Skip to main content
SpringerLink
Log in

Xanthine dehydrogenase and aldehyde oxidase impact plant hormone homeostasis and affect fruit size in ‘Hass’ avocado

  • Original Article
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

The contribution of xanthine dehydrogenase (XDH, EC 1.1.1.204) to fruit size was investigated using the normal and small-fruit variants of Persea americana Mill. cv. ‘Hass’. Inhibition of XDH by treatment of normal fruit, in the linear phase of growth (phase II), with allopurinol (Allo) arrested fruit growth. Adenine (Ade), a less effective inhibitor of this enzyme, also arrested fruit growth when applied in phase II and slowed fruit growth when applied in phase III. A time-course study on the activity of XDH in mesocarp tissue from normal and small fruit showed that maximum activity occurred late in phase II and that the peak in activity was absent in mesocarp of the small fruit. Feeding Ade to growing fruit in phase III caused a transient decline in fruit growth (measured as change in fruit length). Thereafter, growth resumed although fruit size was irreversibly affected. Treatment of fruit with Ade and Ade-containing cytokinins altered activity of another molybdenum enzyme, aldehyde oxidase (EC 1.2.3.1). Cytokinin oxidase was induced by cytokinin and auxin. Purine catabolism via hypoxanthine/xanthine was operative in normal fruit and in mesocarp from the small-fruit variant and as expected, Allo treatment caused accumulation of xanthine and adenine. In the absence of an increase in XDH during growth of the small-fruit phenotype, low levels of Ade were interpreted as resulting from respiration-enhanced adenylate depletion. Stress and/or pathogen induction of the alternative oxidase pathway is proposed as a possible cause.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2A, B
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Anderson JD (1977) Responses of adenine nucleotides in germinating soybean embryonic axes to exogenously applied adenine and adenosine. Plant Physiol 60:689–692

    CAS  Google Scholar 

  • Ashihara H (1983) Changes in activities of purine salvage and ureide synthesis during germination of black gram (Phaseolus mungo) seeds. Z Pflanzenphysiol 113:47–60

    CAS  Google Scholar 

  • Ashihara H, Crozier A (1999) Biosynthesis and metabolism of caffeine and related purine alkaloids in plants. Adv Bot Res 30:118–205

    Google Scholar 

  • Ashihara H, Stasolla C, Loukanina N, Thorpe TA (2001) Purine metabolism during white spruce somatic embryo development: salvage of adenine, adenosine, and inosine. Plant Sci 160:647–657

    Article  CAS  PubMed  Google Scholar 

  • Barabás NK, Omarov RT, Erdei L, Lips SH (2000) Distribution of the Mo-enzymes aldehyde oxidase, xanthine dehydrogenase and nitrate reductase in maize (Zea mays L.) nodal roots as affected by nitrogen and salinity. Plant Sci 155:49–58

    Article  PubMed  Google Scholar 

  • Bittner F, Oreb M, Mendel RR (2001) ABA3 is a molybdenum cofactor sulfurase required for activation of aldehyde oxidase and xanthine dehydrogenase in Arabidopsis thaliana. J Biol Chem 276:40381–40384

    Article  CAS  PubMed  Google Scholar 

  • Blanke MM, Whiley AW (1995) Bioenergetics and water relations of developing avocado fruit. J Plant Physiol 145:87–92

    CAS  Google Scholar 

  • Boland MJ (1981) NAD+:xanthine dehydrogenase from nodules of navy beans: partial purification and properties. Biochem Int 2:567–574

    CAS  Google Scholar 

  • Boland MJ, Blevins DG, Randall DD (1983) Soybean nodule xanthine dehydrogenase: a kinetic study. Arch Biochem Biophys 222:435–441

    CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitative determination of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Bray RC (1975) Molybdenum iron-sulfur flavin hydroxylases and related enzymes. In: Boyer PD (ed) The enzymes, vol 12, part B. Academic, New York, pp 299–419

  • Cames MG, Wright MS (1988) Endosperm hormone levels of immature corn kernels of A188, Missouri 17, and DeKalb XL-12. Plant Sci 57:195–203

    Article  Google Scholar 

  • Corpas FJ, de la Colina C, Sanchez-Rasero F, del Rio LA (1997) A role of leaf peroxisomes in the catabolism of purines. J Plant Physiol 151:246–250

    CAS  Google Scholar 

  • Coruzzi GM, Zhou L (2001) Carbon and nitrogen sensing and signaling in plants: emerging matrix effects. Curr Opin Plant Biol 4:247–253

    Google Scholar 

  • Cowan AK, Moore-Gordon CS, Bertling I, Wolstenholme BN (1997) Metabolic control of avocado fruit growth. Isoprenoid growth regulators and the reaction catalysed by 3-hydroxy-3-methylglutaryl coenzyme A reductase. Plant Physiol 114:511–518

    CAS  PubMed  Google Scholar 

  • Cowan AK, Cairns ALP, Bartels-Rham B (1999) Regulation of abscisic acid metabolism: towards a metabolic basis for abscisic acid-cytokinin antagonism. J Exp Bot 50:595–603

    Article  CAS  Google Scholar 

  • Cowan AK, Cripps RF, Richings EW, Taylor NJ (2001) Fruit size: towards an understanding of the metabolic control of fruit growth using avocado as a model system. Physiol Plant 111:127–136

    Article  CAS  Google Scholar 

  • Davenport TL, Manners MM (1982) Nucellar senescence and ethylene production as they relate to avocado fruitlet abscission. J Exp Bot 33:815–825

    CAS  Google Scholar 

  • Eklöf S, Åstot C, Blackwell J, Moritz T, Olsson O, Sandberg G (1997) Auxin-cytokinin interactions in wild-type and transgenic tobacco. Plant Cell Physiol 38:225–235

    Google Scholar 

  • Gazit S, Blumenfeld A (1972) Inhibitor and auxin activity in the avocado fruit. Physiol Plant 27:77–82

    CAS  Google Scholar 

  • Gillaspy G, Ben-David H, Gruissem W (1993) Fruits: a developmental perspective. Plant Cell 5:1439–1451

    Google Scholar 

  • Gilmore AM, Björkman O (1994) Adenine nucleotides and xanthophyll cycle in leaves. I. Effects of CO2 and temperature-limited photosynthesis on adenylate energy charge and violaxanthin de-epoxidation. Planta 192:526–536

    CAS  Google Scholar 

  • Giovannoni J (2001) Molecular biology of fruit maturation and ripening. Annu Rev Plant Mol Biol Plant Physiol 52:725–749

    Article  CAS  Google Scholar 

  • Guranowski A, Barankiewicz J (1979) Purine salvage in cotyledons of germinating lupin seeds. FEBS Lett 104:95–98

    Article  CAS  PubMed  Google Scholar 

  • Guranowski A, Wasternack C (1982) Adenine and adenosine metabolizing enzymes in cell-free extracts from Euglena gracilis. Comp Biochem Physiol B 71:483–488

    Article  CAS  PubMed  Google Scholar 

  • Jordan RI, Dodds JA, Ohr HD (1983) Evidence for virus like agents in avocado. Phytopathology 73:1130–1135

    Google Scholar 

  • Kamínek M, Motyka V, Vaňková R (1997) Regulation of cytokinin content in plant cells. Physiol Plant 101:689–700

    Article  Google Scholar 

  • Kisker C, Schindelin H, Rees DC (1997) Molybdenum-cofactor-containing enzymes: structure and mechanism. Annu Rev Biochem 66:233–267

    CAS  PubMed  Google Scholar 

  • Koshiba T, Saito E, Ono N, Yamamoto N, Sato M (1996) Purification and properties of flavin- and molybdenum-containing aldehyde oxidase from coleoptiles of maize. Plant Physiol 110:781–789

    CAS  PubMed  Google Scholar 

  • Kumar R, Taneja VA (1977) Xanthine oxidase in lentil (Lens esculenta) seedlings. Biochim Biophys Acta 485:489–491

    Article  CAS  PubMed  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    PubMed  Google Scholar 

  • Loef I, Stitt M, Geigenberger P (2001) Increased levels of adenine nucleotides modify the interaction between starch synthesis and respiration when adenine is supplied to discs from growing potato tubers. Planta 212:782–791

    Article  CAS  PubMed  Google Scholar 

  • Lur HS, Setter TL (1993) Role of auxin in maize endosperm development. Plant Physiol 103:273–280

    CAS  PubMed  Google Scholar 

  • Masferrer A, Arró M, Manzano D, Schaller H, Fernández-Busqueta X, Moncaleán P, Fernández B, Cunillera N, Boronat A, Ferrer A (2002) Overexpression of Arabidopsis thaliana farnesyl diphosphate synthase (FPS1S) in transgenic Arabidopsis induces a cell death/senescence-like response and reduced cytokinin levels. Plant J 30:123–132

    Article  CAS  PubMed  Google Scholar 

  • Mendel RR, Schwarz G (1999) Molybdoenzymes and molybdenum cofactor in plants. Crit Rev Plant Sci 18:33–69

    Article  CAS  Google Scholar 

  • Mizukami Y (2001) A matter of size: developmental control of organ size in plants. Curr Opin Plant Biol 4:533–539

    Article  CAS  PubMed  Google Scholar 

  • Montalbini P (1993) Xanthine oxidase activity in the susceptible and hypersensitive responses of tobacco leaves to tobacco mosaic virus infection. J Phytopath 139:177–186

    CAS  Google Scholar 

  • Montalbini P (1998) Purification and some properties of xanthine dehydrogenase from wheat leaves. Plant Sci 134:89–102

    Article  CAS  Google Scholar 

  • Montalbini P (2000) Xanthine dehydrogenase from leaves of leguminous plants: purification, characterization and properties of the enzyme. J Plant Physiol 156:3–16

    CAS  Google Scholar 

  • Moore-Gordon CS, Cowan AK, Bertling I, Botha CEJ, Cross RHM (1998) Symplastic solute transport and avocado fruit development: a decline in cytokinin/ABA ratio is related to appearance of the Hass small fruit variant. Plant Cell Physiol 39:1027–1038

    CAS  Google Scholar 

  • Motyka V, Kamínek M (1994) Cytokinin oxidase from auxin- and cytokinin-dependent callus cultures of tobacco (Nicotiana tabacum L.). J Plant Growth Regul 13:1–9

    CAS  Google Scholar 

  • Nguyen J (1979) Effect of light deamination and oxidation of adenylic compounds in cotyledons of Pharbitis nil. Physiol Plant 46:255–259

    CAS  Google Scholar 

  • Nguyen J (1986) Plant xanthine dehydrogenase: its distribution, properties and function. Physiol Vég 24:263–281

  • Nguyen J, Feierabend J (1978) Some properties and subcellular localization of xanthine dehydrogenase in pea leaves. Plant Sci Lett 13:125–132

    Article  CAS  Google Scholar 

  • Nguyen J, Machal L, Perrot-Rechenmann C, Gadal P (1986) Immunochemical studies on xanthine dehydrogenase of soybean root nodules. Ontogenic changes in the level of enzyme and immunocytochemical localization. Planta 167:190–195

    CAS  Google Scholar 

  • Nobusawa E, Ashihara H (1983) Purine metabolism in cotyledons and embryonic axes of black gram (Phaseolus mungo) seedlings. Int J Biochem 15:1059–1065

    Article  CAS  Google Scholar 

  • Nygaard J (1973) Nucleotide metabolism during pollen germination. Physiol Plant 28:361–371

    CAS  Google Scholar 

  • Omarov RT, Sagi M, Lips SH (1998) Regulation of aldehyde oxidase and nitrate reductase in roots of barley (Hordeum vulgare L.) by nitrogen source and salinity. J Exp Bot 49:897–902

    Article  CAS  Google Scholar 

  • Palni LMS, Burch L, Horgan R (1988) The effect of auxin concentration on cytokinin stability and metabolism. Planta 174:231–234

    CAS  Google Scholar 

  • Redig P, Motyka V, van Onckelen HA, Kamínek M (1997) Regulation of cytokinin oxidase activity in tobacco callus expressing the T-DNA ipt gene. Physiol Plant 99:89–96

    Article  CAS  Google Scholar 

  • Richings EW, Cripps RF, Cowan AK (2000) Factors affecting ‘Hass’ avocado fruit size: carbohydrate, abscisic acid and isoprenoid metabolism in normal and phenotypically small fruit. Physiol Plant 109:81–89

    Article  CAS  Google Scholar 

  • Rothe GM (1974) Aldehyde oxidase isoenzymes (EC 1.2.3.1) in potato tubers (Solanum tuberosum). Plant Cell Physiol 15:493–499

    CAS  Google Scholar 

  • Sagi M, Lips SH (1998) The levels of nitrate reductase and Moco in annual ryegrass as affected by nitrate and ammonium nutrition. Plant Sci 135:17–24

    Article  CAS  Google Scholar 

  • Sagi M, Savdov NA, L’vov NP, Lips SH (1997) Nitrate reductase and molybdenum cofactor in annual ryegrass as affected by salinity and nitrogen source. Physiol Plant 99:546–553

    Article  CAS  Google Scholar 

  • Sagi M, Omarov RT, Lips SH (1998) The Mo-hydroxylases xanthine dehydrogenase and aldehyde oxidase in ryegrass as affected by nitrogen and salinity. Plant Sci 135:125–135

    Article  CAS  Google Scholar 

  • Sagi M, Fluhr R, Lips SH (1999) Aldehyde oxidase and xanthine dehydrogenase in a flacca tomato mutant with deficient abscisic acid and wilty phenotype. Plant Physiol 120:571–577

    Article  CAS  PubMed  Google Scholar 

  • Sagi M, Scazzocchio C, Fluhr R (2002) The absence of molybdenum cofactor sulfuration is the primary cause of the flacca phenotype in tomato plants. Plant J 31:305–317

    Article  CAS  PubMed  Google Scholar 

  • Sauer P, Frébortová J, Šebela M, Galuszka P, Jacobsen S, Peč P, Frébort I (2002) Xanthine dehydrogenase of pea seedlings: a member of the plant molybdenum oxidoreductase family. Plant Physiol Biochem 40:393–400

    Article  CAS  Google Scholar 

  • Seo M, Peeters AJM, Koiwai H, Oritani T, Marion-Poll A, Zeevaart JAD, Koornneef M, Kamiya Y, Koshiba T (2000a) The Arabidopsis aldehyde oxidase 3 (AAO3) gene product catalyzes the final step in abscisic acid biosynthesis in leaves. Proc Natl Acad Sci USA 97:12908–12913

    Article  CAS  PubMed  Google Scholar 

  • Seo M, Koiwai H, Akaba S, Komano T, Oritani T, Kamiya Y, Koshiba T (2000b) Abscisic aldehyde oxidase in leaves of Arabidopsis thaliana. Plant J 23:481–488

    Article  CAS  PubMed  Google Scholar 

  • Shimazaki A, Ashihara H (1982) Adenine and guanine salvage in cultured cells of Catharanthus roseus. Ann Bot 50:531–534

    CAS  Google Scholar 

  • Siedow JN, Day DA (2000) Respiration and photorespiration. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiology, Rockville, pp 676–728

  • Simons BH, Mulder L, Van Loon LC, Lambers H (1999) Enhanced expression and activation of the alternative oxidase in the interaction of Arabidopsis with pathogenic Pseudomonas syringae. Plant Physiol 120:529–538

    CAS  PubMed  Google Scholar 

  • Smith PMC, Atkins CA (2002) Purine biosynthesis, big in cell division, even bigger in nitrogen assimilation. Plant Physiol 128:793–802

    Article  CAS  PubMed  Google Scholar 

  • Stasolla C, Loukanina N, Ashihara H, Yeung EC, Thorpe TA (2001) Purine and pyrimidine metabolism during partial drying treatment of white spruce (Piccea glauca) somatic embryos. Physiol Plant 111:93–101

    Article  CAS  Google Scholar 

  • Stasolla C, Katahira R, Thorpe TA, Ashihara H (2003) Purine and pyrimidine nucleotide metabolism in higher plants. J Plant Physiol 160:1271–1295

    CAS  PubMed  Google Scholar 

  • Suzuki T, Takahachi E (1975) Metabolism of xanthine and hypoxanthine in the tea plant (Thea sinensis L.) Biochem J 146:79–85

  • Tajima S, Yamamoto Y (1975) Enzymes of purine catabolism in soybean plants. Plant Cell Physiol 16:271–282

    CAS  Google Scholar 

  • Taylor N, Cowan K (2001) Plant hormone homeostasis and the control of avocado fruit size. Plant Growth Regul 35:247–255

    Article  CAS  Google Scholar 

  • Triplett EW, Blevins DG, Randall DD (1982) Purification and properties of soybean nodule xanthine dehydrogenase. Arch Biochem Biophys 219:39–46

    CAS  PubMed  Google Scholar 

  • Vitória AP, Mazzafera P (1999) Xanthine degradation and related enzyme activities in leaves and fruits of two Coffea species differing in caffeine catabolism. J Agric Food Chem 47:1851–1855

    Article  PubMed  Google Scholar 

  • Wasternack C (1982) Metabolism of pyrimidine and purines. In: Pirson A, Zimmermann MH (eds) Encyclopedia of plant physiology, NS, vol 14B. Springer, Berlin Heidelberg New York, pp 263–301

  • Weir E, Fischer JR (1970) The effect of allopurinol on the excretion of oxypurines by the chick. Biochim Biophys Acta 222:556–557

    Article  CAS  PubMed  Google Scholar 

  • Xiong L, Ishitani M, Lee H, Zhu J-K (2001) The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression. Plant Cell 13:2063–2083

    Article  CAS  PubMed  Google Scholar 

  • Yabuki N, Ashihara H (1991) Catabolism of adenine nucleotides in suspension-cultured plant cells. Biochim Biophys Acta 1073:474–480

    Article  CAS  PubMed  Google Scholar 

  • Zažímalová E, Kamínek M, Březinová A, Motyka V (1999) Control of cytokinin biosynthesis and metabolism. In: Hooykaas PJJ, Hall MA, Libbenga KR (eds) Biochemistry and molecular biology of plant hormones. Elsevier, Amsterdam, pp 141–160

Download references

Acknowledgements

This research was supported by grants from the National Research Foundation (GUN 2034569), the University of Natal, and the South African Avocado Growers’ Association.

Author information

Authors and Affiliations

  1. Nutra-Park Inc., Suite 140, 3225 Deming Way, Middleton, WI 53562, USA

    A. Keith Cowan

  2. Research Centre for Plant Growth and Development, University of Natal-Pietermaritzburg, Scottsville, South Africa

    Nicky J. Taylor

Authors
  1. Nicky J. Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Keith Cowan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. Keith Cowan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Taylor, N.J., Cowan, A.K. Xanthine dehydrogenase and aldehyde oxidase impact plant hormone homeostasis and affect fruit size in ‘Hass’ avocado. J Plant Res 117, 121–130 (2004). https://doi.org/10.1007/s10265-003-0136-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-003-0136-0

Keywords

Search

Navigation