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.
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References
Abel S, Theologis A (1996) Early genes and auxin action. Plant Physiol 111:9–17
Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot 53:2039–2055
Argueso CT, Hansen M, Kieber JJ (2007) Regulation of ethylene biosynthesis. J Plant Growth Regul 26:92–105
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
Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–40
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
Bonghi C, Tonutti P, Ramina A (2000) Biochemical and molecular aspects of fruitlet abscission. Plant Growth Regul 31:35–42
Brown KM (1997) Ethylene and abscission. Physiol Plant 100:567–576
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
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
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
del Campillo E, Bennett AB (1996) Pedicel breakstrength and cellulase gene expression during tomato flower abscission. Plant Physiol 111:813–820
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
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
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
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
Hua J, Meyerowitz EM (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94:261–271
Kalaitzis P, Koehler SM, Tucker ML (1995) Cloning of a tomato polygalacturonase expressed in abscission. Plant Mol Biol 28:647–656
Kende H (1993) Ethylene biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 44:283–307
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
Klee HJ (2004) Ethylene signal transduction. Moving beyond Arabidopsis. Plant Physiol 135:660–667
Lashbrook CC, Tieman DM, Klee HJ (1998) Differential regulation of the tomato ETR gene family throughout plant development. Plant J 15:243–252
McMurchie EJ, McGlasson WB, Eaks IL (1972) Treatment of fruit with propane gives information about the biogenesis of ethylene. Nature 237:235–236
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
Osborne DJ (1989) Abscission. CRC Crit Rev Plant Sci 8:103–129
Roberts JA, Elliott KA, Gonzalez-Carranza ZH (2002) Abscission, dehiscence, and other cell separation process. Annu Rev Plant Biol 53:131–158
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
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
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
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
Taylor JE, Whitelaw CA (2001) Signals in abscission. New Phytol 151:323–339
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
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
Tucker ML, Sexton R, Campillo ED, Lewis LN (1988) Bean abscission cellulase. Plant Physiol 88:1257–1262
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
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
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
Wang KLC, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:S131–S151
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
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
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
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This research was partly supported by grants from the Virginia Agricultural Council and Virginia Apple Research Program to RY.
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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
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DOI: https://doi.org/10.1007/s00344-008-9055-6