Abstract
The primary factors that determine the longevity of cut roses are variable and depend on a cultivar’s sensitivity to ethylene. The vase life of ethylene-sensitive cultivars (SENS) is shortened by ethylene synthesis, while for ethylene-insensitive cultivars (INSENS) it is strongly related to water stress. In this study, we determined the effect of ethylene binding on the change in ethylene sensitivity in two rose cultivars with different sensitivities to the hormone. In addition, we determined the effects of ethylene binding and synthesis inhibition on flower senescence and gene expression using 1-methylcyclopropene (1-MCP) and aminoethoxyvinylglycine (AVG). The relationship between the mRNA levels of ethylene biosynthesis, receptor, and signaling genes and the degree of ethylene sensitivity was determined during flower development and senescence. The results showed that simultaneous treatment with AVG and 1-MCP effectively improved water balance, maintained leaf chlorophyll fluorescence ratios, and consequently extended the vase life of cut flowers for both SENS and INSENS cultivars. The results also revealed that the expression of the ethylene biosynthesis (RhACS2 and RhACO1) genes in cut roses was effectively suppressed by simultaneous treatments with both AVG and 1-MCP. The ethylene-induced induction of RhETR1-5 transcript levels and the degradation of RhCTR1-2 were both repressed by AVG and 1-MCP treatments; consequently, RhEIN3s transcripts were greatly inhibited in both SENS and INSENS cultivars. The findings from the current study revealed that a simultaneous inhibition of ethylene binding and synthesis suppressed plant responses to ethylene and consequently extended the vase life for cut rose flowers in both ethylene-sensitive and ethylene-insensitive cultivars.
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References
Ahmadi N, Mibus H, Serek M (2009) Characterization of ethylene-induced organ abscission in F1 breeding lines of miniature roses (Rosa hybrida L.). Postharvest Biol Technol 52(3):260–266. https://doi.org/10.1016/j.postharvbio.2008.12.010
Andersen L, Williams M, Serek M (2004) Reduced water availability improves drought tolerance of potted miniature roses: is the ethylene pathway involved? J Hortic Sci Biotechnol 79(1):1–13. https://doi.org/10.1080/14620316.2004.11511719
Barry CS, Giovannoni JJ (2007) Ethylene and fruit ripening. Plant Growth Regul 26(2):143. https://doi.org/10.1007/s00344-007-9002-y
Binder BM, Mortimore LA, Stepanova AN, Ecker JR, Bleecker AB (2004) Short-term growth responses to ethylene in Arabidopsis seedlings are EIN3/EIL1 independent. Plant Physiol 136(2):2921–2927. https://doi.org/10.1104/pp.104.050393
Blankenship SM, Dole JM (2003) 1-Methylcyclopropene: a review. Postharvest Biol Technol 28(1):1–25. https://doi.org/10.1016/S0925-5214(02)00246-6
Borochov A, Woodson WR (1989) Physiology and biochemistry of flower petal senescence. Hortic Rev 11: 15–43
Cameron AC, Reid MS (2001) 1-MCP blocks ethylene-induced petal abscission of Pelargonium peltatum but the effect is transient. Postharvest Biol Technol 22(2):169–177. https://doi.org/10.1016/S0925-5214(00)00189-7
Capitani G, McCarthy DL, Gut H, Grütter MG, Kirsch JF (2002) Apple 1-aminocyclopropane-1-carboxylate synthase in complex with the inhibitor l-aminoethoxyvinylglycine: evidence for a ketimine intermediate. J Biol Chem 277(51):49735–49742. https://doi.org/10.1074/jbc.M208427200
Capitani G, Tschopp M, Eliot AC, Kirsch JF, Grütter MG (2005) Structure of ACC synthase inactivated by the mechanism-based inhibitor l-vinylglycine. FEBS Lett 579(11):2458–2462. https://doi.org/10.1016/j.febslet.2005.03.048
Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker JR (1997) Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89(7):1133–1144. https://doi.org/10.1016/S0092-8674(00)80300-1
Chen Y-F, Etheridge N, Schaller GE (2005) Ethylene signal transduction. Ann Bot 95(6):901–915. https://doi.org/10.1093/aob/mci100
Cheng Y, Dong Y, Yan H, Ge W, Shen C, Guan J, Liu L, Zhang Y (2012) Effects of 1-MCP on chlorophyll degradation pathway-associated genes expression and chloroplast ultrastructure during the peel yellowing of Chinese pear fruits in storage. Food Chem 135(2):415–422. https://doi.org/10.1016/j.foodchem.2012.05.017
Christians MJ, Gingerich DJ, Hansen M, Binder BM, Kieber JJ, Vierstra RD (2009) The BTB ubiquitin ligases ETO1, EOL1 and EOL2 act collectively to regulate ethylene biosynthesis in Arabidopsis by controlling type-2 ACC synthase levels. Plant J 57:332–345
Ekman JH, Clayton M, Biasi WV, Mitcham EJ (2004) Interactions between 1-MCP concentration, treatment interval and storage time for ‘Bartlett’ pears. Postharvest Biol Technol 31(2):127–136. https://doi.org/10.1016/j.postharvbio.2003.07.002
Fan S-T, Yeh D-M, Wang T-T (2009) Cultivar sensitivity to ethylene during storage and 1-methylcyclopropene protection of Aglaonema. HortScience 44(1):202–205
Fanourakis D, Carvalho SMP, Almeida DPF, van Kooten O, van Doorn WG, Heuvelink E (2012) Postharvest water relations in cut rose cultivars with contrasting sensitivity to high relative air humidity during growth. Postharvest Biol Technol 64(1):64–73. https://doi.org/10.1016/j.postharvbio.2011.09.016
Fanourakis D, Pieruschka R, Savvides A, Macnish AJ, Sarlikioti V, Woltering EJ (2013) Sources of vase life variation in cut roses: a review. Postharvest Biol Technol 78:1–15. https://doi.org/10.1016/j.postharvbio.2012.12.001
Fanourakis D, Velez-Ramirez A, In B-C, Barendse H, Meeteren U, Woltering E (2015) A survey of preharvest conditions affecting the regulation of water loss during vase life. Acta Hortic 1064:195–204. https://doi.org/10.17660/actahortic.2015.1064.22
Fanourakis D, Bouranis D, Giday H, Carvalho DRA, Rezaei Nejad A, Ottosen C-O (2016) Improving stomatal functioning at elevated growth air humidity: a review. J Plant Physiol 207:51–60. https://doi.org/10.1016/j.jplph.2016.10.003
Forney CF, Song J, Fan L, Hildebrand PD, Jordan MA (2003) Ozone and 1-methylcyclopropene alter the postharvest quality of broccoli. J Am Soc Hortic Sci 128(3):403–408
Hahn A, Harter K (2009) Mitogen-activated protein kinase cascades and ethylene: signaling, biosynthesis, or both? Plant Physiol 149:1207–1210
Hua J, Meyerowitz EM (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94(2):261–271. https://doi.org/10.1016/S0092-8674(00)81425-7
Huai Q, Xia Y, Chen Y, Callahan B, Li N, Ke H (2001) Crystal structures of ACC synthase in complex with AVG and PLP provide new insight into catalytic mechanism. J Biol Chem 276(41):38210–38216. https://doi.org/10.1074/jbc.m103840200
In B-C, Lim JH (2018) Potential vase life of cut roses: seasonal variation and relationships with growth conditions, phenotypes, and gene expressions. Postharvest Biol Technol 135:93–103. https://doi.org/10.1016/j.postharvbio.2017.09.006
In B-C, Binder BM, Falbel TG, Patterson SE (2013) Analysis of gene expression during the transition to climacteric phase in carnation flowers (Dianthus caryophyllus L.). J Exp Bot 64(16):4923–4937. https://doi.org/10.1093/jxb/ert281
In B-C, Binder BM, Falbel TG, Patterson SE (2016) Recovery of ethylene sensitivity and responses in carnation petals post-treatment with 1-methylcyclopropene. Postharvest Biol Technol 121:78–86. https://doi.org/10.1016/j.postharvbio.2016.07.010
In BC, Ha STT, Lee YS, Lim JH (2017) Relationships between the longevity, water relations, ethylene sensitivity, and gene expression of cut roses. Postharvest Biol Technol 131:74–83. https://doi.org/10.1016/j.postharvbio.2017.05.003
Jones ML (2003) Ethylene biosynthetic genes are differentially regulated by ethylene and ACC in carnation styles. Plant Growth Regul 40(2):129–138. https://doi.org/10.1023/a:1024241006254
Kevany BM, Tieman DM, Taylor MG, Cin VD, Klee HJ (2007) Ethylene receptor degradation controls the timing of ripening in tomato fruit. Plant J 51(3):458–467. https://doi.org/10.1111/j.1365-313X.2007.03170.x
Konze JR, Kwiatkowski GMK (1981) Rapidly induced ethylene formation after wounding is controlled by the regulation of 1-aminocyclopropane-1-carboxylic acid synthesis. Planta 151(4):327–330. https://doi.org/10.1007/bf00393286
Ku VVV, Wills RBH (1999) Effect of 1-methylcyclopropene on the storage life of broccoli. Postharvest Biol Technol 17(2):127–132. https://doi.org/10.1016/S0925-5214(99)00042-3
Ma N, Tan H, Xue JH, Li YQ, Gao JP (2006) Transcriptional regulation of ethylene receptor and CTR genes involved in ethylene-induced flower opening in cut rose (Rosa hybrida) cv, Samantha. J Exp Bot 57(11):2763–2773. https://doi.org/10.1093/jxb/erl033
Macnish AJ, Simons DH, Joyce DC, Faragher JD, Hofman PJ (2000) Responses of native Australian cut flowers to treatment with 1-methylcyclopropene and ethylene. HortScience 35(2):254–255
Macnish AJ, Leonard RT, Borda AM, Nell TA (2010) Genotypic variation in the postharvest performance and ethylene sensitivity of cut rose flowers. HortScience 45(5):790–796
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51(345):659–668. https://doi.org/10.1093/jexbot/51.345.659
Mir NA, Curell E, Khan N, Whitaker M, Beaudry RM (2001) Harvest maturity, storage temperature, and 1-MCP application frequency alter firmness retention and chlorophyll fluorescence of ‘Redchief Delicious’ apples. J Am Soc Hortic Sci 126(5):618–624
Muñoz-Robredo P, Rubio P, Infante R, Campos-Vargas R, Manríquez D, González-Agüero M, Defilippi BG (2012) Ethylene biosynthesis in apricot: identification of a ripening-related 1-aminocyclopropane-1-carboxylic acid synthase (ACS) gene. Postharvest Biol Technol 63(1):85–90. https://doi.org/10.1016/j.postharvbio.2011.09.001
Nilsson T (2005) Effects of ethylene and 1-MCP on ripening and senescence of European seedless cucumbers. Postharvest Biol Technol 36(2):113–125. https://doi.org/10.1016/j.postharvbio.2004.11.008
O’Malley RC, Rodriguez FI, Esch JJ, Binder BM, O’Donnell P, Klee HJ, Bleecker AB (2005) Ethylene-binding activity, gene expression levels, and receptor system output for ethylene receptor family members from Arabidopsis and tomato. Plant J 41(5):651–659. https://doi.org/10.1111/j.1365-313X.2004.02331.x
Pech JC (2002) Ethylene: agricultural sources and applications: Muhammad Arshad, William T. Frankenberger, Jr.; Kluwer Academic Publishers, November 2001, hardbound, ISBN 0-306-46666-X, EUR 158/USD 1450/GBP 9800. Plant Sci. https://doi.org/10.1016/s0168-9452(02)00061-4
Philosoph-Hadas S, Golan O, Rosenberger I, Salim S, Kochanek B, Meir S (2005) Efficiency of 1-MCP in neutralizing ethylene effects in cut flowers and potted plants following simultaneous or sequential application. In: International Society for Horticultural Science (ISHS), Leuven, Belgium, pp 321–328. https://doi.org/10.17660/actahortic.2005.669.42
Qiao H, Shen Z, Huang SC, Schmitz RJ, Urich MA, Briggs SP, Ecker JR (2012) Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas. Science 338(6105):390–393. https://doi.org/10.1126/science.1225974
Reid MS, Wu MJ (1992) Ethylene and flower senescence. Plant Growth Regul 11(1):37–43. https://doi.org/10.1007/Bf00024431
Reid MS, Evans RY, Dodge LL, Mor Y (1989) Ethylene and silver thiosulfate influence opening of cut rose flowers. J Am Soc Hortic Sci 114(3):436–440
Serek M, Sisler EC, Reid MS (1995) Effects of 1-MCP on the vase life and ethylene response of cut flowers. Plant Growth Regul 16(1):93–97. https://doi.org/10.1007/bf00040512
Serek M, Woltering EJ, Sisler EC, Frello S, Sriskandarajah S (2006) Controlling ethylene responses in flowers at the receptor level. Biotechnol Adv 24(4):368–381. https://doi.org/10.1016/j.biotechadv.2006.01.007
Shibuya K, Yoshioka T, Hashiba T, Satoh S (2000) Role of the gynoecium in natural senescence of carnation (Dianthus caryophyllus L.) flowers. J Exp Bot 51(353):2067–2073. https://doi.org/10.1093/jexbot/51.353.2067
Shibuya K, Nagata M, Tanikawa N, Yoshioka T, Hashiba T, Satoh S (2002) Comparison of mRNA levels of three ethylene receptors in senescing flowers of carnation (Dianthus caryophyllus L.). J Exp Bot 53(368):399–406. https://doi.org/10.1093/jexbot/53.368.399
Shimizu-Yumoto H, Ichimura K (2010) Combination pulse treatment of 1-naphthaleneacetic acid and aminoethoxyvinylglycine greatly improves postharvest life in cut Eustoma flowers. Postharvest Biol Technol 56(1):104–107. https://doi.org/10.1016/j.postharvbio.2009.10.001
Sisler EC, Reid MS, Yang SF (1986) Effect of antagonists of ethylene action on binding of ethylene in cut carnations. Plant Growth Regul 4(3):213–218. https://doi.org/10.1007/bf00028164
Tatsuki M, Endo A, Ohkawa H (2007) Influence of time from harvest to 1-MCP treatment on apple fruit quality and expression of genes for ethylene biosynthesis enzymes and ethylene receptors. Postharvest Biol Technol 43(1):28–35. https://doi.org/10.1016/j.postharvbio.2006.08.010
Tieman DM, 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(10):5663–5668. https://doi.org/10.1073/pnas.090550597
VBN (2014) Evaluation cards for rosa. FloraHolland, Aalsmeer
Verlinden S, Boatright J, Woodson WR (2002) Changes in ethylene responsiveness of senescence-related genes during carnation flower development. Physiol Plantarum 116(4):503–511. https://doi.org/10.1034/j.1399-3054.2002.1160409.x
Wang KLC, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14(Suppl):s131–s151. https://doi.org/10.1105/tpc.001768
Watkins C (2006) The use of 1-methlcyclopropene (1-MCP) on fruits and vegetables. Biotechnol Adv 24:389–409. https://doi.org/10.1016/j.biotechadv.2006.01.005
Xie X, Einhorn T, Wang Y (2015) Inhibition of ethylene biosynthesis and associated gene expression by aminoethoxyvinylglycine and 1-methylcyclopropene and their consequences on eating quality and internal browning of ‘Starkrimson’ pears. J Am Soc Hortic Sci 140(6):587–596
Xie X, Fang C, Wang Y (2017) Inhibition of ethylene biosynthesis and perception by 1-methylcyclopropene and its consequences on chlorophyll catabolism and storage quality of ‘Bosc’ pears. J Am Soc Hortic 142:92–100. https://doi.org/10.21273/jashs04017-16
Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35(1):155–189. https://doi.org/10.1146/annurev.pp.35.060184.001103
Yang Z, Xiaotang Song J, Song J, Campbell-Palmer Leslie, Fillmore SAE, Zhang S, Zhang Z (2012) Effect of ethylene and 1-MCP on expression of genes involved in ethylene biosynthesis and perception during ripening of apple fruit. Postharvest Biol Technol 78:55–66. https://doi.org/10.1016/j.postharvbio.2012.11.012
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(1):101–105
Yuan R, Li J (2008) Effect of Sprayable 1-MCP, AVG, and NAA on ethylene biosynthesis, preharvest fruit drop, fruit maturity, and quality of ‘Delicious’ apples. HortScience 43(5):1454–1460
Acknowledgements
This work was supported partially by a Young Researcher Grant (PJ012295) from the Rural Development Administration of Korea (RDA) and a research project grant (306016-04) from the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries (IPET).
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STT carried out the experiment, analyzed the data, and wrote the manuscript. JH performed the experiment and contributed to sample preparation. BC designed the study, contributed to the writing of the manuscript, and supervised the project.
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Ha, S.T.T., Lim, JH. & In, BC. Simultaneous Inhibition of Ethylene Biosynthesis and Binding Using AVG and 1-MCP in Two Rose Cultivars with Different Sensitivities to Ethylene. J Plant Growth Regul 39, 553–563 (2020). https://doi.org/10.1007/s00344-019-09999-6
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DOI: https://doi.org/10.1007/s00344-019-09999-6