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Plant function and evolutionary biology
RESEARCH ARTICLE

Gradients in stomatal conductance, xylem sap ABA and bulk leaf ABA along canes of Vitis vinifera cv. Shiraz: molecular and physiological studies investigating their source

Christopher J. Soar A B C , Jim Speirs A B , Suzanne M. Maffei B and Brian R. Loveys A B
+ Author Affiliations
- Author Affiliations

A Cooperative Research Centre for Viticulture, PO Box 154, Glen Osmond, SA 5064, Australia.

B CSIRO Division of Plant Industry, PO Box 350, Glen Osmond, SA 5064, Australia.

C Corresponding author; email: chris.soar@csiro.au

Functional Plant Biology 31(6) 659-669 https://doi.org/10.1071/FP03238
Submitted: 3 December 2003  Accepted: 2 March 2004   Published: 23 June 2004

Abstract

Gradients were observed in xylem sap ABA and in stomatal conductance along canes of Vitis vinifera L. cv. Shiraz. To investigate the source of the ABA responsible for these gradients a series of girdling and decapitation experiments were carried out. Leaf stomatal conductance and bulk ABA of leaves and apices were measured in control plants and in response to apex removal or girdling. Gradients in leaf ABA were observed over the first eight expanded leaves of field-grown Shiraz, with higher concentrations of ABA observed towards the apex. Gradients in stomatal conductance that correlated negatively with the concentration of ABA in the leaf ([ABA]leaf) were also observed over the first eight leaves. No significant effect of decapitation was observed on either leaf ABA or stomatal conductance except for the leaf immediately below the apex where a transient increase in [ABA]leaf was observed after 24 h with no corresponding decrease in conductance. Girdling resulted in an increase in [ABA]leaf in leaves distal to the girdle without the corresponding effect on conductance. These effects were further studied at the level of gene activity. To facilitate this, gene sequences encoding two key enzymes involved in the biosynthetic pathway of ABA in grape, zeaxanthin epoxidase (Zep) and 9-cis-epoxycarotenoid dioxygenase (NCED), were isolated and characterised. The cDNA sequences were used as probes to measure the abundances of their respective mRNAs in the leaf and apical material. Levels of expression of one of the two genes encoding NCED, VvNCED1, reflected the gradients in [ABA]leaf in control vines, however treatment-induced changes in ABA were not always associated with corresponding changes in VvNCED1 expression. The abundances of both the VvNCED2 mRNA and Zep mRNA increased with increasing leaf age and did not appear to be associated with either the [ABA]leaf or the expression of VvNCED1.

Our results indicate that observed gradients in g s are correlated with [ABA] gradients in mature leaves and xylem sap and that these [ABA] gradients are not derived directly from the apical tissues but, at least partially, from local synthesis.

Keywords: abscisic acid, gradients, grapevine, NCED, stomatal conductance, Zep.


Acknowledgments

This research was supported by the Commonwealth Cooperative Research Centre Program and conducted through the CRC for Viticulture with support from Australia's grape growers and winemakers through their investment body the Grape and Wine Research and Development Corporation, with matching funds from the Federal Government.


References


Abida PS, Sashidhar VR, Manju RV, Prasad TG, Sudharshana L (1994) Root–shoot communication in drying soil is mediated by the stress hormones abscisic acid and cytokinin synthesised in the roots. Current Science 66, 668–672. open url image1

Audran C, Borel C, Frey A, Sotta B, Meyer C, Simonneau T, Marion-Poll A (1998) Expression studies of the zeaxanthin epoxidase gene in Nicotiana plumbaginifolia.  Plant Physiology 118, 1021–1028.
Crossref | PubMed |
open url image1

Blackman PG, Davies WJ (1985) Root to shoot communication in maize plants of the effects of soil drying. Journal of Experimental Botany 36, 39–48. open url image1

Burbidge A, Grieve TM, Jackson A, Thompson A, McCarty DR, Taylor IB (1999) Characterisation of the ABA-deficient tomato mutant notablis and its relationship with maize Vp 14.  The Plant Journal 17, 427–431.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought — from genes to the whole plant. Functional Plant Biology 30, 239–264.
Crossref | GoogleScholarGoogle Scholar | open url image1

Chernys JT, Zeevaart JAD (2000) Characterisation of the 9-cis-epoxycarotenoid dioxygenase gene family and the regulation of abscisic acid biosynthesis in avocado. Plant Physiology 124, 343–353.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Comstock JP (2002) Hydraulic and chemical signalling in the control of stomatal conductance and transpiration. Journal of Experimental Botany 53, 195–200.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cowan AK, Cairns ALP, Bartels-rahm B (1999) Regulation of abscisic acid metabolism: towards a metabolic basis for abscisic acid–cytokinin antagonism. Journal of Experimental Botany 50, 595–603.
Crossref | GoogleScholarGoogle Scholar | open url image1

Daie J, Wyse R, Hein M, Brenner ML (1984) Abscisic acid metabolism by source and sink tissues of sugar beet. Plant Physiology 74, 810–814. open url image1

Demmig-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress Annual Review of Plant Physiology and Plant Molecular Biology 43, 599–626.
Crossref |
open url image1

Duckham SC, Linforth RST, Taylor IB (1991) Abscisic acid-deficient mutants at the aba gene locus of Arabidopsis thaliana are impaired in the epoxidation of zeaxanthin. Plant, Cell and Environment 14, 601–606. open url image1

Düring H (1987) Stomatal responses to alterations of soil and air humidity in grapevine. Vitis 26, 9–18. open url image1

Düring H, Broquedis M (1980) Effects of abscisic acid and benzyladenine on irrigated and non-irrigated grapevines. Scientia Horticulturae 13, 253–260.
Crossref | GoogleScholarGoogle Scholar | open url image1

Düring H, Scienza A (1975) The role of endogenous abscisic acid during water stress in grapevines. Vitis 14, 20–26. open url image1

Düring H, Loveys BR, Dry PR (1997) Root signals affect water use efficiency and shoot growth. Acta Horticulturae 427, 1–14. open url image1

Felsenstein J (1989) PHYLIP — phylogeny inference package. Version 3.2. Cladistics 5, 164–166. open url image1

Fourney RM, Miyakoshi J, Day RS, Paterson MC (1998) Northern blotting: efficient RNA staining and transfer. Focus 10, 5–9. open url image1

Frohman MA, Dush MK, Martin GR (1988) Rapid production of full-length cDNAs from rare transcripts: Amplification using a single gene-specific oligonucleotide primer. Proceedings of the National Academy of Sciences USA 85, 8998–9002. open url image1

Giraudat J (1995) Abscisic acid signalling. Current Opinion in Cell Biology 7, 232–238.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Guinn G, Brummett DL (1993) Leaf age, decline in photosynthesis, and changes in abscisic acid, indole-3-acetic acid, and cytokinin in cotton leaves. Field Crops Research 32, 269–275.
Crossref | GoogleScholarGoogle Scholar | open url image1

Grossmann K, Hansen H (2001) Ethylene-triggered abscisic acid: a principle in plant growth regulation? Physiologia Plantarum 113, 9–14.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hansen H, Grossmann K (2000) Auxin-induced ethylene triggers abscisic acid biosynthesis and growth inhibition. Plant Physiology 124, 1437–1448.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hartung W, Heilmeier H (1993) Stomatal responses to abscisic acid in natural environments. ‘Interacting stresses on plants in a changing environment’. (Eds MB Jackson, CR Black) pp. 525–542. (Springer-Verlag: Berlin, Germany)

Hiron RWP, Wright STC (1973) The role of endogenous abscisic acid in the response of plants to stress. Journal of Experimental Botany 24, 769–781. open url image1

Jackson MB (1997) Hormones from roots as signals for the shoots of stressed plants. Trends in Plant Science 2, 22–28.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jia W, Zhang J, Jia WS, Zhang JH (1997) Comparison of exportation and metabolism of xylem-delivered ABA in maize leaves at different water status and xylem sap pH. Plant Growth Regulation 21, 43–49.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jia WS, Zhang JH (1999) Stomatal closure is induced rather by prevailing xylem abscisic acid than by accumulated amount of xylem-derived abscisic acid. Physiologia Plantarum 106, 268–275.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jokhan AD, Harink RJ, Jackson MB (1999) Concentration and delivery of abscisic acid in xylem sap are greater at the shoot base than at a target leaf nearer to the shoot apex. Plant Biology 1, 253–260. open url image1

Koorneef M, Jorna ML, Brinkhorst-van der Swan DCL, Karssen CM (1982) The isolation of abscisic acid (ABA) deficient mutants by selection of induced revertant in non-germinating gibberellin sensitive lines of Arabidopsis thaliana (L.) Heynh. Theoretical and Applied Genetics 61, 385–393. open url image1

Kriedemann PE (1968) Photosynthesis in vine leaves as a function of light intensity, temperature and leaf age. Vitis 7, 213–220. open url image1

Leckie CP, McAinsh MR, Montgomery L, Priestley AJ, Staxen I, Webb AAR, Hetherington AM (1998) Second messengers in guard cells. Journal of Experimental Botany 49, 339–349.
Crossref | GoogleScholarGoogle Scholar | open url image1

Liotenberg S, North H, Marion-Poll A (1999) Molecular biology and regulation of abscisic acid biosynthesis in plants. Plant Physiology and Biochemistry 37, 341–350.
Crossref | GoogleScholarGoogle Scholar | open url image1

Loveys BR, Kriedemann PE (1973) Rapid changes in abscisic acid-like inhibitors following alterations in vine leaf water potential. Physiologia Plantarum 28, 476–479. open url image1

Loveys BR, Kriedemann PE (1974) Internal control of stomatal physiology and photosynthesis. I. Stomatal regulation and associated changes in endogenous levels of abscisic and phaseic acids. Australian Journal of Plant Physiology 1, 407–415. open url image1

Loveys BR, van Dijk HM (1988) Improved extraction of abscisic acid from plant tissue. Australian Journal of Plant Physiology 15, 421–427. open url image1

Loveys BR, Dry PR, Stoll M, McCarthy MG (2000) Using plant physiology to improve the water use efficiency of horticultural crops. Acta Horticulturae 537, 187–197. open url image1

Marin E, Nussaume L, Quesada A, Gonneau M, Sotta B, Hugueney P, Frey A, Marion-Poll A (1996) Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana.  EMBO Journal 15, 2331–2342.
PubMed |
open url image1

Passioura JB, Tanner CB (1985) Oscillations in apparent hydraulic conductance of cotton plants. Australian Journal of Plant Physiology 12, 455–461. open url image1

Qin X, Zeevaart JAD (1999) The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proceedings of the National Academy of Sciences USA 96, 15354–15361.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rock CD, Zeevaart JAD (1991) The aba mutant of Arabidopsis thaliana is impaired in epoxy-carotenoid biosynthesis. Proceedings of the National Academy of Sciences USA 88, 7496–7499. open url image1

Schurr U, Gollan T, Schulze ED (1992) Stomatal response to drying soil in relation to changes in the xylem sap composition of Helianthus annuus. II. Stomatal sensitivity to abscisic acid imported from the xylem sap. Plant, Cell and and Environment 15, 561–567. open url image1

Schwartz SH, Tan BC, Gage DA, Zeevaart JAD, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276, 1872–1874.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Seo M, Peeters AJM, Koiwai H, Oritani T, Marion-Pol A, Zeevaart JAD, Koornneef M, Kamiya Y, Koshiba T (2000) The Arabidopsis aldehyde oxidase 3 (AAO3) gene product catalyses the final step in abscisic acid biosynthesis in leaves. Proceedings of the National Academy of Sciences USA 97, 12908–12913.
Crossref | GoogleScholarGoogle Scholar | open url image1

Speirs J, Longhurst T (1993) RNA extraction and fractionation. ‘Methods in plant biochemistry. Vol. 10’. (Ed. J Bryant) pp. 1–32. (Academic Press: San Diego, CA)

Tan BC, Joseph LM, Deng WT, Liu L, Li QB, Cline K, McCarty DR (2003) Molecular characterisation of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. The Plant Journal 35, 44–56.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tan BC, Schwartz SH, Zeevaart JAD, McCarty DR (1997) Genetic control of abscisic acid biosynthesis in maize. Proceedings of the National Academy of Sciences USA 94, 12235–12240.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tardieu F (1995) Control of stomatal conductance in droughted plants by hydraulic and chemical messages from roots. ‘Photosynthesis: from light to biosphere. Volume V. Proceedings of the 10th international photosynthesis congress, Montpellier, France’. (Ed. P Mathis ) pp. 531–536. (Kluwer Academic Publishers: Dordrecht, The Netherlands)


Tardieu F, Davies WJ (1992) Stomatal response to abscisic acid is a function of current plant water status. Plant Physiology 98, 540–545. open url image1

Tardieu F, Davies WJ (1993) Integration of hydraulic and chemical signalling in the control of stomatal conductance and water status of droughted plants. Plant, Cell and Environment 16, 341–349. open url image1

Tardieu F, Zhang J, Gowing DJG (1993) Stomatal control by both [ABA] in the xylem sap and leaf water status: a test of a model for droughted or ABA-fed field-grown maize. Plant, Cell and Environment 16, 413–420. open url image1

Tardieu F, Lafarge T, Simonneau T (1996) Stomatal control by fed or endogenous xylem ABA in sunflower: interpretation of correlations between leaf water potential and stomatal conductance in anisohydric species. Plant, Cell and Environment 19, 75–84. open url image1

Taylor JS, Pharis RP, Loveys B, Notodimedjo S, Edwards GR (1984) Changes in endogenous hormones in apple during bud burst induced by defoliation. Plant Growth Regulation 2, 117–134. open url image1

Taylor IB, Burbidge A, Thompson AJ (2000) Control of abscisic acid synthesis. Journal of Experimental Botany 51, 1563–1574.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
PubMed |
open url image1

Thompson AJ, Jackson AC, Parker RA, Morpeth DR, Burbidge A, Taylor IB (2000) Abscisic acid biosynthesis in tomato: regulation of zeaxanthin epoxidase and 9-cis-epoxycarotenoid dioxygenase mRNAs by light Plant Molecular Biology 42, 833–845.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Trejo CL, Davies WJ, Ruiz LMP (1993) Sensitivity of stomata to abscisic acid. Plant Physiology 102, 497–502.
PubMed |
open url image1

Wan CY, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.) Annals of Biochemistry 223, 7–12.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zeevaart JAD, Boyer GL (1984) Accumulation and transport of abscisic acid and its metabolites in Ricinus and Xanthium.  Plant Physiology 4, 934–939. open url image1

Zhang SQ, Outlaw WH (2001) Abscisic acid introduced into the transpiration stream accumulates in the guard-cell apoplast and causes stomatal closure. Plant, Cell and Environment 24, 1045–1054.
Crossref | GoogleScholarGoogle Scholar | open url image1