Abstract
Understanding the fruit ripening mechanism is critical for fruit quality improvement. Although postharvest ethylene application is known to enhance the onset of fruit ripening, the exact mechanisms remain unclear. In this study, a gel-based proteomic analysis was performed to investigate the changes in protein profiles during the ripening of exogenous-ethylene-treated kiwifruit (Actinidia deliciosa) cultivars ‘Hayward’ and ‘Garmrok’. Based on comparative two-dimensional gel electrophoresis, most of the proteins were aggregated in exogenous-ethylene-treated kiwifruit compared to the untreated kiwifruit. Consequently, 90 and 106 proteins were differentially expressed in ‘Hayward’ and ‘Garmrok’ kiwifruit, respectively. Among the successfully identified proteins by matrix-assisted laser desorption/ionization tandem time-of-flight mass spectrometry, the 50% in ‘Hayward’ kiwifruit and 60% in ‘Garmrok’ kiwifruit were associated with ripening. Also, 18% and 10% of proteins were associated with defense response in ‘Hayward’ and ‘Garmrok’ kiwifruit, respectively. The other major proteins were related to protein biosynthesis and photosynthesis/Calvin cycle during kiwifruit ripening. We used bioinformatics analysis to determine the interactions between identified proteins, and this proteomic approach provided insights into biological pathways and molecular functions in postharvest ripening of exogenous-ethylene-treated kiwifruit.
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Aharoni A, O’Connell AP (2002) Gene expression analysis of strawberry achene and receptacle maturation using DNA microarrays. J Exp Bot 53:2073–2087. https://doi.org/10.1093/jxb/erf026
Ainalidou A, Tanou G, Belghazi M, Samiotaki M, Diamantidis G, Molassiotis A, Karamanoli K (2016) Integrated analysis of metabolites and proteins reveal aspects of the tissue-specific function of synthetic cytokinin in kiwifruit development and ripening. J Proteom 143:318–333. https://doi.org/10.1016/j.jprot.2016.02.013
Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot 53:2039–2055. https://doi.org/10.1093/jxb/erf072
Andrade JDM, Toledo TT, Nogueira SB, Cordenunsi BR, Lajolo FM, do Nascimento JRO (2012) 2D-DIGE analysis of mango (Mangifera indica L.) fruit reveals major proteomic changes associated with ripening. J Proteom 75:3331–3341. https://doi.org/10.1016/j.jprot.2012.03.047
Antunes M (2007) The role of ethylene in kiwifruit ripening and senescence. Stewart Postharvest Rev 3:1–8. https://doi.org/10.2212/spr.2007.2.9
Bianco L, Lopez L, Scalone AG, Di Carli M, Desiderio A, Benvenuto E, Perrotta G (2009) Strawberry proteome characterization and its regulation during fruit ripening and in different genotypes. J Proteom 72:586–607. https://doi.org/10.1016/j.jprot.2008.11.019
Bower JH, Biasi WV, Mitcham EJ (2003) Effect of ethylene in the storage environment on quality if ‘Bartlett pears’. Postharvest Biol Technol 28:371–379. https://doi.org/10.1016/S0925-5214(02),00210-7
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. https://doi.org/10.1016/0003-2697(76),90527-3
Costa F, Alba R, Schouten H, Soglio V, Gianfranceschi L, Serra S, Musacchi S, Sansavini S, Costa G et al (2010) Use of homologous and heterologous gene expression profiling tools to characterize transcription dynamics during apple fruit maturation and ripening. BMC Plant Biol 10:229. https://doi.org/10.1186/1471-2229-10-229
Deytieux C, Gény L, Lapaillerie D, Claverol S, Bonneu M, Donèche B (2007) Proteome analysis of grape skins during ripening. J Exp Bot 58:1851–1862. https://doi.org/10.1093/jxb/erm049
Faurobert M, Mihr C, Bertin N, Pawlowski T, Negroni L, Sommerer N, Causse M (2007) Major proteome variations associated with cherry tomato pericarp development and ripening. Plant Physiol 143:1327–1346. https://doi.org/10.1104/pp.106.092817
Fujisawa M, Shima Y, Nakagawa H, Kitagawa M, Kimbara J, Nakano T, Kasumi T, Ito Y (2014) Transcriptional regulation of fruit ripening by tomato FRUITFULL homologs and associated MADS box proteins. Plant Cell 26:89–101. https://doi.org/10.1105/tpc.113.119453
Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell 16:170–180. https://doi.org/10.1105/tpc.019158
Giribaldi M, Perugini I, Sauvage FX, Schubert A (2007) Analysis of protein changes during grape berry ripening by 2-DE and MALDI-TOF. Proteomics 7:3154–3170. https://doi.org/10.1002/pmic.200600974
Gorovits R, Akad F, Beery H, Vidavsky F, Mahadav A, Czosnek H (2007) Expression of stress-response proteins upon whitefly-mediated inoculation of Tomato yellow leaf curl virus in susceptible and resistant tomato plants. Mol Plant Microbe Interact 20:1376–1383. https://doi.org/10.1094/MPMI-20-11-1376
Huerta-Ocampo JÁ, Osuna-Castro JA, Lino-López GJ, Barrera-Pacheco A, Mendoza-Hernández G, De León-Rodríguez A, de la Rosa APB (2012) Proteomic analysis of differentially accumulated proteins during ripening and in response to 1-MCP in papaya fruit. J Proteom 75:2160–2169. https://doi.org/10.1016/j.jprot.2012.01.015
Ilina N, Alem HJ, Pagano EA, Sozzi GO (2010) Suppression of ethylene perception after exposure to cooling conditions delays the progress of softening in ‘Hayward’ kiwifruit. Postharvest Biol Technol 55:160–168. https://doi.org/10.1016/j.postharvbio.2009.11.005
Jabbar A, East AR (2016) Quantifying the ethylene induced softening and low temperature breakdown of ‘Hayward’ Kiwifruit. Postharvest Biol Technol 113:87–94. https://doi.org/10.1016/j.postharvbio.2015.11.002
Janssen B, Thodey K, Schaffer R, Alba R, Balakrishnan L, Bishop R, Bowen JH, Crowhurst RN, Gleave AP et al (2008) Global gene expression analysis of apple fruit development from the floral bud to ripe fruit. BMC Plant Biol 8:16. https://doi.org/10.1186/1471-2229-8-16
Jimenez A, Creissen G, Kular B, Firmin J, Robinson S, Verhoeyen M, Mullineaux P (2002) Changes in oxidative processes and components of the antioxidant system during tomato fruit ripening. Planta 214:751–758. https://doi.org/10.1007/s004250100667
Kwack YB, Park YS (2007) Kiwifruit. In: Lee JM, Choi GW, Janick J (eds) Horticulture in Korea. Korean Society for Horticulture Science, Suwon, pp 244–249
Kwack YB, Kim HL, Lee JH, Chung KH, Chae WB (2017) ‘Goldone’, a yellow-fleshed kiwifruit cultivar with large fruit size. Hortic Sci Technol 35:142–146. https://doi.org/10.12972/kjhst.20170015
Lee JJ, Park KW, Kwak YS, Ahn JY, Jung YH, Lee BH, Jeong JC, Lee HS, Kwak SS (2012) Comparative proteomic study between tuberous roots of light orange- and purple-fleshed sweet potato cultivars. Plant Sci 193:120–129. https://doi.org/10.1016/j.plantsci.2012.06.003
Li T, Yun Z, Zhang D, Yang C, Zhu H, Jiang Y, Duan X (2015a) Proteomic analysis of differentially expressed proteins involved in ethylene-induced chilling tolerance in harvested banana fruit. Front Plant Sci 6:845. https://doi.org/10.3389/fpls.2015.00845
Li X, Yang B, Wang J, Dong B, Li H, Gong D, Zhao Y, Tang Y, Yu X, Qi Shang (2015b) BTH treatment caused physiological, biochemical and proteomic changes of muskmelon (Cucumis melo L.) fruit during ripening. J Proteom 120:179–193. https://doi.org/10.1016/j.jprot.2015.03.006
Li M, Li D, Feng F, Zhang S, Ma F, Cheng L (2016) Proteomic analysis reveals dynamic regulation of fruit development and sugar and acid accumulation in apple. J Exp Bot 67:5145–5157. https://doi.org/10.1093/jxb/erw277
Lim S, Lee JG, Lee EJ (2017) Comparison of fruit quality and GC-MS-based metabolite profiling of Kiwifruit ‘Jecy green’: natural and exogenous ethylene-induced ripening. Food Chem 234:81–92. https://doi.org/10.1016/j.foodchem.2017.04.163
Lin M, Fang J, Qi X, Li Y, Chen J, Sun L, Zhong Y (2017) iTRAQ-based quantitative proteomic analysis reveals alterations in the metabolism of Actinidia arguta. J Sci Rep 7:1–11. https://doi.org/10.1038/s41598-017-06074-6
Liu J, Sui Y, Chen H, Liu Y, Liu Y (2018) Proteomic analysis of kiwifruit in response to the postharvest pathogen, Botrytis cinerea. Front Plant Sci 9:1–18. https://doi.org/10.3389/fpls.2018.00158
Marondedze C, Gehring C, Thomas L (2014) Dynamic changes in the date palm fruit proteome during development and ripening. Hortic Res 1:14039. https://doi.org/10.1038/hortres.2014.39
Martinez-Esteso MJ, Vilella-Anton MT, Pedreno MA, Valero ML, Bru-Martinez R (2013) iTRAQ-based protein profiling provides insights into the central metabolism changes driving grape berry development and ripening. BMC Plant Biol 13:167–170. https://doi.org/10.1186/1471-2229-13-167
Minas IS, Tanou G, Belghazi M, Job D, Manganaris GA, Molassiotis A, Vasilakakis M (2012) Physiological and proteomic approaches to address the active role of ozone in kiwifruit postharvest ripening. J Exp Bot 63:2449–2464. https://doi.org/10.1093/jxb/err418
Minas IS, Tanou G, Karagiannis E, Belghazi M, Molassiotis A (2016) Coupling of physiological and proteomic analysis to understand the ethylene- and chilling-induced Kiwifruit ripening syndrome. Front Plant Sci 7:120. https://doi.org/10.3389/fpls.2016.00120
Moyle R, Fairbairn DJ, Ripi J, Crowe M, Botella JR (2005) Developing pineapple fruit has a small transcriptome dominated by metallothionein. J Exp Bot 56:101–112. https://doi.org/10.1093/jxb/eri015
Muccilli V, Licciardello C, Fontanini D, Russo MP, Cunsolo V, Saletti R, Reforgiato Recupero G, Foti S (2009) Proteome analysis of Citrus sinensis L. (Osbeck) flesh at ripening time. J Proteom 73:134–152. https://doi.org/10.1016/j.jprot.2009.09.005
Muneer S, Park YG, Manivannan A, Soundararajan P, Jeong BR (2014) Physiological and proteomic analysis in chloroplasts of Solanum lycopersicum L. under silicon efficiency and salinity stress. Int J Mol Sci 15:21803–21824. https://doi.org/10.3390/ijms151221803
Muneer S, Ko CH, Wei H, Chen Y, Jeong BR (2016) Physiological and proteomic investigations to study the response of tomato graft unions under temperature stress. PLoS ONE 11:e0157439. https://doi.org/10.1371/journal.pone.0157439
Negri AS, Prinsi B, Rossoni M, Failla O, Scienza A, Cocucci M, Espen L (2008) Proteome changes in the skin of the grape cultivar Barbera among different stages of ripening. BMC Genom 9:378. https://doi.org/10.1186/1471-2164-9-378
Nieuwenhuizen J, Beuning NL, Sutherland PW, Sharma NN, Cooney JM, Bieleski LRF, Schroeder R, Macrae EA, Atkinson RG (2007) Identification and characterization of acidic and novel basic forms of actinidin, the highly abundant cysteine protease from kiwifruit. Funct Plant Biol 34:946–961. https://doi.org/10.1071/FP07121
Nilo R, Saffie C, Lilley K, Baeza-Yates R, Cambiazo V, Campos-Vargas R, González M, Meisel LA, Retamales J et al (2010) Proteomic analysis of peach fruit mesocarp softening and chilling injury using difference gel electrophoresis (DIGE). BMC Genom 11:43. https://doi.org/10.1186/1471-2164-11-43
Nogueira SB, Labate CA, Gozzo FC, Pilau EJ, Lajolo FM, Oliveira do Nascimento JR (2012) Proteomic analysis of papaya fruit ripening using 2DE-DIGE. J Proteom 75:1428–1439. https://doi.org/10.1016/j.jprot.2011.11.015
Page D, Gouble B, Valot B, Bouchet JP, Callot C, Kretzschmar A, Causse M, Renard CM, Faurobert M (2010) Protective proteins are differentially expressed in tomato genotypes differing for their tolerance to low-temperature storage. Planta 232:483–500. https://doi.org/10.1007/s00425-010-1184-z
Palma JM, Corpas FJ, del Río LA (2011) Proteomics as an approach to the understanding of the molecular physiology of fruit development and ripening. J Proteom 74:1230–1243. https://doi.org/10.1016/j.jprot.2011.04.010
Pech JC, Bouzayen M, Latché A (2008) Climacteric fruit ripening: ethylene-dependent and independent regulation of ripening pathways in melon fruit. Plant Sci 175:114–120. https://doi.org/10.1016/j.plantsci.2008.01.003
Petriccione M, Cecco ID, Arena S, Scaloni A, Scortichini M (2013) Proteomic changes in Actinidia chinensis shoot during systemic infection with a pandemic Pseudomonas syringae pv. actinidiae strain. J Proteom 78:461–476. https://doi.org/10.1016/j.jprot.2012.10.014
Petriccione M, Salzano AM, Cecco ID, Scaloni A, Scortichini M (2014) Proteomic analysis of the Actinidia deliciosa leaf apoplast during biotrophic colonization by Pseudomonas syringae pv. Actinidiae. J Proteomics 101:43–62. https://doi.org/10.1016/j.jprot.2014.01.030
Sapitnitskaya M, Maul P, McCollum GT, Guy CL, Weiss B, Samach A, Porat R (2006) Postharvest heat and conditioning treatments activate different molecular responses and reduce chilling injuries in grapefruit. J Exp Bot 57:2943–2953. https://doi.org/10.1093/jxb/erl055
Shi Y, Jiang L, Zhang L, Kang R, Yu Z (2014) Dynamic changes in proteins during apple (Malus × domestica) fruit ripening and storage. Hortic Res 1:6. https://doi.org/10.1038/hortres.2014.6
Shin MH (2018) Fruit ripening characteristics of kiwifruit by exogenous ethylene treatment and storage temperature. Ph.D. thesis, Division of Applied Life Science Graduate School, Gyeonsang National University, Jinju 52828, Korea
Shin MH, Kwack YB, Kim YH, Kim JG (2019) Fruit ripening and related gene expression in ‘Goldone’ and ‘Jecy Gold’ kiwifruit by exogenous ethylene application. Hortic Sci Technol 37:54–64. https://doi.org/10.12972/kjhst.20190006
Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, Minguez P, Doerks T, Stark M, Muller J (2011) The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 39:561–568. https://doi.org/10.1093/nar/gkq973
Tanou G, Minas IS, Karagiannis E, Tsikou D, Audebert S, Papadopoulou KK, Molassiotis A (2015) The impact of sodium nitroprusside and ozone in kiwifruit ripening physiology: a combined gene and protein expression profiling approach. Ann Bot 116:649–662. https://doi.org/10.1093/aob/mcv107
Terrier N, Sauvage FX, Ageorges A, Romieu C (2001) Changes in acidity and in proton transport at the tonoplast of grape berries during development. Planta 213:20–28. https://doi.org/10.1007/s004250000472
Yin XR, Chen KS, Allan AC, Wu RM, Zhang B, Lallu N, Ferguson IB (2008) Ethylene-induced modulation of genes associated with the ethylene signaling pathway in ripening kiwifruit. J Exp Bot 59:2097–2108. https://doi.org/10.1093/jxb/ern067
Acknowledgements
This work was carried out with the support of the “Cooperative Research Program for Agriculture Science and Technology Development (Project No. PJ010904032017)”, Rural Development Administration, Republic of Korea. Further, we are grateful to Prof. Gon-Sup Kim (Department of Veterinary Science, Gyeongsang National University, Republic of Korea) and his laboratory members for sharing the ‘Progenesis’ software. We also thank to Mr. Joon Ha, Department of Applied Biology, IALS, Gyeongsang National University, Republic of Korea for his technical assistance.
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SMH and MS performed the experiments and analyzed the data. BDW assisted with proteomic measurements and KHMPC helped carry out the results. KJG designed and wrote the manuscript in consultation with KYH and LJJ. KYB helped supervise the experiment. All authors discussed the results and contributed to the final manuscript.
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Shin, M.H., Muneer, S., Kim, YH. et al. Proteomic analysis reveals dynamic regulation of fruit ripening in response to exogenous ethylene in kiwifruit cultivars. Hortic. Environ. Biotechnol. 61, 93–114 (2020). https://doi.org/10.1007/s13580-019-00209-6
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DOI: https://doi.org/10.1007/s13580-019-00209-6