Skip to main content
Log in

NAA and Ethylene Regulate Expression of Genes Related to Ethylene Biosynthesis, Perception, and Cell Wall Degradation During Fruit Abscission and Ripening in ‘Delicious’ Apples

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Expression of genes for ethylene biosynthesis, ethylene perception, and cell wall degradation in the fruit cortex and abscission zone was examined during fruit abscission and ripening in ‘Delicious’ apples (Malus × domestica). An autocatalytic burst of fruit ethylene production and accelerated fruit softening were associated with increased expression of genes related to ethylene biosynthesis (MdACS and MdACO), whereas reduced expression of ethylene receptor genes (MdETR and MdERS), increased expression of an ethylene signal transduction gene (MdCTR1), and increased expression of genes related to cell wall degradation (MdPG and MdEG) in the fruit cortex occurred during fruit ripening. Aminoethoxyvinylglycine (AVG) or 1−methylcyclopropene (1-MCP) inhibited fruit ethylene production, suppressed expression of MdACS1, MdACO1, MdERS1, and MdPG1 in the fruit cortex, and delayed fruit softening, whereas naphthaleneacetic acid (NAA) increased fruit ethylene production, increased expression of MdACS1, MdACO1, MdERS1 and MdPG1 in the fruit cortex, and accelerated fruit softening. Fruit abscission and expression of MdACS5A, MdACS5B, MdACO1, MdPG2, and MdEG1 in the fruit abscission zone were reduced by AVG and 1-MCP. NAA also reduced fruit abscission while reducing expression of MdPG2 and MdEG1 only in the fruit abscission zone. The levels of MdETR1, MdETR2, MdERS1, and MdERS2 transcripts in the fruit abscission zone decreased during fruit abscission and fruit ripening regardless of treatment. The combination of NAA and AVG was more effective in inhibiting expression of MdPG2 and MdEG1 in the fruit abscission zone and reducing fruit abscission than was either NAA or AVG used alone.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abel S, Theologis A (1996) Early genes and auxin action. Plant Physiol 111:9–17

    Article  PubMed  CAS  Google Scholar 

  • Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot 53:2039–2055

    Article  PubMed  CAS  Google Scholar 

  • Argueso CT, Hansen M, Kieber JJ (2007) Regulation of ethylene biosynthesis. J Plant Growth Regul 26:92–105

    Article  CAS  Google Scholar 

  • Barry CS, Llop-Tous MT, Grierson D (2000) The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato. Plant Physiol 123:979–986

    Article  PubMed  CAS  Google Scholar 

  • Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–40

    Article  PubMed  CAS  Google Scholar 

  • Boller T, Herner RC, Kende H (1979) Assay for the enzymatic formation of an ethylene precursor 1-aminocyclopropane-1-carborylic acid. Planta 145:293–303

    Article  CAS  Google Scholar 

  • Bonghi C, Tonutti P, Ramina A (2000) Biochemical and molecular aspects of fruitlet abscission. Plant Growth Regul 31:35–42

    Article  CAS  Google Scholar 

  • Brown KM (1997) Ethylene and abscission. Physiol Plant 100:567–576

    Article  CAS  Google Scholar 

  • Dal Cin V, Danesin M, Boschetti A, Dorigoni A, Ramina A (2005) Ethylene biosynthesis and perception in apple fruitlet abscission (Malus domestica L. Borck). J Exp Bot 56:2995–3005

    Article  CAS  Google Scholar 

  • Dal Cin V, Rizzini FM, Botton A, Tonutti P (2006) The ethylene biosynthetic and signal transduction pathways are differently affected by 1-MCP in apple and peach fruit. Postharvest Biol Technol 42:125–133

    Article  CAS  Google Scholar 

  • Dandekar AM, Teo G, Defilippi BG, Uratsu SL, Passey AJ, Kader AA, Stow JR, Colgan RJ, James DJ (2004) Effect of down-regulation of ethylene biosynthesis on fruit flavor complex in apple fruit. Transgenic Res 13:373–384

    Article  CAS  Google Scholar 

  • del Campillo E, Bennett AB (1996) Pedicel breakstrength and cellulase gene expression during tomato flower abscission. Plant Physiol 111:813–820

    Article  PubMed  Google Scholar 

  • Edgerton LJ, Blanpied GD (1970) Interaction of succinic acid 2,2-dimethyl hydrazide, 2-chloroethylphosphonic acid and auxins on maturity, quality and abscission of apples. J Am Soc Hortic Sci 95:664–666

    CAS  Google Scholar 

  • El-Sharkawy I, Jones B, Li Z, Lelievre J, Pech JC, Latche A (2003) Isolation and characterization of four ethylene perception elements and their expression during ripening in pears with/without cold requirement. J Exp Bot 54:1615–1625

    Article  PubMed  CAS  Google Scholar 

  • Harada T, Sunako T, Wakasa Y, Soejima J, Satoh T, Niizeki M (2000) An allele of the 1-aminocyclopropane-1-carboxylate synthase gene (Md-ACS1) accounts for the low level of ethylene production in climacteric fruits of some apple cultivars. Theor Appl Genet 101:742–746

    Article  CAS  Google Scholar 

  • Hong SB, Sexton R, Tucker ML (2000) Analysis of gene promoters for two tomato polygalacturonases expressed in abscission zones and the stigma. Plant Physiol 123:869–881

    Article  PubMed  CAS  Google Scholar 

  • Hua J, Meyerowitz EM (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94:261–271

    Article  PubMed  CAS  Google Scholar 

  • Kalaitzis P, Koehler SM, Tucker ML (1995) Cloning of a tomato polygalacturonase expressed in abscission. Plant Mol Biol 28:647–656

    Article  PubMed  CAS  Google Scholar 

  • Kende H (1993) Ethylene biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 44:283–307

    Article  CAS  Google Scholar 

  • Kevany BM, Tieman DM, Taylor MG, Dal Cin V, Klee HJ (2007) Ethylene receptor degradation controls the timing of ripening in tomato fruit. Plant J 51:458–467

    Article  PubMed  CAS  Google Scholar 

  • Klee HJ (2004) Ethylene signal transduction. Moving beyond Arabidopsis. Plant Physiol 135:660–667

    Article  PubMed  CAS  Google Scholar 

  • Lashbrook CC, Tieman DM, Klee HJ (1998) Differential regulation of the tomato ETR gene family throughout plant development. Plant J 15:243–252

    Article  PubMed  CAS  Google Scholar 

  • McMurchie EJ, McGlasson WB, Eaks IL (1972) Treatment of fruit with propane gives information about the biogenesis of ethylene. Nature 237:235–236

    Article  PubMed  CAS  Google Scholar 

  • Meir S, Hunter DA, Chen JC, Halaly V, Reid MS (2006) Molecular changes occurring during acquisition of abscission competence following lowering auxin depletion in Mirabilis jalapa. Plant Physiol 141:1604–1616

    Article  PubMed  CAS  Google Scholar 

  • Osborne DJ (1989) Abscission. CRC Crit Rev Plant Sci 8:103–129

    CAS  Google Scholar 

  • Roberts JA, Elliott KA, Gonzalez-Carranza ZH (2002) Abscission, dehiscence, and other cell separation process. Annu Rev Plant Biol 53:131–158

    Article  PubMed  CAS  Google Scholar 

  • Sato-Nara K, Yuhashi K, Higashi K, Hosoya K, Kubota M, Ezura H (1999) Stage- and tissue-specific expression of ethylene receptor homologue genes during fruit development in muskmelon. Plant Physiol 119:321–329

    Article  Google Scholar 

  • Schupp JR, Greene DW (2004) Effect of aminoethoxyvinylglycine (AVG) on preharvest drop, fruit quality, and maturation of ‘McIntosh’ apples. I. Concentration and timing of dilute applications of AVG. HortScience 39:1030–1035

    CAS  Google Scholar 

  • Sisler EC, Dupille E, Serek M (1996) Effects of 1-methylcyclopropene and methylcyclopropene on ethylene binding and ethylene action on cut carnation. Plant Growth Regul 18:79–86

    Article  CAS  Google Scholar 

  • Smock RM, Gross CR (1947) The effect of some hormone materials on the respiration and softening rates of apples. Proc Am Soc Hortic Sci 49:67–77

    CAS  Google Scholar 

  • Taylor JE, Whitelaw CA (2001) Signals in abscission. New Phytol 151:323–339

    Article  CAS  Google Scholar 

  • Tieman DV, Taylor MG, Ciardi JA, Klee HJ (2000) The tomato ethylene receptors NR and LeETR4 are negative regulators of ethylene response and exhibit functional compensation within a multigene family. Proc Natl Acad Sci USA 97:5663–5668

    Article  PubMed  CAS  Google Scholar 

  • Tonutti P, Cass LG, Christoffersen RE (1995) The expression of cellulase gene family members during induced avocado fruit abscission and ripening. Plant Cell Environ 18:709–703

    Article  CAS  Google Scholar 

  • Tucker ML, Sexton R, Campillo ED, Lewis LN (1988) Bean abscission cellulase. Plant Physiol 88:1257–1262

    PubMed  CAS  Google Scholar 

  • Vandenbussche F, Van Der Straeten D (2007) One for all and all for one: Cross-talk of multiple signals controlling the plant phenotype. J. Plant Growth Regul 26:178–187

    Article  CAS  Google Scholar 

  • Wakasa Y, Kudo H, Ishikawa R, Akada S, Senda M, Niizeki M, Harada T (2006) Low expression of an endopolygalacturonase gene in apple fruit with long-term storage potential. Postharvest Biol Technol 39:193–198

    Article  CAS  Google Scholar 

  • Wan CY, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Anal Biochem 223:7–12

    Article  PubMed  CAS  Google Scholar 

  • Wang KLC, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:S131–S151

    PubMed  CAS  Google Scholar 

  • Wiersma PA, Zhang H, Lu C, Quail A, Toivonen PMA (2007) Survey of the expression of genes for ethylene synthesis and perception during maturation and ripening of ‘Sunrise’ and ‘Golden Delicious’ apple fruit. Postharvest Biol Technol 44:204–211

    Article  CAS  Google Scholar 

  • Yuan R, Carbaugh DH (2007) Effects of NAA, AVG, and 1-MCP on ethylene biosynthesis, preharvest fruit drop, fruit maturity, and quality of ‘Golden Supreme’ and ‘Golden Delicious’ apples. HortScience 42:101–105

    CAS  Google Scholar 

  • Yuan R, Hartmond U, Kender WJ (2001) Physiological factors affecting response of mature ‘Valencia’ oranges to CMN-pyrazole. II. Endogenous concentrations of indole-3-acetic acid, abscisic acid, and ethylene. J Am Soc Hortic Sci 126:420–426

    CAS  Google Scholar 

Download references

Acknowledgments

This research was partly supported by grants from the Virginia Agricultural Council and Virginia Apple Research Program to RY.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rongcai Yuan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, J., Yuan, R. NAA and Ethylene Regulate Expression of Genes Related to Ethylene Biosynthesis, Perception, and Cell Wall Degradation During Fruit Abscission and Ripening in ‘Delicious’ Apples. J Plant Growth Regul 27, 283–295 (2008). https://doi.org/10.1007/s00344-008-9055-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-008-9055-6

Keywords

Navigation