The zinc finger transcription factor SlZFP2 negatively regulates abscisic acid biosynthesis and fruit ripening in tomato

Plant Physiology

Volumn 167, Issue 3, 2015, Pages 931-949

  Weng, Lin ^a   Zhao, Fangfang ^a   Li, Rong ^a   Xu, Changjie ^b   Chen, Kunsong ^b   Xiao, Han ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); LYCOPERSICON ESCULENTUM;

ABSCISIC ACID; MESSENGER RNA; PLANT PROTEIN; PROTEIN BINDING; TRANSCRIPTION FACTOR; ZINC FINGER PROTEIN;

BIOSYNTHESIS; FRUIT; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLANT GENE; PLANT SEED; PROMOTER REGION; REPRODUCTION; RNA INTERFERENCE; TOMATO;

ABSCISIC ACID; BASE SEQUENCE; BIOSYNTHETIC PATHWAYS; FRUIT; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GERMINATION; LYCOPERSICON ESCULENTUM; PHENOTYPE; PLANT PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REPRODUCTION; RNA INTERFERENCE; RNA, MESSENGER; SEEDS; TRANSCRIPTION FACTORS; ZINC FINGERS;

EID: 84923673880     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.255174     Document Type: Article

References (92)

1. Barrero JM, Rodríguez PL, Quesada V, Piqueras P, Ponce MR, Micol JL (2006) Both abscisic acid (ABA)-dependent and ABA-independent pathways govern the induction of NCED3, AAO3 and ABA1 in response to salt stress. Plant Cell Environ 29: 2000-2008.
2. 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 Physiol 123: 979-986.
3. Bemer M, Karlova R, Ballester AR, Tikunov YM, Bovy AG, Wolters-Arts M, Rossetto PdeB, Angenent GC, de Maagd RA (2012) The tomato FRUITFULL homologs TDR4/FUL1 and MBP7/FUL2 regulate ethyleneindependent aspects of fruit ripening. Plant Cell 24: 4437-4451.
4. Böttcher 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. J Exp Bot 61: 3615-3625.
5. Burbidge A, Grieve TM, Jackson A, Thompson A, McCarty DR, Taylor IB (1999) Characterization of the ABA-deficient tomato mutant notabilis and its relationship with maize Vp14. Plant J 17: 427-431.
6. Buta JG, Spaulding DW (1994) Changes in indole-3-acetic acid and abscisic acid levels during tomato (Lycopersicon esculentum Mill.) fruit development and ripening. J Plant Growth Regul 13: 163-166.
7. Cai S, Lashbrook CC (2008) Stamen abscission zone transcriptome profiling reveals new candidates for abscission control: enhanced retention of floral organs in transgenic plants overexpressing Arabidopsis ZINC FINGER PROTEIN2. Plant Physiol 146: 1305-1321.
8. 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 Biol 11: 84.
9. Cheng WH, Endo A, Zhou L, Penney J, Chen HC, Arroyo A, Leon P, Nambara E, Asami T, Seo M, et al (2002) A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell 14: 2723-2743.
10. 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. Plant J 64: 936-947.
11. Coen ES, Romero JM, Doyle S, Elliott R, Murphy G, Carpenter R (1990) floricaula: a homeotic gene required for flower development in Antirrhinum majus. Cell 63: 1311-1322.
12. 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 Physiol 163: 1026-1036.
13. Endo A, Sawada Y, Takahashi H, Okamoto M, Ikegami K, Koiwai H, Seo M, Toyomasu T, Mitsuhashi W, Shinozaki K, et al (2008) Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells. Plant Physiol 147: 1984-1993.
14. Englbrecht CC, Schoof H, Böhm S (2004) Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 5: 39.
15. Feurtado JA, Huang D, Wicki-Stordeur L, Hemstock LE, Potentier MS, Tsang EW, Cutler AJ (2011) The Arabidopsis C2H2 zinc finger INDETERMINATE DOMAIN1/ENHYDROUS promotes the transition to germination by regulating light and hormonal signaling during seed maturation. Plant Cell 23: 1772-1794.
16. Frey A, Effroy D, Lefebvre V, Seo M, Perreau F, Berger A, Sechet J, To A, North HM, Marion-Poll A (2012) Epoxycarotenoid cleavage by NCED5 fine-tunes ABA accumulation and affects seed dormancy and drought tolerance with other NCED family members. Plant J 70: 501-512.
17. Frey A, Godin B, Bonnet M, Sotta B, Marion-Poll A (2004) Maternal synthesis of abscisic acid controls seed development and yield in Nicotiana plumbaginifolia. Planta 218: 958-964.
18. Fu X, Kong W, Peng G, Zhou J, Azam M, Xu C, Grierson D, Chen K (2012) Plastid structure and carotenogenic gene expression in red- and whitefleshed loquat (Eriobotrya japonica) fruits. J Exp Bot 63: 341-354.
19. 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.
20. 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. Plant J 53: 717-730.
21. Gan Y, Kumimoto R, Liu C, Ratcliffe O, Yu H, Broun P (2006) GLABROUS INFLORESCENCE STEMS modulates the regulation by gibberellins of epidermal differentiation and shoot maturation in Arabidopsis. Plant Cell 18: 1383-1395.
22. Gan Y, Liu C, Yu H, Broun P (2007) Integration of cytokinin and gibberellin signalling by Arabidopsis transcription factors GIS, ZFP8 and GIS2 in the regulation of epidermal cell fate. Development 134: 2073-2081.
23. Gillaspy G, Ben-David H, Gruissem W (1993) Fruits: a developmental perspective. Plant Cell 5: 1439-1451.
24. Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell (Suppl) 16: S170-S180.
25. Giovannoni JJ (2007) Fruit ripening mutants yield insights into ripening control. Curr Opin Plant Biol 10: 283-289.
26. Harrison E, Burbidge A, Okyere JP, Thompson AJ, Taylor IB (2011) Identification of the tomato ABA-deficient mutant sitiens as a member of the ABA-aldehyde oxidase gene family using genetic and genomic analysis. Plant Growth Regul 64: 301-309.
27. Hauser F, Waadt R, Schroeder JI (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Curr Biol 21: R346-R355.
28. Hichri I, Muhovski Y, Žižkova E, Dobrev PI, Franco-Zorrilla JM, Solano R, Lopez-Vidriero I, Motyka V, Lutts S (2014) The Solanum lycopersicum Zinc Finger2 cysteine-2/histidine-2 repressor-like transcription factor regulates development and tolerance to salinity in tomato and Arabidopsis. Plant Physiol 164: 1967-1990.
29. Hoth S, Morgante M, Sanchez JP, Hanafey MK, Tingey SV, Chua NH (2002) Genome-wide gene expression profiling in Arabidopsis thaliana reveals new targets of abscisic acid and largely impaired gene regulation in the abi1-1 mutant. J Cell Sci 115: 4891-4900.
30. Huang XY, Chao DY, Gao JP, Zhu MZ, Shi M, Lin HX (2009) A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes Dev 23: 1805-1817.
31. Itkin M, Seybold H, Breitel D, Rogachev I, Meir S, Aharoni A (2009) TOMATO AGAMOUS-LIKE 1 is a component of the fruit ripening regulatory network. Plant J 60: 1081-1095.
32. Ito S, Song YH, Josephson-Day AR, Miller RJ, Breton G, Olmstead RG, Imaizumi T (2012) FLOWERING BHLH transcriptional activators control expression of the photoperiodic flowering regulator CONSTANS in Arabidopsis. Proc Natl Acad Sci USA 109: 3582-3587.
33. Je J, Chen H, Song C, Lim CO (2014) Arabidopsis DREB2C modulates ABA biosynthesis during germination. Biochem Biophys Res Commun 452: 91-98.
34. Jensen MK, Lindemose S, de Masi F, Reimer JJ, Nielsen M, Perera V, Workman CT, Turck F, Grant MR, Mundy J, et al (2013) ATAF1 transcription factor directly regulates abscisic acid biosynthetic gene NCED3 in Arabidopsis thaliana. FEBS Open Bio 3: 321-327.
35. Jia HF, Chai YM, Li CL, Lu D, Luo JJ, Qin L, Shen YY (2011) Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiol 157: 188-199.
36. Jiang Y, Liang G, Yu D (2012) Activated expression of WRKY57 confers drought tolerance in Arabidopsis. Mol Plant 5: 1375-1388.
37. 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.
38. Kerschen A, Napoli CA, Jorgensen RA, Müller AE (2004) Effectiveness of RNA interference in transgenic plants. FEBS Lett 566: 223-228.
39. Kim DH, Yamaguchi S, Lim S, Oh E, Park J, Hanada A, Kamiya Y, Choi G (2008) SOMNUS, a CCCH-type zinc finger protein in Arabidopsis, negatively regulates light-dependent seed germination downstream of PIL5. Plant Cell 20: 1260-1277.
40. Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45: 41-59.
41. Ko JH, Yang SH, Han KH (2006) Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J 47: 343-355.
42. Kodaira KS, Qin F, Tran LS, Maruyama K, Kidokoro S, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K (2011) Arabidopsis Cys2/His2 zinc-finger proteins AZF1 and AZF2 negatively regulate abscisic acidrepressive and auxin-inducible genes under abiotic stress conditions. Plant Physiol 157: 742-756.
43. Koiwai H, Nakaminami K, Seo M, Mitsuhashi W, Toyomasu T, Koshiba T (2004) Tissue-specific localization of an abscisic acid biosynthetic enzyme, AAO3, in Arabidopsis. Plant Physiol 134: 1697-1707.
44. Krieger U, Lippman ZB, Zamir D (2010) The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nat Genet 42: 459-463.
45. Lifschitz E, Ayre BG, Eshed Y (2014) Florigen and anti-florigen: a systemic mechanism for coordinating growth and termination in flowering plants. Front Plant Sci 5: 465.
46. Manning K, TörM, 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. Nat Genet 38: 948-952.
47. 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. J Plant Growth Regul 30: 405-415.
48. 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 COLORLESS NONRIPENING-dependent manner. Plant Physiol 157: 1568-1579.
49. Martínez C, Manzano S, Megías Z, Garrido D, Picó B, Jamilena M (2013) Involvement of ethylene biosynthesis and signalling in fruit set and early fruit development in zucchini squash (Cucurbita pepo L.). BMC Plant Biol 13: 139.
50. McAtee P, Karim S, Schaffer R, David K (2013) A dynamic interplay between phytohormones is required for fruit development, maturation, and ripening. Front Plant Sci 4: 79.
51. McCormick S (1991) Transformation of tomato with Agrobacterium tumefaciens. In K Lindsey, ed, Plant Tissue Culture Manual, Vol 6. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 1-9.
52. Meng X, Brodsky MH, Wolfe SA (2005) A bacterial one-hybrid system for determining the DNA-binding specificity of transcription factors. Nat Biotechnol 23: 988-994.
53. Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56: 165-185.
54. 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.
55. Pan X, Welti R, Wang X (2010) Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatographymass spectrometry. Nat Protoc 5: 986-992.
56. Pascual L, Blanca JM, Cañizares 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 Biol 9: 67.
57. Peng H, Zheng L, Lee WH, Rux JJ, Rauscher FJ III (2002) A common DNAbinding site for SZF1 and the BRCA1-associated zinc finger protein, ZBRK1. Cancer Res 62: 3773-3781.
58. Pnueli L, Carmel-Goren L, Hareven D, Gutfinger T, Alvarez J, Ganal M, Zamir D, Lifschitz E (1998) The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development 125: 1979-1989.
59. Sagi M, Scazzocchio C, Fluhr R (2002) The absence of molybdenum cofactor sulfuration is the primary cause of the flacca phenotype in tomato plants. Plant J 31: 305-317.
60. Sakai H, Medrano LJ, Meyerowitz EM (1995) Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries. Nature 378: 199-203.
61. Sakamoto H, Araki T, Meshi T, Iwabuchi M (2000) Expression of a subset of the Arabidopsis Cys(2)/His(2)-type zinc-finger protein gene family under water stress. Gene 248: 23-32.
62. Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Arabidopsis Cys2/His2-type zincfinger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol 136: 2734-2746.
63. Seo M, Koshiba T (2002) Complex regulation of ABA biosynthesis in plants. Trends Plant Sci 7: 41-48.
64. Seymour GB, Østergaard L, Chapman NH, Knapp S,Martin C (2013) Fruit development and ripening. Annu Rev Plant Biol 64: 219-241.
65. Sun L, Sun Y, Zhang M, Wang L, Ren J, Cui M,Wang Y, Ji K, Li P, Li Q, et al (2012a) Suppression of 9-cis-epoxycarotenoid dioxygenase, which encodes a key enzyme in abscisic acid biosynthesis, alters fruit texture in transgenic tomato. Plant Physiol 158: 283-298.
66. Sun L, Yuan B, Zhang M, Wang L, Cui M, Wang Q, Leng P (2012b) Fruitspecific RNAi-mediated suppression of SlNCED1 increases both lycopene and β-carotene contents in tomato fruit. J Exp Bot 63: 3097-3108.
67. Thompson AJ, Jackson AC, Parker RA, Morpeth DR, Burbidge A, Taylor IB (2000) Abscisic acid biosynthesis in tomato: regulation of zeaxanthin epoxidase and 9-cis-epoxycarotenoid dioxygenase mRNAs by light/ dark cycles, water stress and abscisic acid. Plant Mol Biol 42: 833-845.
68. Toh S, Imamura A, Watanabe A, Nakabayashi K, Okamoto M, Jikumaru Y, Hanada A, Aso Y, Ishiyama K, Tamura N, et al (2008) High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiol 146: 1368-1385.
69. Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635-641.
70. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
71. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515.
72. Vrebalov J, Pan IL, Arroyo AJ, McQuinn R, Chung M, Poole M, Rose J, Seymour G, Grandillo S, Giovannoni J, et al (2009) Fleshy fruit expansion and ripening are regulated by the tomato SHATTERPROOF gene TAGL1. Plant Cell 21: 3041-3062.
73. 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.
74. Vriezen WH, Feron R, Maretto F, Keijman J, Mariani C (2008) Changes in tomato ovary transcriptome demonstrate complex hormonal regulation of fruit set. New Phytol 177: 60-76.
75. Wang H, Schauer N, Usadel B, Frasse P, Zouine M, Hernould M, Latché 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.
76. Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valon C, Freidit Frey N, Leung J (2008) An update on abscisic acid signaling in plants and more. Mol Plant 1: 198-217.
77. Weingartner M, Subert C, Sauer N (2011) LATE, a C(2)H(2) zinc-finger protein that acts as floral repressor. Plant J 68: 681-692.
78. Xiao H, Jiang N, Schaffner E, Stockinger EJ, van der Knaap E (2008) A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science 319: 1527-1530.
79. Xiao H, Radovich C, Welty N, Hsu J, Li D, Meulia T, van der Knaap E (2009) Integration of tomato reproductive developmental landmarks and expression profiles, and the effect of SUN on fruit shape. BMC Plant Biol 9: 49.
80. Xiao H, Wang Y, Liu D, Wang W, Li X, Zhao X, Xu J, Zhai W, Zhu L (2003) Functional analysis of the rice AP3 homologue OsMADS16 by RNA interference. Plant Mol Biol 52: 957-966.
81. Xiong L, Gong Z, Rock CD, Subramanian S, Guo Y, Xu W, Galbraith D, Zhu JK (2001a) Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. Dev Cell 1: 771-781.
82. Xiong L, Ishitani M, Lee H, Zhu JK (2001b) The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression. Plant Cell 13: 2063-2083.
83. Xiong L, Lee H, Ishitani M, Zhu JK (2002) Regulation of osmotic stressresponsive gene expression by the LOS6/ABA1 locus in Arabidopsis. J Biol Chem 277: 8588-8596.
84. Xiong L, Zhu JK (2003) Regulation of abscisic acid biosynthesis. Plant Physiol 133: 29-36.
85. Yaish MW, El-Kereamy A, Zhu T, Beatty PH, Good AG, Bi YM, Rothstein SJ (2010) The APETALA-2-like transcription factor OsAP2-39 controls key interactions between abscisic acid and gibberellin in rice. PLoS Genet 6: e1001098.
86. Yang J, Worley E, Udvardi M (2014) A NAP-AAO3 regulatory module promotes chlorophyll degradation via ABA biosynthesis in Arabidopsis leaves. Plant Cell 26: 4862-4874.
87. Yang M, Zhang B, Jia J, Yan C, Habaike A, Han Y (2013) RRP41L, a putative core subunit of the exosome, plays an important role in seed germination and early seedling growth in Arabidopsis. Plant Physiol 161: 165-178.
88. Yano R, Kanno Y, Jikumaru Y, Nakabayashi K, Kamiya Y, Nambara E (2009) CHOTTO1, a putative double APETALA2 repeat transcription factor, is involved in abscisic acid-mediated repression of gibberellin biosynthesis during seed germination in Arabidopsis. Plant Physiol 151: 641-654.
89. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565-1572.
90. Zhang M, Yuan B, Leng P (2009) The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. J Exp Bot 60: 1579-1588.
91. Zhou Z, An L, Sun L, Zhu S, XiW, Broun P, Yu H, Gan Y (2011) Zinc Finger Protein5 is required for the control of trichome initiation by acting upstream of Zinc Finger Protein8 in Arabidopsis. Plant Physiol 157: 673-682.
92. Zhou Z, Sun L, Zhao Y, An L, Yan A, Meng X, Gan Y (2013) Zinc Finger Protein 6 (ZFP6) regulates trichome initiation by integrating gibberellin and cytokinin signaling in Arabidopsis thaliana. New Phytol 198: 699- 708.