Role of plant hormones and their interplay in development and ripening of fleshy fruits

Journal of Experimental Botany

Volumn 65, Issue 16, 2014, Pages 4561-4575

  Kumar, Rahul ^a,c   Khurana, Ashima ^b   Sharma, Arun K ^a  

^a UNIVERSITY OF DELHI   (India)

^b UNIVERSITY OF DELHI   (India)

^c UNIVERSITY OF HYDERABAD   (India)

Author keywords

ABA; Auxin; ethylene; fruit development; phytohormone; ripening; tomato

Indexed keywords

PHYTOHORMONE;

FRUIT; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; TOMATO;

EPIGENESIS, GENETIC; FRUIT; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; LYCOPERSICON ESCULENTUM; PLANT GROWTH REGULATORS;

EID: 84905472365     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru277     Document Type: Review

References (152)

1. Abel S, Nguyen MD, Chow W, Theologis A. 1995. ACS4, a primary indoleacetic acid-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis thaliana. Structural characterization, expression in Escherichia coli, and expression characteristics in response to auxin. Journal of Biological Chemistry 270, 19093-19099.
2. Achard P, Baghour M, Chapple A, Hedden P, Van Der Straeten D, Genschik P, Moritz T, Harberd NP. 2007. The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes. Proceedings of the National Academy of Sciences, USA 104, 6484-6489.
3. Alcazar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF. 2010. Polyamines: Molecules with regulatory functions in plant abiotic stress tolerance. Planta 231, 1237-1249.
4. Arnaud N, Girin T, Sorefan K, Fuentes S, Wood TA, Lawrenson T, Sablowski R, Ostergaard L. 2010. Gibberellins control fruit patterning in Arabidopsis thaliana. Genes and Development 24, 2127-2132.
5. 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.
6. 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.
7. Bastias A, Lopez-Climent M, Valcarcel M, Rosello S, Gomez-Cadenas A, Casaretto JA. 2011. Modulation of organic acids and sugar content in tomato fruits by an abscisic acid-regulated transcription factor. Physiologia Plantarum 141, 215-226.
8. Bemer M, Karlova R, Ballester AR, Tikunov YM, Bovy AG, Wolters-Arts M, Rossetto Pde B, Angenent GC, de Maagd RA. 2012. The Tomato FRUITFULL homologs TDR4/FUL1 and MBP7/FUL2 regulate ethylene-independent aspects of fruit ripening. Plant Cell 24, 4437-4451.
9. Blumenfeld A, Gazit S. 1970. Cytokinin activity in avocado seeds during fruit development. Plant Physiology 46, 331-333.
10. Botondi R, DeSantis D, Bellincontro A, Vizovitis K, Mencarelli F. 2003. Influence of ethylene inhibition by 1-methylcyclopropene on apricot quality, volatile production, and glycosidase activity of low-and higharoma varieties of apricots. Journal of Agricultural and Food Chemistry 51, 1189-1200.
11. Bottcher C, Boss PK, Davies C. 2011. Acyl substrate preferences of an IAA-amido synthetase account for variations in grape (Vitis vinifera L.) berry ripening caused by different auxinic compounds indicating the importance of auxin conjugation in plant development. Journal of Experimental Botany 62, 4267-4280.
12. Bottcher C, Keyzers RA, Boss PK, Davies C. 2010. Sequestration of auxin by the indole-3-acetic acid-amido synthetase GH3-1 in grape berry (Vitis vinifera L.) and the proposed role of auxin conjugation during ripening. Journal of Experimental Botany 61, 3615-3625.
13. Bregoli AM, Scaramagli S, Costa G, Sabatini E, Ziosi V, Biondi S, Torrigiani P. 2002. Peach (Prunus persica) fruit ripening: Aminoethoxyvinylglycine (AVG) and exogenous polyamines affect ethylene emission and flesh firmness. Physiologia Plantarum 114, 472-481.
14. Carbonell-Bejerano P, Urbez C, Granell A, Carbonell J, Perez-Amador MA. 2011. Ethylene is involved in pistil fate by modulating the onset of ovule senescence and the GA-mediated fruit set in Arabidopsis. BMC Plant Biology 11, 84.
15. Carrari F, Baxter C, Usadel B et al. 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.
16. Carrera E, Ruiz-Rivero O, Peres LE, Atares A, Garcia-Martinez JL. 2012. Characterization of the procera tomato mutant shows novel functions of the SlDELLA protein in the control of flower morphology, cell division and expansion, and the auxin-signaling pathway during fruit-set and development. Plant Physiology 160, 1581-1596.
17. Chai Y-M, Jia H-F, Li C-L, Dong Q-H, Shen Y-Y. 2013. FaPYR1 is involved in strawberry fruit ripening. Journal of Experimental Botany 62, 5079-5089.
18. Cheng G, Yang E, Lu W, Jia Y, Jiang Y, Duan X. 2009. Effect of nitric oxide on ethylene synthesis and softening of banana fruit slice during ripening. Journal of Agricultural and Food Chemistryistry 57, 5799-5804.
19. Chernys JT, Zeevaart JA. 2000. Characterization of the 9-cisepoxycarotenoid dioxygenase gene family and the regulation of abscisic acid biosynthesis in avocado. Plant Physiology 124, 343-353.
20. Chervin C, El-Kereamy A, Roustan JP, Latche 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.
21. Chung MY, Vrebalov J, Alba R, Lee J, McQuinn R, Chung JD, Klein P, Giovannoni J. 2010. A tomato (Solanum lycopersicum) APETALA2/ERF gene, SlAP2a, is a negative regulator of fruit ripening. The Plant Journal 64, 936-947.
22. Coenen C, Christian M, Luthen H, Lomax TL. 2003. Cytokinin inhibits a subset of diageotropica-dependent primary auxin responses in tomato. Plant Physiology 131, 1692-1704.
23. Crane JC. 1964. Growth substances in fruit setting and development. Annual Review of Plant Physiology 15, 303-326.
24. Cui X, Ge C, Wang R, Wang H, Chen W, Fu Z, Jiang X, Li J, Wang Y. 2010. The BUD2 mutation affects plant architecture through altering cytokinin and auxin responses in Arabidopsis. Cell Research 20, 576-586.
25. Daminato M, Guzzo F, Casadoro G. 2013. A SHATTERPROOF-like gene controls ripening in non-climacteric strawberries, and auxin and abscisic acid antagonistically affect its expression. Journal of Experimental Botany 64, 3775-3786.
26. Davey JE, Van Staden J. 1978. Endogenous cytokinins in the fruits of ripening and non-ripening tomatoes. Plant Science Letters 11, 359-364.
27. de Jong M, Wolters-Arts M, Feron R, Mariani C, Vriezen WH. 2009. The Solanum lycopersicum auxin response factor 7 (SlARF7) regulates auxin signaling during tomato fruit set and development. The Plant Journal 57, 160-170.
28. de Jong M, Wolters-Arts M, Garcia-Martinez JL, Mariani C, Vriezen WH. 2011. The Solanum lycopersicum AUXIN RESPONSE FACTOR 7 (SlARF7) mediates cross-talk between auxin and gibberellin signalling during tomato fruit set and development. Journal of Experimental Botany 62, 617-626.
29. Deluc LG, Grimplet J, Wheatley MD, Tillett RL, Quilici DR, Osborne C, Schooley DA, Schlauch KA, Cushman JC, Cramer GR. 2007. Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development. BMC Genomics 8, 429-429.
30. Devoghalaere F, Doucen T, Guitton B et al. 2012. A genomics approach to understanding the role of auxin in apple (Malus x domestica) fruit size control. 12, 7.
31. Dong T, Hu Z, Deng L, Wang Y, Zhu M, Zhang J, Chen G. 2013. A tomato MADS-box transcription factor, SlMADS1, acts as a negative regulator of fruit ripening. Plant Physiology 163, 1026-1036.
32. Dorcey E, Urbez C, Blazquez MA, Carbonell J, Perez-Amador MA. 2009. Fertilization-dependent auxin response in ovules triggers fruit development through the modulation of gibberellin metabolism in Arabidopsis. The Plant Journal 58, 318-332.
33. Dostal HC, Leopold AC. 1967. Gibberellin delays ripening of tomatoes. Science 158, 1579-1580.
34. Duan X, Su X, You Y, Qu H, Li Y, Jiang Y. 2007. Effect of nitric oxide on pericarp browning of harvested longan fruit in relation to phenolic metabolism. Food Chemistry 104, 571-576.
35. Eum HL, Kim HB, Choi SB, Lee SK. 2009. Regulation of ethylene biosynthesis by nitric oxide in tomato (Solanum lycopersicum L.) fruit harvested at different ripening stages. European Food Research and Technology 228, 331-338.
36. Fait A, Hanhineva K, Beleggia R, Dai N, Rogachev I, Nikiforova VJ, Fernie AR, Aharoni A. 2008. Reconfiguration of the achene and receptacle metabolic networks during strawberry fruit development. Plant Physiology 148, 730-750.
37. Fan X, Matches JP, Fellowman JK. 1996. Inhibition of apple fruit 1-aminocyclopropane-1-carboxylic acid oxides activity and respiration by acetylsalicylic acid. Journal of Plant Physiology 149, 469-471.
38. Fan X, Mattheis JP, Fellman JK. 1998. A role for jasmonates in climacteric fruit ripening. Planta 204, 444-449.
39. Flores F, El Yahyaoui F, de Billerbeck G, Romojaro F, Latche A, Bouzayen M, Pech JC, Ambid C. 2002. Role of ethylene in the biosynthetic pathway of aliphatic ester aroma volatiles in Charentais Cantaloupe melons. Journal of Experimental Botany 53, 201-206.
40. Fu FQ, Mao WH, Shi K, Zhou YH, Asami T, Yu JQ. 2008. A role of brassinosteroids in early fruit development in cucumber. Journal of Experimental Botany 59, 2299-2308.
41. Fuentes S, Ljung K, Sorefan K, Alvey E, Harberd NP, Ostergaard L. 2012. Fruit growth in Arabidopsis occurs via DELLA-dependent and DELLA-independent gibberellin responses. Plant Cell 24, 3982-3996.
42. Fujisawa M, Nakano T, Shima Y, Ito Y. 2013. A large-scale identification of direct targets of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening. Plant Cell 25, 371-386.
43. 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 doi: Http://dx.doi.org/ 10.1105/tpc.113.119453.
44. Galpaz N, Wang Q, Menda N, Zamir D, Hirschberg J. 2008. Abscisic acid deficiency in the tomato mutant high-pigment 3 leading to increased plastid number and higher fruit lycopene content. The Plant Journal 53, 717-730.
45. Gambetta GA, Matthews MA, Shaghasi TH, McElrone AJ, Castellarin SD. 2010. Sugar and abscisic acid signaling orthologs are activated at the onset of ripening in grape. Planta 232, 219-234.
46. Gao C, Ju Z, Li S, Zuo J, Fu D, Tian H, Luo Y, Zhu B. 2013. Deciphering ascorbic acid regulatory pathways in ripening tomato fruit using a weighted gene correlation network analysis approach. Journal of Integrative Plant Biology 55, 1080-1091.
47. García-Martínez JL, Carbonell J. 1980. Fruit-set of unpollinated ovaries of Pisum sativum L. Influence of plant-growth regulators. Planta 147, 451-456.
48. Gillaspy G, Ben-David H, Gruissem W. 1993. Fruits: A developmental perspective. Plant Cell 5, 1439-1451.
49. Giovannoni JJ. 2004. Genetic regulation of fruit development and ripening. Plant Cell 16 Suppl, S170-180.
50. Given NK, Venis MA, Grierson D. 1988. Hormonal regulation of ripening in the strawberry, a non-climacteric fruit. Planta 174, 402-406.
51. Goetz M, Hooper LC, Johnson SD, Rodrigues JC, Vivian-Smith A, Koltunow AM. 2007. Expression of aberrant forms of AUXIN RESPONSE FACTOR8 stimulates parthenocarpy in Arabidopsis and tomato. Plant Physiology 145, 351-366.
52. Guillon F, Philippe S, Bouchet B, Devaux M-F, Frasse P, Jones B, Bouzayen M, Lahaye M. 2008. Down-regulation of an auxin response factor in the tomato induces modification of fine pectin structure and tissue architecture. Journal of Experimental Botany 59, 273-288.
53. Harberd NP. 2003. Botany. Relieving DELLA restraint. Science 299, 1853-1854.
54. He Y, Tang RH, Hao Y et al. 2004. Nitric oxide represses the Arabidopsis floral transition. Science 305, 1968-1971.
55. Ireland HS, Yao JL, Tomes S, Sutherland PW, Nieuwenhuizen N, Gunaseelan K, Winz RA, David KM, Schaffer RJ. 2013. Apple SEPALLATA1/2-like genes control fruit flesh development and ripening. The Plant Journal 73, 1044-1056.
56. Jaakola L, Poole M, Jones MO et al. 2010. A SQUAMOSA MADS box gene involved in the regulation of anthocyanin accumulation in bilberry fruits. Plant Physiology 153, 1619-1629.
57. 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.
58. Jiang Y, Joyce DC, Macnish AJ. 2000. Effect of abscisic acid on banana fruit ripening in relation to the role of ethylene. Journal of Plant Growth Regulation 19, 106-111.
59. Johnston JW, Gunaseelan K, Pidakala P, Wang M, Schaffer RJ. 2009. Co-ordination of early and late ripening events in apples is regulated through differential sensitivities to ethylene. Journal of Experimental Botany 60, 2689-2699.
60. Jones B, Frasse P, Olmos E, Zegzouti H, Li ZG, Latche A, Pech JC, Bouzayen M. 2002. Down-regulation of DR12, an auxin-response-factor homolog, in the tomato results in a pleiotropic phenotype including dark green and blotchy ripening fruit. The Plant Journal 32, 603-613.
61. Kang C, Darwish O, Geretz A, Shahan R, Alkharouf N, Liu Z. 2013. Genome-scale transcriptomic insights into early-stage fruit development in woodland strawberry Fragaria vesca. Plant Cell 25, 1960-1978.
62. Kanno Y, Jikumaru Y, Hanada A, Nambara E, Abrams SR, Kamiya Y. 2010. Comprehensive hormone profiling in developing Arabidopsis seeds: Examination of the site of ABA biosynthesis, ABA transport and hormone interactions. Plant Cell Physiology 51, 1988-2001.
63. Karlova R, Rosin FM, Busscher-Lange J, Parapunova V, Do PT, Fernie AR, Fraser PD, Baxter C, Angenent GC, de Maagd RA. 2011. Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening. Plant Cell 23, 923-941.
64. Karlova R, van Haarst JC, Maliepaard C, van de Geest H, Bovy AG, Lammers M, Angenent GC, de Maagd RA. 2013. Identification of microRNA targets in tomato fruit development using high-throughput sequencing and degradome analysis. Journal of Experimental Botany 64, 1863-1878.
65. Kausch KD, Sobolev AP, Goyal RK, Fatima T, Laila-Beevi R, Saftner RA, Handa AK, Mattoo AK. 2011. Methyl jasmonate deficiency alters cellular metabolome, including the aminome of tomato (Solanum lycopersicum L.) fruit. Amino Acids 42, 843-856.
66. Klee HJ, Giovannoni JJ. 2011. Genetics and control of tomato fruit ripening and quality attributes. Annual Review of Genetics 45, 41-59.
67. Knapp S. 2002. Tobacco to tomatoes: A phylogenetic perspective on fruit diversity in the Solanaceae. Journal of Experimental Botany 53, 2001-2022.
68. Kondo S, Tomyiama A, Seto H. 2000. Changes of endogenous jasmonic acid and methyl jasmonate in apples and sweet cherries during fruit development. Journal of the American Society for Horticultural Science 125, 282-287.
69. Kumar R, Agarwal P, Tyagi AK, Sharma AK. 2012a. Genome-wide investigation and expression analysis suggest diverse roles of auxinresponsive GH3 genes during development and response to different stimuli in tomato (Solanum lycopersicum). Molecular Genetics and Genomics 287, 221-235.
70. Kumar R, Sharma MK, Kapoor S, Tyagi AK, Sharma AK. 2012b. Transcriptome analysis of rin mutant fruit and in silico analysis of promoters of differentially regulated genes provides insight into LeMADSRIN-regulated ethylene-dependent as well as ethylene-independent aspects of ripening in tomato. Molecular Genetics and Genomics 287, 189-203.
71. Kumar R, Tyagi AK, Sharma AK. 2011. Genome-wide analysis of auxin response factor (ARF) gene family from tomato and analysis of their role in flower and fruit development. Molecular Genetics and Genomics 285, 245-260.
72. Lee JM, Joung JG, McQuinn R, Chung MY, Fei Z, Tieman D, Klee H, Giovannoni J. 2012. Combined transcriptome, genetic diversity and metabolite profiling in tomato fruit reveals that the ethylene response factor SlERF6 plays an important role in ripening and carotenoid accumulation. The Plant Journal 70, 191-204.
73. Lemaire-Chamley M, Petit J, Garcia V, Just D, Baldet P, Germain V, Fagard M, Mouassite M, Cheniclet C, Rothan C. 2005. Changes in transcriptional profiles are associated with early fruit tissue specialization in tomato. Plant Physiology 139, 750-769.
74. Li N, Parsons BL, Liu DR, Mattoo AK. 1992. Accumulation of woundinducible ACC synthase transcript in tomato fruit is inhibited by salicylic acid and polyamines. Plant Molecular Biology 18, 477-487.
75. Lin Z, Arciga-Reyes L, Zhong S, Alexander L, Hackett R, Wilson I, Grierson D. 2008a. SlTPR1, a tomato tetratricopeptide repeat protein, interacts with the ethylene receptors NR and LeETR1, modulating ethylene and auxin responses and development. Journal of Experimental Botany 59, 4271-4287.
76. Lin Z, Hong Y, Yin M, Li C, Zhang K, Grierson D. 2008b. A tomato HD-Zip homeobox protein, LeHB-1, plays an important role in floral organogenesis and ripening. The Plant Journal 55, 301-310.
77. Liu K, Kang BC, Jiang H, Moore SL, Li H, Watkins CB, Setter TL, Jahn MM. 2005. A GH3-like gene, CcGH3, isolated from Capsicum chinense L. fruit is regulated by auxin and ethylene. Plant Molecular Biology 58, 447-464.
78. Liu L, Wei J, Zhang M, Zhang L, Li C, Wang Q. 2012. Ethylene independent induction of lycopene biosynthesis in tomato fruits by jasmonates. Journal of Experimental Botany 63, 5751-5761.
79. Lohani S, Trivedi PK, Nath P. 2004. Changes in activities of cell wall hydrolases during ethylene-induced ripening in banana: Effect of 1-MCP, ABA and IAA. Postharvest Biology and Technology 31, 119-126.
80. Lopez-Gomez R, Cabrera-Ponce JL, Saucedo-Arias LJ, Carreto-Montoya L, Villanueva-Arce R, Diaz-Perez JC, Gomez-Lim MA, Herrera-Estrella L. 2009. Ripening in papaya fruit is altered by ACC oxidase cosuppression. Transgenic Research 18, 89-97.
81. Manjunatha G, Gupta KJ, Lokesh V, Mur LA, Neelwarne B. 2012. Nitric oxide counters ethylene effects on ripening fruits. Plant Signaling and Behavior 7, 476-483.
82. Manning K, Tor 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.
83. Manriquez D, El-Sharkawy I, Flores FB, El-Yahyaoui F, Regad F, Bouzayen M, Latche A, Pech JC. 2006. Two highly divergent alcohol dehydrogenases of melon exhibit fruit ripening-specific expression and distinct biochemical characteristics. Plant Molecular Biology 61, 675-685.
84. Mariotti L, Picciarelli P, Lombardi L, Ceccarelli N. 2011. Fruit-set and early fruit growth in tomato are associated with increases in indoleacetic acid, cytokinin, and bioactive gibberellin contents. Journal of Plant Growth Regulation 30, 405-415.
85. Marsch-Martinez N, Reyes-Olalde JI, Ramos-Cruz D, Lozano-Sotomayor P, Zuniga-Mayo VM, de Folter S. 2012. Hormones talking: Does hormonal cross-talk shape the Arabidopsis gynoecium? Plant Signaling and Behavior 7, 1698-1701.
86. Martel C, Vrebalov J, Tafelmeyer P, Giovannoni JJ. 2011. The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLOURLESS NONRIPENING-dependent manner. Plant Physiology 157, 1568-1579.
87. Marti C, Orzaez D, Ellul P, Moreno V, Carbonell J, Granell A. 2007. Silencing of DELLA induces facultative parthenocarpy in tomato fruits. The Plant Journal 52, 865-876.
88. Martínez-Romero D, Valero D, Serrano M, Burló F, Carbonell A, Burgos L, Riquelme F. 2000. Exogenous polyamines and gibberellic acid effects on peach (Prunus persica L.) storability improvement. Journal of Food Science 65, 288-294.
89. Matsuo S, Kikuchi K, Fukuda M, Honda I, Imanishi S. 2012. Roles and regulation of cytokinins in tomato fruit development. Journal of Experimental Botany 63, 5569-5579.
90. McAtee P, Karim S, Schaffer R, David K. 2013. A dynamic interplay between phytohormones is required for fruit development, maturation, and ripening. Front Plant Science 4, 79.
91. Mounet F, Moing A, Garcia V et al. 2009. Gene and metabolite regulatory network analysis of early developing fruit tissues highlights new candidate genes for the control of tomato fruit composition and development. Plant Physiology 149, 1505-1528.
92. Mounet F, Moing A, Kowalczyk M et al. 2012. Down-regulation of a single auxin efflux transport protein in tomato induces precocious fruit development. Journal of Experimental Botany 63, 4901-4917.
93. Nishiyama K, Guis M, Rose JK et al. 2007. Ethylene regulation of fruit softening and cell wall disassembly in Charentais melon. Journal of Experimental Botany 58, 1281-1290.
94. Nitsch JP. 1952. Plant hormones in the development of fruits. The Quarterly Review of Biology 27, 33-57.
95. Nitsch L, Kohlen W, Oplaat C et al. 2012. ABA-deficiency results in reduced plant and fruit size in tomato. Journal of Plant Physiology 169, 878-883.
96. Nitsch LM, Oplaat C, Feron R, Ma Q, Wolters-Arts M, Hedden P, Mariani C, Vriezen WH. 2009. Abscisic acid levels in tomato ovaries are regulated by LeNCED1 and SlCYP707A1. Planta 229, 1335-1346.
97. Ogawa M, Kay P, Wilson S, Swain SM. 2009. ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE1 (ADPG1), ADPG2, and QUARTET2 are Polygalacturonases required for cell separation during reproductive development in Arabidopsis. Plant Cell 21, 216-233.
98. Osorio S, Alba R, Damasceno CM et al. 2011. Systems biology of tomato fruit development: Combined transcript, protein, and metabolite analysis of tomato transcription factor (nor, rin) and ethylene receptor (Nr) mutants reveals novel regulatory interactions. Plant Physiology 157, 405-425.
99. Ozga JA, Brenner ML, Reinecke DM. 1992. Seed effects on gibberellin metabolism in pea pericarp. Plant Physiology 100, 88-94.
100. Ozga JA, Yu J, Reinecke DM. 2003. Pollination-, development-, and auxin-specific regulation of gibberellin 3beta-hydroxylase gene expression in pea fruit and seeds. Plant Physiology 131, 1137-1146.
101. Parra-Lobato MC, Gomez-Jimenez MC. 2011. Polyamine-induced modulation of genes involved in ethylene biosynthesis and signalling pathways and nitric oxide production during olive mature fruit abscission. Journal of Experimental Botany 62, 4447-4465.
102. Pascual L, Blanca JM, Canizares J, Nuez F. 2009. Transcriptomic analysis of tomato carpel development reveals alterations in ethylene and gibberellin synthesis during pat3/pat4 parthenocarpic fruit set. BMC Plant Biology 9, 67.
103. Pattison RJ, Catala C. 2012. Evaluating auxin distribution in tomato (Solanum lycopersicum) through an analysis of the PIN and AUX/LAX gene families. The Plant Journal 70, 585-598.
104. Payasi A, Misra PC, Sanwal GG. 2004. Effect of phytohormones on pectate lyase activity in ripening Musa acuminata. Plant Physiology and Biochemistry 42, 861-865.
105. Perez AG, Sanz C, Olias R, Olias JM. 1997. Effect of methyl jasmonate on in vitro strawberry ripening. Journal of Agricultural and Food Chemistryistry 45, 3733-3737.
106. Pristijono P, Wills R, Golding J. 2006. Inhibition of browning on the surface of apple slices by short term exposure to nitric oxide (NO) gas. Postharvest Biology and Technology 42, 256-259.
107. Qin G, Wang Y, Cao B, Wang W, Tian S. 2012. Unraveling the regulatory network of the MADS box transcription factor RIN in fruit ripening. The Plant Journal 70, 243-255.
108. Quesada MA, Blanco-Portales R, Pose S et al. 2009. Antisense down-regulation of the FaPG1 gene reveals an unexpected central role for polygalacturonase in strawberry fruit softening. Plant Physiology 150, 1022-1032.
109. Raghavan V. 2003. Some reflections on double fertilization, from its discovery to the present. New Phytologist 159, 565-583.
110. Ren Z, Li Z, Miao Q, Yang Y, Deng W, Hao Y. 2011. The auxin receptor homologue in Solanum lycopersicum stimulates tomato fruit set and leaf morphogenesis. Journal of Experimental Botany 62, 2815-2826.
111. Rohrmann J, Tohge T, Alba R et al. 2011. Combined transcription factor profiling, microarray analysis and metabolite profiling reveals the transcriptional control of metabolic shifts occurring during tomato fruit development. The Plant Journal 68, 999-1013.
112. Rossetto MRM, Purgatto E, Do Nascimento JRO, Lajolo FM, Cordenunsi BR. 2003. Effects of gibberellic acid on sucrose accumulation and sucrose biosynthesizing enzymes activity during banana ripening. Plant Growth Regulation 31, 207-214.
113. Ruan YL, Patrick JW, Bouzayen M, Osorio S, Fernie AR. 2012. Molecular regulation of seed and fruit set. Trends Plant Science 17, 656-665.
114. Saladie M, Matas AJ, Isaacson T et al. 2007. A reevaluation of the key factors that influence tomato fruit softening and integrity. Plant Physiology 144, 1012-1028.
115. Santisree P, Nongmaithem S, Vasuki H, Sreelakshmi Y, Ivanchenko MG, Sharma R. 2011. Tomato root penetration in soil requires a coaction between ethylene and auxin signaling. Plant Physiology 156, 1424-1438.
116. Schaffer RJ, Friel EN, Souleyre EJ et al. 2007. A genomics approach reveals that aroma production in apple is controlled by ethylene predominantly at the final step in each biosynthetic pathway. Plant Physiology 144, 1899-1912.
117. Schaffer RJ, Ireland HS, Ross JJ, Ling TJ, David KM. 2013. SEPALLATA1/2-suppressed mature apples have low ethylene, high auxin and reduced transcription of ripening-related genes. AoB PLANTS 5, pls047.
118. Serrani JC, Ruiz-Rivero O, Fos M, Garcia-Martinez JL. 2008. Auxininduced fruit-set in tomato is mediated in part by gibberellins. The Plant Journal 56, 922-934.
119. Seymour GB, Ostergaard L, Chapman NH, Knapp S, Martin C. 2013. Fruit development and ripening. Annual Review of Plant Biology 64, 219-241.
120. Seymour GB, Ryder CD, Cevik V, Hammond JP, Popovich A, King GJ, Vrebalov J, Giovannoni JJ, Manning K. 2011. A SEPALLATA gene is involved in the development and ripening of strawberry (Fragaria x ananassa Duch.) fruit, a non-climacteric tissue. Journal of Experimental Botany 62, 1179-1188.
121. Singh R, Singh P, Pathak N, Singh VK, Dwivedi UN. 2007. Modulation of mango ripening by chemicals: Physiological and biochemical aspects. Plant Growth Regulation 53, 137-145.
122. Srivastava A, Handa AK. 2005. Hormonal regulation of tomato fruit development: A molecular perspective. Journal of Plant Growth Regulation 24, 67-82.
123. Srivastava MK, Dwivedi UN. 2000. Delayed ripening of banana fruit by salicylic acid. Plant Science 158, 87-96.
124. Sudha RR, Amutha S, Muthulaksmi W, Baby R, Indira K, Mareeswari P. 2007. Influence of pre and post harvest chemical treatments on physical characteristics of sapota (Achras sapota L.) var. PKM 1. Journal of Agricultural and Biological Science 3, 450-452.
125. Sun L, Sun Y, Zhang M et al. 2012a. Suppression of 9-cisepoxycarotenoid dioxygenase, which encodes a key enzyme in abscisic acid biosynthesis, alters fruit texture in transgenic tomato. Plant Physiology 158, 283-298.
126. Sun L, Yuan B, Zhang M, Wang L, Cui M, Wang Q, Leng P. 2012b. Fruit-specific RNAi-mediated suppression of SlNCED1 increases both lycopene and beta-carotene contents in tomato fruit. Journal of Experimental Botany 63, 3097-3108.
127. Sun Y, Chen P, Duan C et al. 2012c. Transcriptional regulation of genes encoding key enzymes of abscisic acid metabolism during melon (Cucumis melo L.) fruit development and ripening. Journal of Plant Growth Regulation 32, 233-244.
128. 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.
129. Tatsuki M, Nakajima N, Fujii H, Shimada T, Nakano M, Hayashi K, Hayama H, Yoshioka H, Nakamura Y. 2013. Increased levels of IAA are required for system 2 ethylene synthesis causing fruit softening in peach (Prunus persica L. Batsch). Journal of Experimental Botany 64, 1049-1059.
130. Thompson AJ, Tor M, Barry CS, Vrebalov J, Orfila C, Jarvis MC, Giovannoni JJ, Grierson D, Seymour GB. 1999. Molecular and genetic characterization of a novel pleiotropic tomato-ripening mutant. Plant Physiology 120, 383-390.
131. Tomato Genome Consortium. 2012. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485, 635-641.
132. Torrigiani P, Bressanin D, Beatriz Ruiz K, Tadiello A, Trainotti L, Bonghi C, Ziosi V, Costa G. 2012. Spermidine application to young developing peach fruits leads to a slowing down of ripening by impairing ripening-related ethylene and auxin metabolism and signaling. Physiologia Plantarum 146, 86-98.
133. Trainotti L, Tadiello A, Casadoro G. 2007. The involvement of auxin in the ripening of climacteric fruits comes of age: The hormone plays a role of its own and has an intense interplay with ethylene in ripening peaches. Journal of Experimental Botany 58, 3299-3308.
134. Van de Poel B, Bulens I, Markoula A et al. 2012. Targeted systems biology profiling of tomato fruit reveals coordination of the yang cycle and a distinct regulation of ethylene biosynthesis during postclimacteric ripening. Plant Physiology 160, 1498-1514.
135. Van Huizen R, Ozga JA, Reinecke DM. 1997. Seed and hormonal regulation of gibberellin 20-oxidase expression in Pea pericarp. Plant Physiology 115, 123-128.
136. Vardhini VB, Rao SS. 2002. Acceleration of ripening of tomato pericarp discs by brassinosteroids. Phytochemistry 61, 843-847.
137. Vivian-Smith A, Koltunow AM. 1999. Genetic analysis of growth-regulatorinduced parthenocarpy in Arabidopsis. Plant Physiology 121, 437-451.
138. Vrebalov J, Pan IL, Arroyo AJM et al. 2009. Fleshy fruit expansion and ripening are regulated by the Tomato SHATTERPROOF gene TAGL1. Plant Cell 21, 3041-3062.
139. 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.
140. Vriezen WH, Feron R, Maretto F, Keijman J, Mariani C. 2008. Changes in tomato ovary transcriptome demonstrate complex hormonal regulation of fruit set. New Phytologist 177, 60-76.
141. Wang H, Schauer N, Usadel B, Frasse P, Zouine M, Hernould M, Latche A, Pech JC, Fernie AR, Bouzayen M. 2009. Regulatory features underlying pollination-dependent and-independent tomato fruit set revealed by transcript and primary metabolite profiling. Plant Cell 21, 1428-1452.
142. Werner T, Hanus J, Holub J, Schmulling T, Van Onckelen H, Strnad M. 2003. New cytokinin metabolites in IPT transgenic Arabidopsis thaliana plants. Physiologia Plantarum 118, 127-137.
143. Xiong AS, Yao QH, Peng RH, Li X, Han PL, Fan HQ. 2005. Different effects on ACC oxidase gene silencing triggered by RNA interference in transgenic tomato. Plant Cell Reports 23, 639-646.
144. Xu WP, Chen KS, Li F, Zhang SL. 2000. Regulation of lipoxygenase on jasmonic acid biosynthesis in ripening kiwifruit. Acta Phytophysiologica Sinica 26, 507-514.
145. Yamagami T, Tsuchisaka A, Yamada K, Haddon WF, Harden LA, Theologis A. 2003. Biochemical diversity among the 1-aminocyclopropane-1-carboxylate synthase isozymes encoded by the Arabidopsis gene family. Journal of Biological Chemistry 278, 49102-49112.
146. Yang J, Zhang J, Huang Z, Wang Z, Zhu Q, Liu L. 2002. Correlation of cytokinin levels in the endosperms and roots with cell number and cell division activity during endosperm development in rice. Annals of Botany 90, 369-377.
147. Zaharah S, Singh Z, Symons G, J. R. 2012. Role of brassinosteroids, ethylene, abscisic acid, and indole-3-acetic acid in mango fruit ripening. Journal of Plant Growth Regulation 31, 363-372.
148. Zhang M, Yuan B, Leng P. 2009. The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. Journal of Experimental Botany 60, 1579-1588.
149. Zheng Y, Hong H, Chen L, Li J, Sheng J, Shen L. 2014. LeMAPK1, LeMAPK2 and LeMAPK3 are associated with nitric oxide-induced defense response against Botrytis cinerea in the Lycopersicon esculentum fruit. Journal of Agricultural and Food Chemistry DOI: 10.1021/jf404870d.
150. Zhong S, Fei Z, Chen YR, Zheng Y, Huang M, Vrebalov J, McQuinn R, Gapper N, Liu B, Xiang J, Shao Y, Giovannoni JJ. 2013. Singlebase resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nature Biotechnology 31, 154-159.
151. Zifkin M, Jin A, Ozga JA, Zaharia LI, Schernthaner JP, Gesell A, Abrams SR, Kennedy JA, Constabel CP. 2012. Gene expression and metabolite profiling of developing highbush blueberry fruit indicates transcriptional regulation of flavonoid metabolism and activation of abscisic acid metabolism. Plant Physiology 158, 200-224.
152. Ziosi V, Bonghi C, Bregoli AM, Trainotti L, Biondi S, Sutthiwal S, Kondo