Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Proteomic analysis during capsicum ripening reveals differential expression of ACC oxidase isoform 4 and other candidates

Wan M. Aizat A , Jason A. Able A , James C. R. Stangoulis B and Amanda J. Able A C
+ Author Affiliations
- Author Affiliations

A School of Agriculture, Food and Wine, The University of Adelaide, Waite Research Institute, Glen Osmond, SA 5064, Australia.

B School of Biological Science, Flinders University, Bedford Park, SA 5042, Australia.

C Corresponding author. Email: amanda.able@adelaide.edu.au

Functional Plant Biology 40(11) 1115-1128 https://doi.org/10.1071/FP12330
Submitted: 2 November 2012  Accepted: 14 May 2013   Published: 21 June 2013

Abstract

Capsicum (Capsicum annuum L.) is categorised as a non-climacteric fruit that exhibits limited ethylene production during ripening and the molecular mechanisms associated with this process are poorly understood. A proteomic approach was used to identify the differentially expressed proteins during various ripening stages (Green (G), Breaker Red 1 (BR1) and Light Red (LR)) and the genes associated with their synthesis. From 2D gel electrophoresis (2DGE), seven protein spots were identified as selectively present either in G or BR1 and are involved in carbon metabolism, colour and fruit development, protein synthesis and chaperones or biosynthesis of amino acids and polyamines. One candidate of interest, 1-aminocyclopropane-1-carboxylic acid (ACC) oxidase (ACO) is known to be involved in ethylene biosynthesis and was only present in BR1 and is related to the tomato ACO isoform 4 (LeACO4) and hence named CaACO4. CaACO4 RNA expression as well as total ACO protein expression in multiple stages of ripening (G, Breaker (B), BR1, Breaker Red 2 (BR2), LR and Deep Red (DR)) corresponded to the 2DGE protein spot abundance in breaker stages. Our findings highlight the involvement of the ethylene pathway in non-climacteric fruit ripening.

Additional keywords: Capsicum annuum, fruit ripening, non-climacteric ripening, pepper, proteomics, 2D gel electrophoresis.


References

Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. Journal of Experimental Botany 53, 2039–2055.
Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening.CrossRef | 1:CAS:528:DC%2BD38XnsVGks7s%3D&md5=37a209a5b57fdccb15b5fe6ad70150f1CAS | 12324528PubMed |

Angelini R, Cona A, Federico R, Fincato P, Tavladoraki P, Tisi A (2010) Plant amine oxidases ‘on the move’: an update. Plant Physiology and Biochemistry 48, 560–564.
Plant amine oxidases ‘on the move’: an update.CrossRef | 1:CAS:528:DC%2BC3cXntlCrtrc%3D&md5=8806c335fb729a6b8089f5ea4ce553adCAS | 20219383PubMed |

Balogh A, Koncz T, Tisza V, Kiss E, Heszky L (2005) The effect of 1-MCP on the expression of several ripening-related genes in strawberries. HortScience 40, 2088–2090.

Bapat VA, Trivedi PK, Ghosh A, Sane VA, Ganapathi TR, Nath P (2010) Ripening of fleshy fruit: molecular insight and the role of ethylene. Biotechnology Advances 28, 94–107.
Ripening of fleshy fruit: molecular insight and the role of ethylene.CrossRef | 1:CAS:528:DC%2BD1MXhsFGrtLrJ&md5=1c9e829450da11c40563153b56761c3fCAS | 19850118PubMed |

Barry CS, Giovannoni JJ (2007) Ethylene and fruit ripening. Journal of Plant Growth Regulation 26, 143–159.
Ethylene and fruit ripening.CrossRef | 1:CAS:528:DC%2BD2sXot1yksrk%3D&md5=cea0d726181d273ef4a278d6d723f773CAS |

Barry CS, Blume B, Bouzayen M, Cooper W, Hamilton AJ, Grierson D (1996) Differential expression of the 1-aminocyclopropane-1-carboxylate oxidase gene family of tomato. The Plant Journal 9, 525–535.
Differential expression of the 1-aminocyclopropane-1-carboxylate oxidase gene family of tomato.CrossRef | 1:CAS:528:DyaK28XivFWntLg%3D&md5=e09706004caa36e26cb0bcbbe6644437CAS | 8624515PubMed |

Barry CS, Llop-Tous MI, 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 Physiology 123, 979–986.
The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from System-1 to System-2 ethylene synthesis in tomato.CrossRef | 1:CAS:528:DC%2BD3cXlt1Sltrw%3D&md5=228ca4c7fecf932ed77d12de7f895de3CAS | 1:CAS:528:DC%2BD3cXlt1Sltrw%3D&md5=228ca4c7fecf932ed77d12de7f895de3CAS | 10889246PubMed |

Biale JB (1964) Growth maturation and senescence in fruits – recent knowledge on growth regulation and on biological oxidations has been applied to studies with fruits. Science 146, 880–888.
Growth maturation and senescence in fruits – recent knowledge on growth regulation and on biological oxidations has been applied to studies with fruits.CrossRef | 1:CAS:528:DyaF2MXhtVGnsQ%3D%3D&md5=fceec0ad0809b865b98c24ad823dd629CAS | 17777049PubMed |

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. Journal of Proteomics 72, 586–607.
Strawberry proteome characterization and its regulation during fruit ripening and in different genotypes.CrossRef | 1:CAS:528:DC%2BD1MXktlylsrg%3D&md5=8660728aa0bd0f7bb230590ae0fc44d6CAS | 19135558PubMed |

Bidonde S, Ferrer MA, Zegzouti H, Ramassamy S, Latché A, Pech J-C, Hamilton AJ, Grierson D, Bouzayen M (1998) Expression and characterization of three tomato 1-aminocyclopropane-1-carboxylate oxidase cDNAs in yeast. European Journal of Biochemistry 253, 20–26.
Expression and characterization of three tomato 1-aminocyclopropane-1-carboxylate oxidase cDNAs in yeast.CrossRef | 1:CAS:528:DyaK1cXisFGiur4%3D&md5=3e84f2e4d7d472c43504fa9a8b49ae82CAS | 1:CAS:528:DyaK1cXisFGiur4%3D&md5=3e84f2e4d7d472c43504fa9a8b49ae82CAS | 9578456PubMed |

Biles CL, Wall MM, Blackstone K (1993) Morphological and physiological changes during maturation of new Mexican type peppers. Journal of the American Society for Horticultural Science 118, 476–480.

Blume B, Barry CS, Hamilton AJ, Bouzayen M, Grierson D (1997) Identification of transposon-like elements in non-coding regions of tomato ACC oxidase genes. Molecular & General Genetics 254, 297–303.
Identification of transposon-like elements in non-coding regions of tomato ACC oxidase genes.CrossRef | 1:CAS:528:DyaK2sXjsFOjs7w%3D&md5=d28bd1d728b028946d4290ca5ad59c32CAS | 1:CAS:528:DyaK2sXjsFOjs7w%3D&md5=d28bd1d728b028946d4290ca5ad59c32CAS |

Bradford MM (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for quantification of microgram quantities of protein utilizing principle of protein-dye binding.CrossRef | 1:CAS:528:DyaE28XksVehtrY%3D&md5=bead43c1adb6f57157bea3eab849e63cCAS | 1:CAS:528:DyaE28XksVehtrY%3D&md5=bead43c1adb6f57157bea3eab849e63cCAS | 942051PubMed |

Bulens I, Van de Poel B, Hertog M, De Proft MP, Geeraerd AH, Nicolaï BM (2011) Protocol: an updated integrated methodology for analysis of metabolites and enzyme activities of ethylene biosynthesis. Plant Methods 7, 17
Protocol: an updated integrated methodology for analysis of metabolites and enzyme activities of ethylene biosynthesis.CrossRef | 1:CAS:528:DC%2BC3MXpt1Grtr4%3D&md5=60ed965afc579afe684008d96f13e6b2CAS | 1:CAS:528:DC%2BC3MXpt1Grtr4%3D&md5=60ed965afc579afe684008d96f13e6b2CAS | 21696643PubMed |

Cara B, Giovannoni JJ (2008) Molecular biology of ethylene during tomato fruit development and maturation. Plant Science 175, 106–113.
Molecular biology of ethylene during tomato fruit development and maturation.CrossRef | 1:CAS:528:DC%2BD1cXmvFegu70%3D&md5=30f9b85c7cbda45b1aada99be5df77b6CAS |

Carrari F, Baxter C, Usadel B, Urbanczyk-Wochniak E, Zanor M-I, Nunes-Nesi A, Nikiforova V, Centero D, Ratzka A, Pauly M, Sweetlove LJ, Fernie AR (2006) Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior. Plant Physiology 142, 1380–1396.
Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior.CrossRef | 1:CAS:528:DC%2BD28XhtlCns7rP&md5=57a7e31dbbd9eb24eb28fcc7a396b234CAS | 1:CAS:528:DC%2BD28XhtlCns7rP&md5=57a7e31dbbd9eb24eb28fcc7a396b234CAS | 17071647PubMed |

Cazzonelli CI, Cavallaro AS, Botella JR (1998) Cloning and characterisation of ripening-induced ethylene biosynthetic genes from non-climacteric pineapple (Ananas comosus) fruits. Australian Journal of Plant Physiology 25, 513–518.
Cloning and characterisation of ripening-induced ethylene biosynthetic genes from non-climacteric pineapple (Ananas comosus) fruits.CrossRef | 1:CAS:528:DyaK1cXls1Kru7o%3D&md5=ea5944d1693c7ec560d9ee9ebb7d01e4CAS |

Chang S-C, Lin P-C, Chen H-M, Wu J-S, Juang R-H (2000) The isolation and characterization of Chaperonin 60 from sweet potato roots – involvement of the chaperonins in starch biosynthesis. Botanical Bulletin of Academia Sinica 41, 105–111.

Chervin C, El-Kereamy A, Roustan JP, Latché A, Lamon J, Bouzayen M (2004) Ethylene seems required for the berry development and ripening in grape, a non-climacteric fruit. Plant Science 167, 1301–1305.
Ethylene seems required for the berry development and ripening in grape, a non-climacteric fruit.CrossRef | 1:CAS:528:DC%2BD2cXnslGisL4%3D&md5=20d7329de446f6c32cc75316841fef4eCAS |

Chomczynski P, Sacchi N (2006) The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nature Protocols 1, 581–585.
The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on.CrossRef | 1:CAS:528:DC%2BD28XhtFOitLjK&md5=0331eb5bb00253169149a78fbc1f4610CAS | 17406285PubMed |

Choudhury SR, Roy S, Senguptaa DN (2008) Characterization of transcriptional profiles of MA-ACS1 and MA-ACO1 genes in response to ethylene, auxin, wounding, cold and different photoperiods during ripening in banana fruit. Journal of Plant Physiology 165, 1865–1878.
Characterization of transcriptional profiles of MA-ACS1 and MA-ACO1 genes in response to ethylene, auxin, wounding, cold and different photoperiods during ripening in banana fruit.CrossRef | 1:CAS:528:DC%2BD1MXhtlCmsb4%3D&md5=13256a3efd1cb982d6d281e5852247d2CAS | 18554749PubMed |

Collazo-Siqués P, Valverde ME, Paredes-López O, Guevara-Lara F (2003) Expression of ripening-related genes in prickly pear (Opuntia sp.) fruits. Plant Foods for Human Nutrition 58, 317–326.
Expression of ripening-related genes in prickly pear (Opuntia sp.) fruits.CrossRef | 15354791PubMed |

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 Physiology 143, 1327–1346.
Major proteome variations associated with cherry tomato pericarp development and ripening.CrossRef | 1:CAS:528:DC%2BD2sXjsVyqsbo%3D&md5=5c49b4b3853d6f264e39988b8efa3839CAS | 1:CAS:528:DC%2BD2sXjsVyqsbo%3D&md5=5c49b4b3853d6f264e39988b8efa3839CAS | 17208958PubMed |

Fernández-Trujillo JP, Serrano JM, Martínez JA (2009) Quality of red sweet pepper fruit treated with 1-MCP during a simulated post-harvest handling chain. Food Science & Technology International 15, 23–30.
Quality of red sweet pepper fruit treated with 1-MCP during a simulated post-harvest handling chain.CrossRef |

Fox AJ, Del Pozo-Insfran D, Lee JH, Sargent SA, Talcott ST (2005) Ripening-induced chemical and antioxidant changes in bell peppers as affected by harvest maturity and postharvest ethylene exposure. HortScience 40, 732–736.

García-Hernández M, Davies E, Baskin TI, Staswick PE (1996) Association of plant p40 protein with ribosomes is enhanced when polyribosomes form during periods of active tissue growth. Plant Physiology 111, 559–568.

Garcia-Pineda E, Lozoya-Gloria E (1999) Induced gene expression of 1-aminocyclopropane-1-carboxylic acid (ACC oxidase) in pepper (Capsicum annuum L.) by arachidonic acid. Plant Science 145, 11–21.
Induced gene expression of 1-aminocyclopropane-1-carboxylic acid (ACC oxidase) in pepper (Capsicum annuum L.) by arachidonic acid.CrossRef | 1:CAS:528:DyaK1MXktlyhuro%3D&md5=67f8e6d65d5362f22f897cfeff00849fCAS | 1:CAS:528:DyaK1MXktlyhuro%3D&md5=67f8e6d65d5362f22f897cfeff00849fCAS |

Ghosh S, Meli VS, Kumar A, Thakur A, Chakraborty N, Chakraborty S, Datta A (2011) The N-glycan processing enzymes α-mannosidase and β-D-N-acetylhexosaminidase are involved in ripening-associated softening in the non-climacteric fruits of capsicum. Journal of Experimental Botany 62, 571–582.
The N-glycan processing enzymes α-mannosidase and β-D-N-acetylhexosaminidase are involved in ripening-associated softening in the non-climacteric fruits of capsicum.CrossRef | 1:CAS:528:DC%2BC3cXhsFyrsbzF&md5=cabe659c31a9d0809f3cc19980fe2cbdCAS | 1:CAS:528:DC%2BC3cXhsFyrsbzF&md5=cabe659c31a9d0809f3cc19980fe2cbdCAS | 21030387PubMed |

Giovannoni JJ (2007) Fruit ripening mutants yield insights into ripening control. Current Opinion in Plant Biology 10, 283–289.
Fruit ripening mutants yield insights into ripening control.CrossRef | 1:CAS:528:DC%2BD2sXlt1Sit70%3D&md5=6877159aa47b5f9bf45a2e8695bb8403CAS | 17442612PubMed |

Giribaldi M, Perugini L, Sauvage FX, Schubert A (2007) Analysis of protein changes during grape berry ripening by 2-DE and MALDI-TOF. Proteomics 7, 3154–3170.
Analysis of protein changes during grape berry ripening by 2-DE and MALDI-TOF.CrossRef | 1:CAS:528:DC%2BD2sXhtFSkt7zP&md5=d40881563534bb275d5e79d7f405c978CAS | 17683049PubMed |

Gross KC, Watada AE, Kang MS, Kim SD, Kim KS, Lee SW (1986) Biochemical changes associated with the ripening of hot pepper fruit. Physiologia Plantarum 66, 31–36.
Biochemical changes associated with the ripening of hot pepper fruit.CrossRef | 1:CAS:528:DyaL28XhtVKnsrk%3D&md5=8d8f8ead99018c39d0762c6f1a36edabCAS | 1:CAS:528:DyaL28XhtVKnsrk%3D&md5=8d8f8ead99018c39d0762c6f1a36edabCAS |

Han SE, Seo YS, Kim D, Sung SK, Kim WT (2007) Expression of MdCAS1 and MdCAS2, encoding apple β-cyanoalanine synthase homologs, is concomitantly induced during ripening and implicates MdCASs in the possible role of the cyanide detoxification in Fuji apple (Malus domestica Borkh.) fruits. Plant Cell Reports 26, 1321–1331.
Expression of MdCAS1 and MdCAS2, encoding apple β-cyanoalanine synthase homologs, is concomitantly induced during ripening and implicates MdCASs in the possible role of the cyanide detoxification in Fuji apple (Malus domestica Borkh.) fruits.CrossRef | 1:CAS:528:DC%2BD2sXotFymt78%3D&md5=89fa395991a6677ff0eb37dcb2617872CAS | 17333023PubMed |

Handa AK, Mattoo AK (2010) Differential and functional interactions emphasize the multiple roles of polyamines in plants. Plant Physiology and Biochemistry 48, 540–546.
Differential and functional interactions emphasize the multiple roles of polyamines in plants.CrossRef | 1:CAS:528:DC%2BC3cXntlCrtrg%3D&md5=379fec3e074d203fa625ce5d33d98a45CAS | 20227284PubMed | 20227284PubMed |

Hubbard NL, Pharr DM (1992) Developmental changes in carbohydrate concentration and activities of sucrose metabolizing enzymes in fruits of two Capsicum annuum L. genotypes. Plant Science 86, 33–39.
Developmental changes in carbohydrate concentration and activities of sucrose metabolizing enzymes in fruits of two Capsicum annuum L. genotypes.CrossRef | 1:CAS:528:DyaK38XmsVyltLc%3D&md5=0910391e1fe458e380c0d257192dc758CAS |

Hugueney P, Bouvier F, Badillo A, Quennemet J, d’Harlingue A, Camara B (1996) Developmental and stress regulation of gene expression for plastid and cytosolic isoprenoid pathways in pepper fruits. Plant Physiology 111, 619–626.
Developmental and stress regulation of gene expression for plastid and cytosolic isoprenoid pathways in pepper fruits.CrossRef | 1:CAS:528:DyaK28Xjs1Ghsrw%3D&md5=277e451b8840d33631cfb0cc15d52b8bCAS | 1:CAS:528:DyaK28Xjs1Ghsrw%3D&md5=277e451b8840d33631cfb0cc15d52b8bCAS | 8787029PubMed | 8787029PubMed |

Iannetta PPM, Laarhoven LJ, Medina-Escobar N, James EK, McManus MT, Davies HV, Harren FJM (2006) Ethylene and carbon dioxide production by developing strawberries show a correlative pattern that is indicative of ripening climacteric fruit. Physiologia Plantarum 127, 247–259.
Ethylene and carbon dioxide production by developing strawberries show a correlative pattern that is indicative of ripening climacteric fruit.CrossRef | 1:CAS:528:DC%2BD28XmtFSrsr8%3D&md5=1e3f02cbd4223a8c05ffc4f8878a9849CAS | 1:CAS:528:DC%2BD28XmtFSrsr8%3D&md5=1e3f02cbd4223a8c05ffc4f8878a9849CAS |

Ilić Z, Trajković R, Perzelan Y, Alkalai-Tuvia S, Fallik E (2012) Influence of 1-methylcyclopropene (1-MCP) on postharvest storage quality in green bell pepper fruit. Food and Bioprocess Technology 5, 2758–2767.
Influence of 1-methylcyclopropene (1-MCP) on postharvest storage quality in green bell pepper fruit.CrossRef |

Jia H-F, Chai Y-M, Li C-L, Lu D, Luo J-J, Qin L, Shen Y-Y (2011) Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiology 157, 188–199.
Abscisic acid plays an important role in the regulation of strawberry fruit ripening.CrossRef | 1:CAS:528:DC%2BC3MXht1Sit7%2FJ&md5=7ebefca5e7800d3d3688a4d5bd51c69dCAS | 1:CAS:528:DC%2BC3MXht1Sit7%2FJ&md5=7ebefca5e7800d3d3688a4d5bd51c69dCAS | 21734113PubMed | 21734113PubMed |

Katz YS, Galili G, Amir R (2006) Regulatory role of cystathionine-γ-synthase and de novo synthesis of methionine in ethylene production during tomato fruit ripening. Plant Molecular Biology 61, 255–268.
Regulatory role of cystathionine-γ-synthase and de novo synthesis of methionine in ethylene production during tomato fruit ripening.CrossRef | 1:CAS:528:DC%2BD28XlvFaitrk%3D&md5=6cd37caa61171807621f58bbbb2e2de4CAS | 1:CAS:528:DC%2BD28XlvFaitrk%3D&md5=6cd37caa61171807621f58bbbb2e2de4CAS | 16786305PubMed | 16786305PubMed |

Khoo KHP, Able AJ, Able JA (2012a) Poor homologous synapsis 1 (PHS1) interacts with chromatin but does not co-localise with Asynapsis 1 (ASY1) during early meiosis in bread wheat. International Journal of Plant Genomics 2012, 514398

Khoo KHP, Able AJ, Chataway TK, Able JA (2012b) Preliminary characterisation of two early meiotic wheat proteins after identification through 2D gel electrophoresis proteomics. Functional Plant Biology 39, 222–235.
Preliminary characterisation of two early meiotic wheat proteins after identification through 2D gel electrophoresis proteomics.CrossRef | 1:CAS:528:DC%2BC38XktFWhtbk%3D&md5=45d3f325ad4d63582845690c16a9dc15CAS | 1:CAS:528:DC%2BC38XktFWhtbk%3D&md5=45d3f325ad4d63582845690c16a9dc15CAS |

Knavel DE, Kemp TR (1973) Ethephon and CPTA on colour development in bell pepper fruits. HortScience 8, 403–404.

Kobayashi K, Baba S, Obayashi T, Sato M, Toyooka K, Keränen M, Aro E-M, Fukaki H, Ohta H, Sugimoto K, Masuda T (2012) Regulation of root greening by light and auxin/cytokinin signaling in Arabidopsis. The Plant Cell 24, 1081–1095.
Regulation of root greening by light and auxin/cytokinin signaling in Arabidopsis.CrossRef | 1:CAS:528:DC%2BC38Xmsl2jt7k%3D&md5=b3a623c1b1db3f136d320a19f0bbc605CAS | 1:CAS:528:DC%2BC38Xmsl2jt7k%3D&md5=b3a623c1b1db3f136d320a19f0bbc605CAS | 22415275PubMed | 22415275PubMed |

Kochevenko A, Araújo WL, Maloney GS, Tieman DM, Do PT, Taylor MG, Klee HJ, Fernie AR (2012) Catabolism of branched chain amino acids supports respiration but not volatile synthesis in tomato fruits. Molecular Plant 5, 366–375.
Catabolism of branched chain amino acids supports respiration but not volatile synthesis in tomato fruits.CrossRef | 1:CAS:528:DC%2BC38Xks1Sjs74%3D&md5=778bc51093210053d395efdf20998526CAS | 22199237PubMed | 22199237PubMed |

Kok EJ, Lehesranta SJ, van Dijk JP, Helsdingen JR, Dijksma WTP, Van Hoef AMA, Koistinen KM, Kärenlampi SO, Kuiper HA, Keijer J (2008) Changes in gene and protein expression during tomato ripening – consequences for the safety assessment of new crop plant varieties. Food Science & Technology International 14, 503–518.
Changes in gene and protein expression during tomato ripening – consequences for the safety assessment of new crop plant varieties.CrossRef | 1:CAS:528:DC%2BD1MXovFSksrs%3D&md5=e44ee5a21a6c6733a4655463d2d3d16cCAS |

Krajayklang M, Klieber A, Dry PR (2000) Colour at harvest and post-harvest behaviour influence paprika and chilli spice quality. Postharvest Biology and Technology 20, 269–278.
Colour at harvest and post-harvest behaviour influence paprika and chilli spice quality.CrossRef | 1:CAS:528:DC%2BD3cXmslKktro%3D&md5=ba730c33a881fed41a99e918689742a0CAS |

Krishnaswamy SS, Srivastava S, Mohammadi M, Rahman MH, Deyholos MK, Kav NNV (2008) Transcriptional profiling of pea ABR17 mediated changes in gene expression in Arabidopsis thaliana. BMC Plant Biology 8, 91
Transcriptional profiling of pea ABR17 mediated changes in gene expression in Arabidopsis thaliana.CrossRef | 18783601PubMed | 18783601PubMed |

Lelièvre J-M, Latché A, Jones B, Bouzayen M, Pech J-C (1997) Ethylene and fruit ripening. Physiologia Plantarum 101, 727–739.
Ethylene and fruit ripening.CrossRef |

Lin ZF, Zhong SL, Grierson D (2009) Recent advances in ethylene research. Journal of Experimental Botany 60, 3311–3336.
Recent advances in ethylene research.CrossRef | 1:CAS:528:DC%2BD1MXhtVWitrzJ&md5=15f32a9110a0815a8de5040d51e3fb19CAS |

Liu J-J, Ekramoddoullah AKM (2006) The family 10 of plant pathogenesis-related proteins: their structure, regulation, and function in response to biotic and abiotic stresses. Physiological and Molecular Plant Pathology 68, 3–13.
The family 10 of plant pathogenesis-related proteins: their structure, regulation, and function in response to biotic and abiotic stresses.CrossRef | 1:CAS:528:DC%2BD28XhtFersrbJ&md5=b30cad42dca56e4d7a4574efbb3be22fCAS |

Liu T-C, Liu Y-C, Chen K-E, Chao C-W, Wu C-T (2012) The nonclimacteric guava cultivar ‘Jen-Ju Bar’ is defective in System 2 1-aminocyclopropane-1-carboxylate synthase activity. Postharvest Biology and Technology 67, 10–18.
The nonclimacteric guava cultivar ‘Jen-Ju Bar’ is defective in System 2 1-aminocyclopropane-1-carboxylate synthase activity.CrossRef | 1:CAS:528:DC%2BC38Xjt1Wgsbw%3D&md5=2999d1b1d30ee91de9606c64a4b50f7eCAS |

Manning K, Tör M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nature Genetics 38, 948–952.
A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening.CrossRef | 1:CAS:528:DC%2BD28XnsVCgsr8%3D&md5=32d2a82ce05941a209e476f4bec9ac21CAS | 16832354PubMed | 16832354PubMed |

Marković-Housley Z, Degano M, Lamba D, von Roepenack-Lahaye E, Clemens S, Susani M, Ferreira F, Scheiner O, Breiteneder H (2003) Crystal structure of a hypoallergenic isoform of the major birch pollen allergen Bet v 1 and its likely biological function as a plant steroid carrier. Journal of Molecular Biology 325, 123–133.
Crystal structure of a hypoallergenic isoform of the major birch pollen allergen Bet v 1 and its likely biological function as a plant steroid carrier.CrossRef | 12473456PubMed | 12473456PubMed |

Martín-Trillo M, Cubas P (2010) TCP genes: a family snapshot 10 years later. Trends in Plant Science 15, 31–39.
TCP genes: a family snapshot 10 years later.CrossRef | 19963426PubMed | 19963426PubMed |

McMurchie EJ, McGlasson WB, Eaks IL (1972) Treatment of fruit with propylene gives information about biogenesis of ethylene. Nature 237, 235–236.
Treatment of fruit with propylene gives information about biogenesis of ethylene.CrossRef | 1:CAS:528:DyaE38XksVGmtLk%3D&md5=f381b65563a1ca7afa807eca8c34eae7CAS | 4557321PubMed | 4557321PubMed |

Moore S, Payton P, Wright M, Tanksley S, Giovannoni J (2005) Utilization of tomato microarrays for comparative gene expression analysis in the Solanaceae. Journal of Experimental Botany 56, 2885–2895.
Utilization of tomato microarrays for comparative gene expression analysis in the Solanaceae.CrossRef | 1:CAS:528:DC%2BD2MXhtFCjt7jP&md5=12c7f3f28de96fb62220aac9a981c519CAS | 16216847PubMed | 16216847PubMed |

Moradinezhad F, Sedgley M, Klieber A, Able AJ (2008) Variability of responses to 1-methylcyclopropene by banana: Influence of time of year at harvest and fruit position in the bunch. Annals of Applied Biology 152, 223–234.
Variability of responses to 1-methylcyclopropene by banana: Influence of time of year at harvest and fruit position in the bunch.CrossRef | 1:CAS:528:DC%2BD1cXmtFyltrw%3D&md5=5ef35ab0cd1893a597486934c8015511CAS |

Nakatsuka A, Murachi S, Okunishi H, Shiomi S, Nakano R, Kubo Y, Inaba A (1998) Differential expression and internal feedback regulation of 1-aminocyclopropane-1-carboxylate synthase, 1-aminocyclopropane-1-carboxylate oxidase, and ethylene receptor genes in tomato fruit during development and ripening. Plant Physiology 118, 1295–1305.
Differential expression and internal feedback regulation of 1-aminocyclopropane-1-carboxylate synthase, 1-aminocyclopropane-1-carboxylate oxidase, and ethylene receptor genes in tomato fruit during development and ripening.CrossRef | 1:CAS:528:DyaK1MXhtFE%3D&md5=be61641937416237ac64c0f78c26b037CAS | 9847103PubMed | 9847103PubMed |

Nick P, Heuing A, Ehmann B (2000) Plant chaperonins: a role in microtubule-dependent wall formation? Protoplasma 211, 234–244.
Plant chaperonins: a role in microtubule-dependent wall formation?CrossRef | 1:CAS:528:DC%2BD3cXlsFGhtbc%3D&md5=35142e403e8e019a83d328329b0e3479CAS | 1:CAS:528:DC%2BD3cXlsFGhtbc%3D&md5=35142e403e8e019a83d328329b0e3479CAS |

Nielsen TH, Skjærbæk HC, Karlsen P (1991) Carbohydrate metabolism during fruit development in sweet-pepper (Capsicum annuum) plants. Physiologia Plantarum 82, 311–319.
Carbohydrate metabolism during fruit development in sweet-pepper (Capsicum annuum) plants.CrossRef | 1:CAS:528:DyaK3MXks1ymtL0%3D&md5=129f383b0e9b2565d4d95365c71982c9CAS | 1:CAS:528:DyaK3MXks1ymtL0%3D&md5=129f383b0e9b2565d4d95365c71982c9CAS |

Nikiforova V, Kempa S, Zeh M, Maimann S, Kreft O, Casazza AP, Riedel K, Tauberger E, Hoefgen R, Hesse H (2002) Engineering of cysteine and methionine biosynthesis in potato. Amino Acids 22, 259–278.
Engineering of cysteine and methionine biosynthesis in potato.CrossRef | 1:CAS:528:DC%2BD38XkvFOmu7o%3D&md5=1036cefd929f4973fb9569dfb2ffaa32CAS | 1:CAS:528:DC%2BD38XkvFOmu7o%3D&md5=1036cefd929f4973fb9569dfb2ffaa32CAS | 12083069PubMed | 12083069PubMed |

Ogasawara S, Abe K, Nakajima T (2007) Pepper β-galactosidase 1 (PBG1) plays a significant role in fruit ripening in bell pepper (Capsicum annuum). Bioscience, Biotechnology, and Biochemistry 71, 309–322.
Pepper β-galactosidase 1 (PBG1) plays a significant role in fruit ripening in bell pepper (Capsicum annuum).CrossRef | 1:CAS:528:DC%2BD2sXivV2itrw%3D&md5=45b00dc6ce044e0e5efac6ea72f9fb09CAS | 17284822PubMed | 17284822PubMed |

Osorio S, Alba R, Nikoloski Z, Kochevenko A, Fernie AR, Giovannoni JJ (2012) Integrative comparative analyses of transcript and metabolite profiles from pepper and tomato ripening and development stages uncovers species-specific patterns of network regulatory behavior. Plant Physiology 159, 1713–1729.
Integrative comparative analyses of transcript and metabolite profiles from pepper and tomato ripening and development stages uncovers species-specific patterns of network regulatory behavior.CrossRef | 1:CAS:528:DC%2BC38Xht1CgsL%2FM&md5=92dadc676119731e4d84ad636db5593cCAS | 1:CAS:528:DC%2BC38Xht1CgsL%2FM&md5=92dadc676119731e4d84ad636db5593cCAS | 22685169PubMed | 22685169PubMed |

Paran I, van der Knaap E (2007) Genetic and molecular regulation of fruit and plant domestication traits in tomato and pepper. Journal of Experimental Botany 58, 3841–3852.
Genetic and molecular regulation of fruit and plant domestication traits in tomato and pepper.CrossRef | 1:CAS:528:DC%2BD1cXkvVah&md5=4046d02ef2d66c89e366972861969e2aCAS | 1:CAS:528:DC%2BD1cXkvVah&md5=4046d02ef2d66c89e366972861969e2aCAS | 18037678PubMed | 18037678PubMed |

Périn C, Gomez-Jimenez M, Hagen L, Dogimont C, Pech J-C, Latché A, Pitrat M, Lelièvre J-M (2002) Molecular and genetic characterization of a non-climacteric phenotype in melon reveals two loci conferring altered ethylene response in fruit. Plant Physiology 129, 300–309.
Molecular and genetic characterization of a non-climacteric phenotype in melon reveals two loci conferring altered ethylene response in fruit.CrossRef | 12011360PubMed | 12011360PubMed |

Pham TNT (2007) Ripening behaviour of capsicum (Capsicum annuum L.) fruit. PhD thesis, University of Adelaide, Australia.

Prasanna V, Prabha TN, Tharanathan RN (2007) Fruit ripening phenomena – an overview. Critical Reviews in Food Science and Nutrition 47, 1–19.
Fruit ripening phenomena – an overview.CrossRef | 1:CAS:528:DC%2BD2sXhsFahtb0%3D&md5=90b0b8e3fba3c1feb770cfafbf0dd48aCAS | 17364693PubMed | 17364693PubMed |

Pretel MT, Serrano M, Amoros A, Riquelme F, Romojaro F (1995) Non-involvement of ACC and ACC oxidase activity in pepper fruit ripening. Postharvest Biology and Technology 5, 295–302.
Non-involvement of ACC and ACC oxidase activity in pepper fruit ripening.CrossRef | 1:CAS:528:DyaK2MXmtFWmsbc%3D&md5=f2d926f12adfd59cf0cde09cf61fda10CAS |

Qin GZ, Wang YY, Cao BH, Wang WH, Tian SP (2012) Unraveling the regulatory network of the MADS box transcription factor RIN in fruit ripening. The Plant Journal 70, 243–255.
Unraveling the regulatory network of the MADS box transcription factor RIN in fruit ripening.CrossRef | 1:CAS:528:DC%2BC38XmvFegtrs%3D&md5=b68253a212d61fe7bbadee2be72555f3CAS |

Raines CA (2003) The Calvin cycle revisited. Photosynthesis Research 75, 1–10.
The Calvin cycle revisited.CrossRef | 1:CAS:528:DC%2BD3sXht1Kru7o%3D&md5=bc9e130e6ae436bc7fcbccd8b8943908CAS | 16245089PubMed | 16245089PubMed |

Rocco M, D’Ambrosio C, Arena S, Faurobert M, Scaloni A, Marra M (2006) Proteomic analysis of tomato fruits from two ecotypes during ripening. Proteomics 6, 3781–3791.
Proteomic analysis of tomato fruits from two ecotypes during ripening.CrossRef | 1:CAS:528:DC%2BD28XntlCjsLc%3D&md5=aa6f9903d80d538aace7cb20d3ecfbcbCAS | 16739135PubMed | 16739135PubMed |

Römer S, d’Harlingue A, Camara B, Schantz R, Kuntz M (1992) Cysteine synthase from Capsicum annuum chromoplasts – characterization and cDNA cloning of an upregulated enzyme during fruit development Journal of Biological Chemistry 267, 17966–17970.

Saltveit ME (1977) Carbon-dioxide, ethylene, and color development in ripening mature green bell peppers. Journal of the American Society for Horticultural Science 102, 523–525.

Saravanan RS, Rose JKC (2004) A critical evaluation of sample extraction techniques for enhanced proteomic analysis of recalcitrant plant tissues. Proteomics 4, 2522–2532.
A critical evaluation of sample extraction techniques for enhanced proteomic analysis of recalcitrant plant tissues.CrossRef | 1:CAS:528:DC%2BD2cXns1Ors70%3D&md5=19b616254d5066c69a5c05e9a891b4b6CAS | 15352226PubMed | 15352226PubMed |

Shin L-J, Lo J-C, Yeh K-C (2012) Copper chaperone antioxidant protein1 is essential for copper homeostasis. Plant Physiology 159, 1099–1110.
Copper chaperone antioxidant protein1 is essential for copper homeostasis.CrossRef | 1:CAS:528:DC%2BC38XhtVGlsbjP&md5=8adf0893c248ca42618cd571338d3469CAS | 22555879PubMed | 22555879PubMed |

Spíchal L (2012) Cytokinins – recent news and views of evolutionally old molecules. Functional Plant Biology 39, 267–284.
Cytokinins – recent news and views of evolutionally old molecules.CrossRef |

Sun LA, Zhang M, Ren J, Qi JX, Zhang GJ, Leng P (2010) Reciprocity between abscisic acid and ethylene at the onset of berry ripening and after harvest. BMC Plant Biology 10, 257
Reciprocity between abscisic acid and ethylene at the onset of berry ripening and after harvest.CrossRef |

Sweetman C, Deluc LG, Cramer GR, Ford CM, Soole KL (2009) Regulation of malate metabolism in grape berry and other developing fruits. Phytochemistry 70, 1329–1344.
Regulation of malate metabolism in grape berry and other developing fruits.CrossRef | 1:CAS:528:DC%2BD1MXhtFyqs7jN&md5=6bc5b4bfc0287500bc363d3322c95226CAS | 19762054PubMed | 19762054PubMed |

Symons GM, Davies C, Shavrukov Y, Dry IB, Reid JB, Thomas MR (2006) Grapes on steroids. Brassinosteroids are involved in grape berry ripening. Plant Physiology 140, 150–158.
Grapes on steroids. Brassinosteroids are involved in grape berry ripening.CrossRef | 1:CAS:528:DC%2BD28XhtVCgsbw%3D&md5=19cf38e44aad45fe3f5429c97b8852c8CAS | 16361521PubMed | 16361521PubMed |

Trainotti L, Pavanello A, Casadoro G (2005) Different ethylene receptors show an increased expression during the ripening of strawberries: does such an increment imply a role for ethylene in the ripening of these non-climacteric fruits? Journal of Experimental Botany 56, 2037–2046.
Different ethylene receptors show an increased expression during the ripening of strawberries: does such an increment imply a role for ethylene in the ripening of these non-climacteric fruits?CrossRef | 1:CAS:528:DC%2BD2MXmt1GmsrY%3D&md5=ce9a81cc813b3d3563de4a47b7565410CAS | 15955790PubMed | 15955790PubMed |

Villavicencio L, Blankenship SM, Sanders DC, Swallow WH (1999) Ethylene and carbon dioxide production in detached fruit of selected pepper cultivars. Journal of the American Society for Horticultural Science 124, 402–406.

Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J (2002) A MADS-box gene necessary for fruit ripening at the tomato Ripening-Inhibitor (Rin) locus. Science 296, 343–346.
A MADS-box gene necessary for fruit ripening at the tomato Ripening-Inhibitor (Rin) locus.CrossRef | 1:CAS:528:DC%2BD38XjtVWhsrk%3D&md5=77a14170c0a9d2d58952c24299a8280bCAS | 1:CAS:528:DC%2BD38XjtVWhsrk%3D&md5=77a14170c0a9d2d58952c24299a8280bCAS | 11951045PubMed | 11951045PubMed |

Watkins CB (2006) The use of 1-methylcyclopropene (1-MCP) on fruits and vegetables. Biotechnology Advances 24, 389–409.
The use of 1-methylcyclopropene (1-MCP) on fruits and vegetables.CrossRef | 1:CAS:528:DC%2BD28XltFOrs7Y%3D&md5=626fee0a3fe8578ec9ec3c911f1a2325CAS | 16530376PubMed | 16530376PubMed |

Whitelegge JP (2004) Mass spectrometry for high throughput quantitative proteomics in plant research: lessons from thylakoid membranes. Plant Physiology and Biochemistry 42, 919–927.
Mass spectrometry for high throughput quantitative proteomics in plant research: lessons from thylakoid membranes.CrossRef | 1:CAS:528:DC%2BD2MXhtFGht74%3D&md5=7fd73d8091ef481174baca78eb7d1fc5CAS | 15707830PubMed | 15707830PubMed |

Yamane M, Abe D, Yasui S, Yokotani N, Kimata W, Ushijima K, Nakano R, Kubo Y, Inaba A (2007) Differential expression of ethylene biosynthetic genes in climacteric and non-climacteric Chinese pear fruit. Postharvest Biology and Technology 44, 220–227.
Differential expression of ethylene biosynthetic genes in climacteric and non-climacteric Chinese pear fruit.CrossRef | 1:CAS:528:DC%2BD2sXjvFOls7c%3D&md5=f5a2d94f987c7afef5ece6939fa7057cCAS |

Yokotani N, Nakano R, Imanishi S, Nagata M, Inaba A, Kubo Y (2009) Ripening-associated ethylene biosynthesis in tomato fruit is autocatalytically and developmentally regulated. Journal of Experimental Botany 60, 3433–3442.
Ripening-associated ethylene biosynthesis in tomato fruit is autocatalytically and developmentally regulated.CrossRef | 1:CAS:528:DC%2BD1MXhtVWisbnF&md5=0b2337f3ed98fabbfa1c6a3002915edaCAS | 19605457PubMed | 19605457PubMed |

Zhang XJ, Agrawal A, San KY (2012) Improving fatty acid production in Escherichia coli through the overexpression of malonyl coA-Acyl carrier protein transacylase. Biotechnology Progress 28, 60–65.
Improving fatty acid production in Escherichia coli through the overexpression of malonyl coA-Acyl carrier protein transacylase.CrossRef |



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