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Indole-3-acetic acid metabolism and growth in young kiwifruit berry

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Abstract

The patterns of auxin concentration and metabolism were investigated in distinct kiwifruit portions and compared with the rate of fruit growth during early developmental stages. Indole-3-acetic acid (IAA) level was higher in inner fruit tissues, particularly in younger fruit, while the hormone was barely detectable in outer tissues. Modulation of free IAA concentration did not appear to depend tightly on conjugation of the hormone. Despite the lack of a strong correlation between the levels of IAA and enzymes involved in its catabolism, in some portions of the fruit a low hormone level corresponded to a higher IAA degradation activity. An inverse correlation was also observed between hormone levels and the appearance/increase in some bands with high mobility in peroxidase gel activity assay. Phenols, compounds with a potential auxin-protecting activity, appeared to be involved mostly in photoprotection of the fruit than in the regulation of IAA levels. Beyond catabolism and conjugation, other metabolic pathways, particularly those occurring in the developing seeds, may have decisively influenced auxin levels in fruit tissues, as well as the amount of the hormone exported from the fruit. The latter, estimated by analyzing the concentration of IAA in the sap exuded from the pedicel, showed a time course which was similar to that displayed by inner fruit tissues. Furthermore, similarities were found between the pattern of IAA concentration in inner fruit tissues and fruit growth rate. The possible role of IAA in promoting growth during early fruit development is discussed.

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References

  • Albacete A, Ghanem ME, Martínez-Andújar C, Acosta M, Sánchez-Bravo J, Martínez V, Lutts S, Dodd IC, Pérez-Alfocea F (2008) Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants. J Exp Bot 59:4119–4131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amarante CVT, Miqueloto A, De Freitas ST, Steffens CA, Silveira, JPG, Corrêa TR (2013) Fruit sampling methods to quantify calcium and magnesium contents to predict bitter pit development in ‘Fuji’ apple: a multivariate approach. Sci Hortic 157:19–23

    Article  Google Scholar 

  • Arezki O, Boxus P, Kevers C, Gaspar T (2001) Changes in peroxidase activity, and level of phenolic compounds during light-induced plantlet regeneration from Eucalyptus camaldulensis Dehn. nodes in vitro. Plant Growth Regul 33:215–219

    Article  CAS  Google Scholar 

  • Bailly C (2004) Active oxygen species and antioxidants in seed biology. Seed Sci Res 14:93–107

    Article  CAS  Google Scholar 

  • Bangerth F (1976) A role for auxin and auxin transport inhibitors on the Ca content of artificially induced parthenocarpic fruits. Physiol Plant 37:191–194

    Article  CAS  Google Scholar 

  • Banuelos GS, Bangerth F, Marschner H (1987) Relationship between polar basipetal auxin transport and acropetal Ca2+ transport into tomato fruits. Physiol Plant 71:321–327

    Article  CAS  Google Scholar 

  • Beffa R, Martin HV, Pilet PE (1990) In vitro oxidation of indoleacetic acid by soluble auxin-oxidases and peroxidases from maize roots. Plant Physiol 94:485–491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bregoli AM, Fabbroni C, Costa F, Raimondi V, Costa G (2007) Auxin and ethylene interaction during fruit growth and ripening of Actinidia deliciosa. In: Ramina A et al (eds) Advances in plant ethylene research: proceedings of the 7th International Symposium on the plant hormone ethylene. Springer, Dordrecht, pp 105–107

    Chapter  Google Scholar 

  • Brenner ML, Cheikh N (1995) The role of hormones in photosynthate partitioning and seed filling. In: Davies PJ (ed.) Plant hormones: physiology, biochemistry and molecular biology, 2nd edn, Kluwer Academic Publishers, Dordrecht, pp. 649–670

    Chapter  Google Scholar 

  • Brookfield PL, Ferguson IB, Watkins CB, Bowen JH (1996) Seed number and calcium concentrations of ‘Braeburn’ apple fruit. J Hortic Sci 71:265–271

    Article  Google Scholar 

  • Brown MM, Ho LC (1993) Factors affecting calcium-transport and basipetal IAA movement in tomato fruit in relation to blossom-end rot. J Exp Bot 44:1111–1117

    Article  CAS  Google Scholar 

  • Chen J, Mao L, Mi H, Lu W, Ying T, Luo Z (2016) Involvement of three annexin genes in the ripening of strawberry fruit regulated by phytohormone and calcium signal transduction. Plant Cell Rep 35:733–743

    Article  CAS  PubMed  Google Scholar 

  • Cheniany M, Ebrahimzadeh H, Masoudi-nejad A, Vahdati K, Leslie C (2010) Effect of endogenous phenols and some antioxidant enzyme activities on rooting of Persian walnut (Juglans regia L.). Afr J Plant Sci 4:479–487

    CAS  Google Scholar 

  • Clark CJ, Smith GS (1988) Seasonal accumulation of mineral nutrients by kiwifruit. 2. Fruit. New Phytol 108:399–409

    Article  CAS  Google Scholar 

  • Clark CJ, Smith GS (1991) Seasonal changes in the form and distribution of calcium in the fruit of kiwifruit vines. J Hortic Sci 66:747–753

    Article  CAS  Google Scholar 

  • Cutting JGM, Bower JP (1989) The relationship between basipetal auxin transport and calcium allocation in vegetative and reproductive flushes in avocado. Sci Hortic 41:27–34

    Article  Google Scholar 

  • Cutting JC, Lishman AW, Hofman PJ, Wolstenholme BN (1986) Plant growth substance trends in developing avocado fruit as determined by radioimmunoassay. Acta Hortic 175:285–290

    Article  Google Scholar 

  • Davies PJ (2010) The plant hormones: their nature, occurrence, and functions. In: Davies PJ (ed.) Plant hormones. biosynthesis, signal transduction, action! Revised 3rd edn, Springer, Dordrecht, pp. 1–15

    Google Scholar 

  • Devoghalaere F, Doucen T, Guitton B, Keeling J, Payne W, Ling TJ, Ross JJ, Hallett IC, Gunaseelan K, Dayatilake GA, Diak R, Breen KC, Tustin DS, Costes E, Chagné D, Schaffer RJ, David KM (2012) A genomics approach to understanding the role of auxin in apple (Malus x domestica) fruit size control. BMC Plant Biol 12:7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Faust M, Shear CB, Brooks HJ (1969) Mineral element gradients in pears. J Sci Food Agric 20:257–258

    Article  Google Scholar 

  • Ferguson IB (1980) Movement of mineral nutrients into the developing fruit of the kiwifruit (Actinidia chinensis Planch.). N Z J Agric Res 23: 349–353

    Article  CAS  Google Scholar 

  • Ferguson AR (1984) Kiwifruit: a botanical review. Hortic Rev 6:1–64

    Google Scholar 

  • Ferguson IB, Volz R, Woolf A (1999) Preharvest factors affecting physiological disorders of fruit. Postharvest Biol Technol 15: 255–262

    Article  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Hocking B, Tyerman SD, Burton RA, Gilliham M (2016) Fruit calcium: transport and physiology. Front Plant Sci 7:569

    Article  PubMed  PubMed Central  Google Scholar 

  • Hopping ME (1976) Structure and development of fruit and seeds in Chinese gooseberry (Actinidia chinensis Planch.). N Z J Bot 14:63–68

    Article  Google Scholar 

  • Howpage D, Spooner-Hart RN, Vithanage V (2001) Influence of honey bee (Apis mellifera) on kiwifruit pollination and fruit quality under Australian conditions. N Z J Crop Hortic 29: 51–59

    Article  Google Scholar 

  • Huyskens-Keil S, Eichholz I, Kroh LW, Rohn S (2007) UV-B induced changes of phenol composition and antioxidant activity in black currant fruit (Ribes nigrum L.). J Appl Bot Food Qual 81:140–144

    CAS  Google Scholar 

  • Kefeli VI, Kalevitch MV, Borsari B (2003) Phenolic cycle in plants and environment. J Cell Mol Biol 2:13–18

    Google Scholar 

  • Kojima K (2005) Phytohormones in shoots and fruits of tomato; apoplast solution and seedless fruit. JARQ 39:77–81

    Article  CAS  Google Scholar 

  • Krylov SN, Dunford HB (1996) Detailed model of the peroxidase-catalyzed oxidation of indole-3-acetic acid at neutral pH. J Phys Chem 100:913–920

    Article  CAS  Google Scholar 

  • Kumar R, Khurana A, Sharma AK (2014) Role of plant hormones and their interplay in development and ripening of fleshy fruits. J Exp Bot 65:4561–4575

    Article  CAS  PubMed  Google Scholar 

  • Lattanzio V, Lattanzio VMT, Cardinali A (2006) Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects. In: Imperato F (ed.) Phytochemistry: Advances in Research, Research Signpost, Trivandrum, pp. 23–67

    Google Scholar 

  • Lee BR, Kim KY, Jung WJ, Avice JC, Ourry A, Kim TH (2007) Peroxidases and lignification in relation to the intensity of water-deficit stress in white clover (Trifolium repens L.). J Exp Bot 58:1271–1279

    Article  CAS  PubMed  Google Scholar 

  • Lepeduš H, Jozić M, Štolfa I, Pavičić N, Hackenbereger K, Cesar V (2005) Changes in peroxidase activity in the peel of Unshiu mandarin (Citrus unshiu Marc.) fruit with different storage treatments. Food Technol Biotechnol 43:71–77

    Google Scholar 

  • Li W, Liu Y, Zeng S, Xiao G, Wang G, Wang Y, Peng M, Huang H (2015) Correction: Gene expression profiling of development and anthocyanin accumulation in kiwifruit (Actinidia chinensis) based on transcriptome sequencing. PLoS ONE 10(9):e0138743. doi:10.1371/journal.pone.0138743

    Article  PubMed  PubMed Central  Google Scholar 

  • Ljung K (2013) Auxin metabolism and homeostasis during plant development. Development 140:943–950

    Article  CAS  PubMed  Google Scholar 

  • Marzinek J, Mourão KSM (2003) Morphology and anatomy of the fruit and seed in development of Chorisia speciosa A. St.-Hil.—Bombacaceae. Rev Bras Bot 26: 23–34

    Article  Google Scholar 

  • Mazzeo M, Dichio B, Clearwater MJ, Montanaro G, Xiloyannis C (2013) Hydraulic resistance of developing Actinidia fruit. Ann Bot 112:197–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McLaughlin SB, Wimmer R (1999) Tansley review no. 104 calcium physiology and terrestrial ecosystem processes. New Phytol 142:373–417

    Article  CAS  Google Scholar 

  • McPherson HG, Richardson AC, Snelgar WP, Patterson KJ, Currie MB (2001) Flower quality and fruit size in kiwifruit (Actinidia deliciosa). N Z J Crop Hortic 29: 93–101

    Article  Google Scholar 

  • Mellor N, Band LR, Pěnčík A, Novác O, Rashed A, Holman T, Wilson MH, Voβ U, Bishopp A, King JR, Ljung K, Bennett MJ, Owen MR (2016) Dynamic regulation of auxin oxidase and conjugating enzymes AtDAO1 and GH3 modulates auxin homeostasis. PNAS 113:11022–11027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Milone MT, Sgherri C, Clijsters H, Navari-Izzo F (2003) Antioxidative responses of wheat treated with realistic concentration of cadmium. Environ Exp Bot 50:265–276

    Article  CAS  Google Scholar 

  • Montanaro G, Treutter D, Xiloyannis C (2007) Phenolic compounds in young developing kiwifruit in relation to light exposure: implications for fruit calcium accumulation. J Plant Interact 2(1):63–69

    Article  CAS  Google Scholar 

  • Montanaro G, Dichio B, Xiloyannis C (2010) Significance of fruit transpiration on calcium nutrition in developing apricot fruit. J Plant Nutr Soil Sci 173:618–622

    Article  CAS  Google Scholar 

  • Montanaro G, Dichio B, Lang A, Mininni AN, Nuzzo V, Clearwater MJ, Xiloyannis C (2014) Internal versus external control of calcium nutrition in kiwifruit. J Plant Nutr Soil Sci 177:819–830

    Article  CAS  Google Scholar 

  • Montanaro G, Dichio B, Lang A, Mininni AN, Xiloyannis C (2015) Fruit calcium accumulation coupled and uncoupled from its transpiration in kiwifruit. J Plant Physiol 181:67–74

    Article  CAS  PubMed  Google Scholar 

  • 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. Ann Bot 105:913–923

    Article  PubMed  PubMed Central  Google Scholar 

  • Normanly J, Slovin JP, Cohen JD (2010) Hormone biosynthesis, metabolism and its regulation. Auxin biosynthesis and metabolism. In: Davies PJ (ed.) Plant hormones. Biosynthesis, signal transduction, action!, Revised 3rd ed, Springer, Dordrecht, pp. 36–62

    Google Scholar 

  • Ozga JA, van Huizen R, Reinecke DM (2002) Hormone and seed-specific regulation of pea fruit growth. Plant Physiol 128:1379–1389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pattison RJ, Català C (2012) Evaluating auxin distribution in tomato (Solanum lycopersicum) through an analysis of the PIN and AUX/LAX gene families. Plant J 70:585–598

    Article  CAS  PubMed  Google Scholar 

  • Pattison RJ, Csukasia F, Català C (2014) Mechanisms regulating auxin action during fruit development. Physiol Plant 151:62–72

    Article  CAS  PubMed  Google Scholar 

  • Pilet P-E, Lavanchy P (1969) Purification d’extraits peroxydasiques (Racine de Lens) à activité ‘auxines-oxydasique’. Physiol Veg 7:19–29

    CAS  Google Scholar 

  • Porco S, Pěnčík A, Rashed A, Voβ U, Casanova-Sáez R, Bishopp A, Golebiowska A, Bhosale R, Swarup R, Swarup K, Peňáková P, Novák O, Staswick P, Hedden P, Phillips AL, Vissenberg K, Bennett MJ, Ljung K (2016) Dioxygenase-encoding AtDAO1 gene controls IAA oxidation and homeostasis in Arabidopsis. PNAS 113:11016–11021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pratt HS, Reid MS (1974) Chinese gooseberry: seasonal patterns in fruit growth and maturation, ripening, respiration and the role of ethylene. J Sci Food Agr 25:747–757

    Article  CAS  Google Scholar 

  • Purgatto E, do Nascimento JR, Lajolo FM, Cordenunsi BR (2002) The onset of starch degradation during banana ripening is concomitant to changes in the content of free and conjugated forms of indole-3-acetic acid. J Plant Physiol 159:1105–1111

    Article  CAS  Google Scholar 

  • Solar A, Colarič M, Usenik V, Stampar F (2006) Seasonal variations of selected flavonoids, phenolic acids and quinones in annual shoots of common walnut (Juglans regia L.). Plant Sci 170:453–461

    Article  CAS  Google Scholar 

  • Sorce C, Lombardi L, Giorgetti L, Parisi B, Ranalli P, Lorenzi R (2009) Indoleacetic acid concentration and metabolism changes during bud development in tubers of two potato (Solanum tuberosum) cultivars. J Plant Physiol 166:1023–1033

    Article  CAS  PubMed  Google Scholar 

  • Sorce C, Lombardi L, Remorini D, Montanaro G (2011) Occurrence of natural auxin and accumulation of calcium during early fruit development in kiwifruit. Aust J Crop Sci 5:895–898

    CAS  Google Scholar 

  • Sorce C, Giovannelli A, Sebastiani L, Anfodillo T (2013) Hormonal signals involved in the regulation of cambial activity, xylogenesis and vessel patterning in trees. Plant Cell Rep 32:885–898

    Article  CAS  PubMed  Google Scholar 

  • Stahly EA, Benson NR (1970) Calcium levels of ‘golden delicious’ apples sprayed with 2,3,5-triidrobenzoic acid. J Am Soc Hortic Sci 95:726–727

    CAS  Google Scholar 

  • Thomas RL, Jen JJ, Morr CV (1982) Changes in soluble and bound peroxidase—IAA oxidase during tomato fruit development. J Food Sci 47:158–161

    Article  Google Scholar 

  • Tiwari A, Vivian-Smith A, Ljung K, Offringa R, Heuvelink E (2013) Physiological and morphological changes during early and later stages of fruit growth in Capsicum annuum. Physiol Plant 147:396–406

    Article  CAS  PubMed  Google Scholar 

  • Vanneste S, Friml J (2013) Calcium: the missing link in auxin action. Plants 2:650–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Varga A, Bruinsma J (1976) Roles of seeds and auxins in tomato fruit growth. Z Pflanzenphysiol 80: 85–104

    Article  Google Scholar 

  • Volz RK, Tustin DS, Ferguson IB (1996) Pollination effects on fruit mineral composition, seeds and cropping characteristics of ‘Braeburn’ apple trees. Sci Hortic 66:169–180

    Article  CAS  Google Scholar 

  • Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Lin JE, Harris C, Pereira FCM, Wu F, Blakeslee JJ, Peer WA (2016) DAO1 catalyzes temporal and tissue-specific oxidative inactivation of auxin in Arabidopsis thaliana. PNAS 113:11010–11015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Z, Zhang Y, Liu X, Zhang X, Liu S, Yu X, Ren Y, Zheng X, Zhou K, Jiang L, Guo X, Gai Y, Wu C, Zhai H, Wang H, Wan J (2013) A role for a dioxygenase in auxin metabolism and reproductive development in rice. Dev Cell 27:113–122

    Article  CAS  PubMed  Google Scholar 

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GM was supported by an RTDb research contract (No. 06/2016).

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Correspondence to Carmelina Spanò.

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Sorce, C., Montanaro, G., Bottega, S. et al. Indole-3-acetic acid metabolism and growth in young kiwifruit berry. Plant Growth Regul 82, 505–515 (2017). https://doi.org/10.1007/s10725-017-0279-y

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