Proteome changes in banana fruit peel tissue in response to ethylene and high-temperature treatments

Lina Du , Jun Song , Charles Forney , Leslie Campbell Palmer , Sherry Fillmore , ZhaoQi Zhang

Horticulture Research ›› 2016, Vol. 3 ›› Issue (1) : 16012

PDF (3398KB)
Horticulture Research ›› 2016, Vol. 3 ›› Issue (1) :16012 DOI: 10.1038/hortres.2016.12
ARTICLE
research-article
Proteome changes in banana fruit peel tissue in response to ethylene and high-temperature treatments
Author information +
History +
PDF (3398KB)

Abstract

Banana (Musa AAA group) is one of the most consumed fruits in the world due to its flavor and nutritional value. As a typical climacteric fruit, banana responds to ethylene treatment, which induces rapid changes of color, flavor (aroma and taste), sweetness and nutritional composition. It has also been reported that ripening bananas at temperatures above 24 °C inhibits chlorophyll breakdown and color formation but increases the rate of senescence. To gain fundamental knowledge about the effects of high temperature and ethylene on banana ripening, a quantitative proteomic study employing multiplex peptide stable isotope dimethyl labeling was conducted. In this study, green (immature) untreated banana fruit were subjected to treatment with 10 μL L−1 of ethylene for 24 h. After ethylene treatment, treated and untreated fruit were stored at 20 or 30 °C for 24 h. Fruit peel tissues were then sampled after 0 and 1 day of storage, and peel color and chlorophyll fluorescence were evaluated. Quantitative proteomic analysis was conducted on the fruit peels after 1 day of storage. In total, 413 common proteins were identified and quantified from two biological replicates. Among these proteins, 91 changed significantly in response to ethylene and high-temperature treatments. Cluster analysis on these 91 proteins identified 7 groups of changed proteins. Ethylene treatment and storage at 20 °C induced 40 proteins that are correlated with pathogen resistance, cell wall metabolism, ethylene biosynthesis, allergens and ribosomal proteins, and it repressed 36 proteins that are associated with fatty acid and lipid metabolism, redox– oxidative responses, and protein biosynthesis and modification. Ethylene treatment and storage at 30 °C induced 32 proteins, which were mainly similar to those in group 1 but also included 8 proteins in group 3 (identified as chitinase, cinnamyl alcohol dehydrogenase 1, cysteine synthase, villin-2, leucine-transfer RNA ligase, CP47 protein and calmodulin) and repressed 43 proteins in 4 groups (groups 4–7), of which 6 were associated with photosynthesis II oxygen-evolving protein, the photosynthesis I reaction center, sugar metabolism, the redox–oxidative system and fatty acid metabolism. Differences in the response to ethylene and holding temperature at 30 °C were also revealed and have been discussed. The identities and quantities of the proteins found were linked with quality changes. This study demonstrates that ethylene and high temperature influence banana fruit ripening and senescence at the proteomic level and reveals the mechanisms by which high temperature accelerates banana fruit ripening.

Cite this article

Download citation ▾
Lina Du, Jun Song, Charles Forney, Leslie Campbell Palmer, Sherry Fillmore, ZhaoQi Zhang. Proteome changes in banana fruit peel tissue in response to ethylene and high-temperature treatments. Horticulture Research, 2016, 3 (1) : 16012 DOI:10.1038/hortres.2016.12

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Seymour G. Banana. In: Seymour G, Taylor J, Tucker G (eds.). Biochemistry of fruit ripening . Netherlands: Springer, 1993: 83-106.

[2]

Seymour GB, John P, Thompson AK . Inhibition of degreening in the peel of bananas ripened at tropical temperatures. I. Effect of high temperature on changes in the pulp and peel during ripening. Ann Appl Biol 1987; 110: 153-161.

[3]

Blackbourn HD, Jeger MJ, John P, Thompson AK . Inhibition of degreening in the peel of bananas ripened at tropical temperatures. III. Changes in plastid ultrastructure and chlorophyll-protein complexes accompanying ripening in bananas and plantains. Ann Appl Biol 1990; 117: 147-161.

[4]

Yang X, Zhang Z, Joyce D, Huang X, Xu L, Pang X . Characterization of chlorophyll degradation in banana and plantain during ripening at high temperature. Food Chemistry 2009; 114: 383-390.

[5]

Plainsirichai M, Turner DW . Storage temperature during the early stage of ripening determines whether or not the peel of banana (Musa spp. AAA, Cavendish subgroup) degreens . Fruits 2010; 65: 69-74.

[6]

Matile P, Hörtensteiner S, Thomas H . Chlorophyll degradation. Annu Rev Plant Physiol Plant Mol Biol 1999; 50: 67-95.

[7]

Hörtensteiner S. Chlorophyll degradation during senescence. Ann Rev Plant Biol 2006; 57: 55-57.

[8]

Müller T, Kräutler B . Chlorophyll breakdown as seen in bananas: Sign of aging and ripening-a mini-review. Gerontology 2011; 57: 521-527.

[9]

Kusaba M, Ito H, Morita R, Iida S, Sato Y, Fujimoto M et al. Rice non-yellow coloring1 is involved in light-harvesting complex II and grana degradation during leaf senescence. Plant Cell 2007; 19: 1362-1375.

[10]

Horie Y, Ito H, Kusaba M, Tanaka R, Tanaka A . Participation of chlorophyll b reductase in the initial step of the degradation of light-harvesting chlorophyll a/b-protein complexes in Arabidopsis . J Biol Chem 2009; 284: 17449-17456.

[11]

Sato Y, Morita R, Katsuma S, Nishimura M, Tanaka A, Kusaba M . Two short-chain dehydrogenase/reductases, NON-YELLOW COLORING 1 and NYC1-LIKE, are required for chlorophyll b and light-harvesting complex II degradation during senescence in rice. Plant J 2009; 57: 120-131.

[12]

Moser S, Müller T, Holzinger A, Lütz C, Kräutler B . Structures of chlorophyll catabolites in bananas (Musa acuminata) reveal a split path of chlorophyll breakdown in a ripening fruit . Chemistry 2012; 18: 10873-10885.

[13]

Yang X, Pang X, Xu L, Fang R, Huang X, Guan P et al. Accumulation of soluble sugars in peel at high temperature leads to stay-green ripe banana fruit. J Exp Botany 2009; 60: 4051-4062.

[14]

Ogura N, Nakaya H, Takehana H . Studies on the storage temprature of tomato fruit. I. Effect of high temperature-short term storage of mature green tomato fruits on changes of their chemical composition after ripening at room temperature. J Agric Chem Soc Jpn 1975; 49: 189-196.

[15]

Cohen E . The effect of temperature and relative humidity during degreening on the colouring of Shamouti orange fruit. J Hortic Sci Biotechnol 1978; 53: 143-146.

[16]

Pang XQ, Yang XT, Zhang ZQ . Chlorophyll degradation and its control in postharvest fruits. Stewart Postharvest Rev 2008; 4: 1-4.

[17]

Golding JB, Shearer D, McGlasson WB, Wyllie SG . Relationships between respiration, ethylene, and aroma production in ripening banana. J Agric Food Chem 1999; 47: 1646-1651.

[18]

Manrique-Trujillo SM, Ramírez-López AC, Ibarra-Laclette E, Angel Gómez-Lim M . Identification of genes differentially expressed during ripening of banana. J Plant Physiol 2007; 164: 1037-1050.

[19]

Drury R, Hörtensteiner S, Donnison I, Bird CR, Seymour GB . Chlorophyll catabolism and gene expression in the peel of ripening banana fruits. Physiol Plant 1999; 107: 32-38.

[20]

Amnuaysin N, Jones ML, Seraypheap K . Changes in activities and gene expression of enzymes associated with cell wall modification in peels of hot water treated bananas. Sci Hort 2012; 142: 98-104.

[21]

Beekwilder J, Alvarez-Huerta M, Neef E, Verstappen FW, Bouwmeester HJ, Aharoni A . Functional characterization of enzymes forming volatile esters from strawberry and banana. Plant Physiol 2004; 135: 1865-1878.

[22]

Jayanty S, Song J, Rubinstein NM, Chong A, Beaudry RM . Temporal relationship between ester biosynthesis and ripening events in bananas. J Am Soc Hortic Sci 2002; 127: 998-1005.

[23]

Esteve C, D'Amato A, Marina ML, García MC, Righetti PG . In-depth proteomic analysis of banana (Musa spp.) fruit with combinatorial peptide ligand libraries . Electrophoresis 2013; 34: 207-214.

[24]

Toledo TT, Nogueira SB, Cordenunsi BR, Gozzo FC, Pilau EJ, Lajolo FM et al. Proteomic analysis of banana fruit reveals proteins that are differentially accumulated during ripening. Postharvest Biology and Technology 2012; 70: 51-58.

[25]

Palacin A, Quirce S, Sanchez-Monge R, Bobolea I, Diaz-Perales A, Martin-Muñoz F et al. Sensitization profiles to purified plant food allergens among pediatric patients with allergy to banana. Pediatr Allergy Immunol 2011; 22: 186-195.

[26]

Yang X, Song J, Fillmore S, Pang X, Zhang Z . Effect of high temperature on color, chlorophyll fluorescence and volatile biosynthesis in green-ripe banana fruit. Postharvest Biol Technol 2011; 62: 246-257.

[27]

Zheng Q, Song J, Doncaster K, Rowland E, Byers DM . Qualitative and quantitative evaluation of protein extraction protocols for apple and strawberry fruit suitable for two-dimensional electrophoresis and mass spectrometry analysis. J Agric Food Chem 2007; 55: 1663-1673.

[28]

Hustoft HK, Reubsaet L, Greibrokk T, Lundanes E, Malerod H . Critical assessment of accelerating trypsination methods. J Pharm Biomed Anal 2011; 56: 1069-1078.

[29]

Zheng Q, Song J, Campbell-Palmer L, Thompson K, Li L, Walker B et al. A proteomic investigation of apple fruit during ripening and in response to ethylene treatment. J Proteomics 2013; 93: 276-294.

[30]

Yang X, Li L, Song J, Palmer LC, Li X, Zhang Z . Peptide prefractionation is essential for proteomic approaches employing multiple-reaction monitoring of fruit proteomic research. J Sep Sci 2014; 37: 77-84.

[31]

Boersema PJ, Raijmakers R, Lemeer S, Mohammed S, Heck AJR . Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat Protoc 2009; 4: 484-494.

[32]

Li L, Song J, Kalt W, Forney C, Tsao R, Pinto D et al. Quantitative proteomic investigation employing stable isotope labeling by peptide dimethylation on proteins of strawberry fruit at different ripening stages. J Proteomics 2013; 94: 219-239.

[33]

Wright H, DeLong J, Harrison PA, Gunawardena A H L A N, Prange RK . The effect of temperature and other factors on chlorophyll a fluorescence and the lower oxygen limit in apples (Malus domestica) . Postharvest Biol Technol 2010; 55: 21-28.

[34]

Clendennen SK, May GD . Differential gene expression in ripening banana fruit. Plant Physiol 1997; 115: 463-469.

[35]

Bricker TM, Frankel LK . The structure and function of CP47 and CP43 in Photosystem II. Photosynth Res 2002; 72: 131-146.

[36]

Shah PK, Perez-Iratxeta C, Bork P, Andrade MA . Information extraction from full text scientific articles: Where are the keywords? BMC Bioinformatics 2003; 4: 20.

[37]

Owiti J, Grossmann J, Gehrig P, Dessimoz C, Laloi C, Hansen MB et al. ITRAQ-based analysis of changes in the cassava root proteome reveals pathways associated with post-harvest physiological deterioration. Plant J 2011; 67: 145-156.

[38]

Ohkama-Ohtsu N, Oikawa A, Zhao P, Xiang C, Saito K, Oliver DJ . A γ-glutamyl transpeptidase-independent pathway of glutathione catabolism to glutamate via 5-oxoproline in Arabidopsis . Plant Physiol 2008; 148: 1603-1613.

[39]

Schiller D, Contreras C, Vogt J, Dunemann F, Defilippi BG, Beaudry R et al. A dual positional specific lipoxygenase functions in the generation of flavor compounds during climacteric ripening of apple. Hort Res 2015; 2: 1-13.

[40]

Vogt J, Schiller D, Ulrich D, Schwab W, Dunemann F . Identification of lipoxygenase (LOX) genes putatively involved in fruit flavour formation in apple (Malus × domestica) . Tree Genet Genomes 2013; 9: 1493-1511.

[41]

Chen G, Hackett R, Walker D, Taylor A, Lin Z, Grierson D . Identification of a specific isoform of tomato lipoxygenase (TomloxC) involved in the generation of fatty acid-derived flavor compounds. Plant Physiol 2004; 136: 2641-2651.

[42]

Han M, Zhang T, Zhao C, Zhi J . Regulation of the expression of lipoxygenase genes in Prunus persica fruit ripening . Acta Physiol Plant 2011; 33: 1345-1352.

[43]

Snedden WA, Fromm H . Calmodulin as a versatile calcium signal transducer in plants. New Phytol 2001; 151: 35-66.

[44]

Zhang W, Zhou RG, Gao YJ, Zheng SZ, Xu P, Zhang SQ et al. Molecular and genetic evidence for the key role of AtCaM3 in heat-shock signal transduction in Arabidopsis . Plant Physiol 2009; 149: 1773-1784.

[45]

Yang T, Peng H, Whitaker BD, Jurick WM . Differential expression of calcium/calmodulin-regulated SlSRs in response to abiotic and biotic stresses in tomato fruit. Physiol Plant 2013; 148: 445-455.

[46]

Romero LC, Aroca , Laureano-Marín AM, Moreno I, García I, Gotor C . Cysteine and cysteine-related signaling pathways in arabidopsis thaliana . Mol Plant 2014; 7: 264-276.

[47]

Gotor C, Laureano-Marín AM, Moreno I, Aroca Á, García I, Romero LC . Signaling in the plant cytosol: Cysteine or sulfide? Amino Acids 2014; 47: 2155-2164.

[48]

Turowski VR, Busi MV, Gomez-Casati DF . Structural and functional studies of the mitochondrial cysteine desulfurase from arabidopsis thaliana . Mol Plant 2012; 5: 1001-1010.

[49]

Kumar S, Kaur A, Chattopadhyay B, Bachhawat AK . Defining the cytosolic pathway of glutathione degradation in Arabidopsis thaliana: Role of the ChaC/GCG family of γ-glutamyl cyclotransferases as glutathione-degrading enzymes and AtLAP1 as the Cys-Gly peptidase . Biochem J 2015; 468: 73-85.

[50]

Biron DG, Brun C, Lefevre T, Lebarbenchon C, Loxdale HD, Chevenet F et al. The pitfalls of proteomics experiments without the correct use of bioinformatics tools. Proteomics 2006; 6: 5577-5596.

PDF (3398KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/