression of a cytosolic isoform of the enzyme. The results are also consistent with the relative levels of the bifunctional dehydroquinate dehydratase/SDH enzyme and QDH enzyme controlling the accumulation and utilisation of quinic acid in kiwifruit.

Additional keywords: acid accumulation, quinate dehydrogenase, shikimate dehydrogenase.


Acknowledgements

This work was supported by the Foundation for Research, Science and Technology (C06X0403) and the Horticultural and Food Research Institute of New Zealand Limited.


References


Bischoff M, Schaller A, Bieri F, Kessler F, Amrhein N, Schmid J (2001) Molecular characterization of tomato 3-dehydroquinate dehydratase-shikimate: NADP oxidoreductase. Plant Physiology 125, 1891–1900.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Bonner CA, Jensen RA (1994) Cloning of cDNA encoding the bifunctional dehydroquinase shikimate dehydrogenase of aromatic-amino-acid biosynthesis in Nicotiana tabacum. The Biochemical Journal 302, 11–14.
CAS | PubMed |
open url image1

Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principal of protein–dye binding. Analytical Biochemistry 72, 248–254.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Cheng C, Seal A, Boldingh H, Marsh K, MacRae EA, Murphy S, Ferguson AR (2004) Inheritance of fruit characters and fruit size in a diploid Actinidia chinensis (kiwifruit) population. Euphytica 138, 185–195.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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 | open url image1

Ding L, Hofius D, Hajirezaei M-R, Fernie AR, Bornke F, Sonnewald U (2007) Functional analysis of the essential bifunctional tobacco enzyme 3-dehydroquinate dehydratase/shikimate dehydrogenase in transgenic tobacco plants. Journal of Experimental Botany 58, 2053–2067.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Gamborg OL (1966) Aromatic metabolism in plants III. Quinate dehydrogenase from mung bean cell suspension cultures. Biochimica et Biophysica Acta 128, 483–491. open url image1

Kang X, Scheibe R (1993) Purification and characterization of the quinate oxidoreductase from Phaseolus mungo sprouts. Phytochemistry 33, 769–773.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Kang XB, Neuhaus HE, Scheibe R (1994) Subcellular-localization of quinate – oxidoreductase from Phaseolus-mungo l sprouts. Zeitschrift für Naturforschung 49, 415–420.
CAS |
open url image1

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, 61–68.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Laing WA, Frearson N, Bulley S, MacCrae E (2004) Kiwifruit l-Galactose dehydrogenase: molecular, biochemical and physiological aspects of the enzyme. Functional Plant Biology 31, 1015–1025.
Crossref | l
-Galactose dehydrogenase: molecular, biochemical and physiological aspects of the enzyme.&journal=Functional Plant Biology&volume=31&pages=1015-1025&publication_year=2004&author=E%20MacCrae&hl=en&doi=10.1071/FP04090" target="_blank" rel="nofollow noopener noreferrer" class="reftools">GoogleScholarGoogle Scholar | CAS | open url image1

Lindner HA, Nadeau G, Matte A, Michel G, Menard R, Cygler M (2005) Site-directed mutagenesis of the active site region in the quinate/shikimate 5-dehydrogenase YdiB of Escherichia coli. The Journal of Biological Chemistry 280, 7162–7169.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Lopez-Gomez R, Gomez-Lim MA (1992) A method for extracting intact RNA from fruits rich in polysaccharides using ripe mango mesocarp. HortScience 27, 440–442.
CAS |
open url image1

Michel G, Roszak AW, Sauve V, Maclean J, Matte A, Coggins JR, Cygler M, Lapthorn AJ (2003) Structures of shikimate dehydrogenase AroE and its paralog YdiB: a common structural framework for different activities. The Journal of Biological Chemistry 278, 19463–19472.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Nishiyama I, Fukuda T, Shimohashi A, Oota T (2008) Sugar and acid composition in the fruit juice of different Actinidia varieties. Food Science and Technology Research 14, 67–73.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Okuse I, Ryugo K (1981) Compositional changes in the developing ‘Hayward’ kiwifruit in California. Journal of the American Society for Horticultural Science 106, 73–76.
CAS |
open url image1

Ossipov V, Bonner C, Ossipova S, Jensen R (2000) Broad-specificity quinate (shikimate) dehydrogenase from Pinus taeda needles. Plant Physiology and Biochemistry 38, 923–928.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Refeno G, Ranjeva R, Boudet A (1982) Modulation of quinate: NAD+ oxidoreductase activity through reversible phosphorylation in carrot cell suspensions. Planta 154, 193–198.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Singh SA, Christendat D (2006) Structure of Arabidopsis dehydroquinate dehydratase–shikimate dehydrogenase and implications for metabolic channeling in the shikimate pathway. Biochemistry 45, 7787–7796.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Walton EF, De Jong TM (1990) Growth and compositional changes in kiwifruit berries from three Californian locations. Annals of Botany 66, 285–298.
CAS |
open url image1