Interaction analysis of grapevine MIKCc-type MADS transcription factors and heterologous expression of putative véraison regulators in tomato

Journal of Plant Physiology

Volumn 170, Issue 16, 2013, Pages 1424-1433

  Mellway, Robin D ^a   Lund, Steven T ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Berry; Fruit; Grapevine; MADS; Ripening; Transcription factor; V raison

Indexed keywords

LYCOPERSICON ESCULENTUM; SOLANUM; VITACEAE; VITIS; VITIS VINIFERA;

2 AMINO 3 PHOSPHONOPROPIONIC ACID; HOMEODOMAIN PROTEIN; MADS DOMAIN PROTEIN; SILVER; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

AGAMOUS; AP1; APETALA1; APETALA3; ARTICLE; BERRY; FRUIT; GENE EXPRESSION REGULATION; GENETICS; GRAPEVINE; GROWTH, DEVELOPMENT AND AGING; MADS; METABOLISM; PI; PISTILLATA; RIPENING; SEP; SEPALLATA; TOMATO; TRANSGENIC PLANT; TWO HYBRID SYSTEM; VÉRAISON; VITIS;

AG; AGAMOUS; AP1; AP3; APETALA1; APETALA3; BERRY; FRUIT; GRAPEVINE; MADS; PI; PISTILLATA; RIPENING; SEP; SEPALLATA; TRANSCRIPTION FACTOR; VÉRAISON;

FRUIT; GENE EXPRESSION REGULATION, PLANT; HOMEODOMAIN PROTEINS; LYCOPERSICON ESCULENTUM; MADS DOMAIN PROTEINS; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; TWO-HYBRID SYSTEM TECHNIQUES; VITIS;

EID: 84884142658     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2013.05.010     Document Type: Article

References (57)

1. Alba R., Payton P., Fei Z., McQuinn R., Debbie P., Martin G.B., et al. Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development. Plant Cell 2005, 17:2954-2965.
2. Barry C.S., Giovannoni J.J. Ripening in the tomato green-ripe mutant is inhibited by ectopic expression of a protein that disrupts ethylene signaling. Proc Natl Acad Sci USA 2006, 103:7923-7928.
3. Bino R.J., Ric de Vos C.H., Lieberman M., Hall R.D., Bovy A., Jonker H.H., et al. The light-hyperresponsive high pigment-2dg mutation of tomato: alterations in the fruit metabolome. New Phytol 2005, 166:427-438.
4. Boss P.K., Sensi E., Hua C., Davies C., Thomas M.R. Cloning and characterisation of grapevine (Vitis vinifera L.) MADS-box genes expressed during inflorescence and berry development. Plant Sci 2002, 162:887-895.
5. Boss P.K., Vivier M., Matsumoto S., Dry I.B., Thomas M.R. A cDNA from grapevine (Vitis vinifera L.), which shows homology to AGAMOUS and SHATTERPROOF, is not only expressed in flowers but also throughout berry development. Plant Mol Biol 2001, 45:541-553.
6. Bowman J.L., Drews G.N., Meyerowitz E.M. Expression of the Arabidopsis floral homeotic gene AGAMOUS is restricted to specific cell types late in flower development. Plant Cell 1991, 3:749-758.
7. Calonje M., Cubas P., Martínez-Zapater J.M., Carmona M.J. Floral meristem identity genes are expressed during tendril development in grapevine. Plant Physiol 2004, 135:1491-1501.
8. Causier B., Schwarz-Sommer Z., Davies B. Floral organ identity: 20 years of ABCs. Semin Cell Dev Biol 2010, 21:73-79.
9. Coen E.S., Meyerowitz E.M. The war of the whorls: genetic interactions controlling flower development. Nature 1991, 353:31-37.
10. Cortina C., Culianez-Maci F.A. Tomato transformation and transgenic plant production. Plant Cell Tissue Organ Cult 2004, 76:269-275.
11. Davies B., Motte P., Keck E., Saedler H., Sommer H., Schwarz-Sommer Z. PLENA and FARINELLI: redundancy and regulatory interactions between two Antirrhinum MADS-box factors controlling flower development. EMBO J 1999, 18:4023-4034.
12. de Folter S., Angenent G.C. Trans meets cis in MADS science. Trends Plant Sci 2006, 11:224-231.
13. Deluc L.G., Grimplet J., Wheatley M.D., Tillett R.L., Quilici D.R., Osborne C., et al. Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development. BMC Genomics 2007, 8:429.
14. c-type MADS box genes in grapevine. Plant Physiol 2009, 149:354-369.
15. Elitzur T., Vrebalov J., Giovannoni J.J., Goldschmidt E.E., Friedman H. The regulation of MADS-box gene expression during ripening of banana and their regulatory interaction with ethylene. J Exp Bot 2010, 61:1523-1535.
16. Favaro R., Pinyopich A., Battaglia R., Kooiker M., Borghi L., Ditta G., et al. MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell 2003, 15:2603-2611.
17. Fei Z., Tang X., Alba R.M., White J.A., Ronning C.M., Martin G.B., et al. Comprehensive EST analysis of tomato and comparative genomics of fruit ripening. Plant J 2004, 40:47-59.
18. Fujisawa M., Nakano T., Shima Y., Ito Y. A large-scale identification of direct targets of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening. Plant Cell 2013, 25:371-386.
19. Fujisawa M., Shima Y., Higuchi N., Nakano T., Koyama Y., Kasumi T., et al. Direct targets of the tomato-ripening regulator RIN identified by transcriptome and chromatin immunoprecipitation analyses. Planta 2012, 235:1107-1122.
20. Fujisawa M., Nakano T., Ito Y. Identification of potential target genes for the tomato fruit-ripening regulator RIN by chromatin immunoprecipitation. BMC Plant Biol 2011, 30:11-26.
21. Giménez E., Pineda B., Capel J., Antón M.T., Atarés A., Pérez-Martín F., et al. Functional analysis of the Arlequin mutant corroborates the essential role of the Arlequin/TAGL1 gene during reproductive development of tomato. PLoS ONE 2010, 5:e14427.
22. Herner R.C., Sink K.C. Ripening behavior of the rin tomato mutant. Acta Hort 1977, 62:239-246.
23. Immink R.G., Tonaco I.A., de Folter S., Shchennikova A., van Dijk A.D., Busscher-Lange J., et al. SEPALLATA3: the 'glue' for MADS box transcription factor complex formation. Genome Biol 2009, 10:R24.
24. Ireland H.S., Yao J.L., Tomes S., Sutherland P.W., Nieuwenhuizen N., Gunaseelan K., et al. Apple SEPALLATA1/2-like genes control fruit flesh development and ripening. Plant J 2013, 73:1044-1056.
25. Itkin M., Seybold H., Breitel D., Rogachev I., Meir S., Aharoni A. TOMATO AGAMOUS-LIKE 1 is a component of the fruit ripening regulatory network. Plant J 2009, 60:1081-1095.
26. Jaillon O., Aury J.M., Noel B., Policriti A., Clepet C., Casagrande A., et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 2007, 449:463-467.
27. Kaufmann K., Muiño J.M., Jauregui R., Airoldi C.A., Smaczniak C., Krajewski P., et al. Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower. PLoS Biol 2009, 7:e1000090.
28. Lanahan M.B., Yen H.C., Giovannoni J.J., Klee H.J. The never ripe mutation blocks ethylene perception in tomato. Plant Cell 1994, 6:521-530.
29. Leseberg C.H., Eissler C.L., Wang X., Johns M.A., Duvall M.R., Mao L. Interaction study of MADS-domain proteins in tomato. J Exp Bot 2008, 59:2253-2265.
30. Litt A., Kramer E.M. The ABC model and the diversification of floral organ identity. Semin Cell Dev Biol 2010, 21:129-137.
31. Liu J.H., Zhang J., Jia C.H., Zhang J.B., Wang J.S., Yang Z.X., et al. The interaction of banana MADS-box protein MuMADS1 and ubiquitin-activating enzyme E-MuUBA in post-harvest banana fruit. Plant Cell Rep 2013, 32:129-137.
32. Liu J., Xu B., Hu L., Li M., Su W., Wu J., et al. Involvement of a banana MADS-box transcription factor gene in ethylene-induced fruit ripening. Plant Cell Rep 2009, 28:103-111.
33. Lund S.T., Peng F.Y., Nayar T., Reid K.E., Schlosser J. Gene expression analyses in individual grape (Vitis vinifera L.) berries during ripening initiation reveal that pigmentation intensity is a valid indicator of developmental staging within the cluster. Plant Mol Biol 2008, 68:301-315.
34. Malcomber S.T., Kellogg E.A. SEPALLATA gene diversification: brave new whorls. Trends Plant Sci 2005, 10:427-435.
35. Martel C., Vrebalov J., Tafelmeyer P., Giovannoni J.J. The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plant Physiol 2011, 157:1568-1579.
36. Mizzotti C., Mendes M.A., Caporali E., Schnittger A., Kater M.M., Battaglia R., et al. The MADS box genes SEEDSTICK and ARABIDOPSIS Bsister play a maternal role in fertilization and seed development. Plant J 2012, 70:409-420.
37. Nicolas P., Lecourieux D., Gomès E., Delrot S., Lecourieux F. The grape berry-specific basic helix-loop-helix transcription factor VvCEB1 affects cell size. J Exp Bot 2013, 64:991-1003.
38. Périn C., Gomez-Jimenez M., Hagen L., Dogimont C., Pech J-C., Latché A., et al. Molecular and genetic characterization of a non-climacteric phenotype in melon reveals two loci conferring altered ethylene response in fruit. Plant Physiol 2002, 129:300-309.
39. Pilati S., Perazzolli M., Malossini A., Cestaro A., Demattè L., Fontana P., et al. Genome-wide transcriptional analysis of grapevine berry ripening reveals a set of genes similarly modulated during three seasons and the occurrence of an oxidative burst at vèraison. BMC Genomics 2007, 22:428.
40. Pinyopich A., Ditta G.S., Savidge B., Liljegren S.J., Baumann E., Wisman E., et al. Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 2003, 424:85-88.
41. Pirogovskaia T., Kempler C., Kitts D.D., Lund S.T. Phenotypic diversity in antioxidant phytochemical composition among fruits from several genotypes of red raspberry (Rubus idaeus L.). J Berry Res 2012, 2:229-238.
42. Pnueli L., Hareven D., Rounsley S.D., Yanofsky M.F., Lifschitz E. Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell 1994, 6:163-173.
43. Poupin M.J., Federici F., Medina C., Matus J.T., Timmermann T., Arce-Johnson P. Isolation of the three grape sub-lineages of B-class MADS-box TM6, PISTILLATA and APETALA3 genes which are differentially expressed during flower and fruit development. Gene 2007, 404:10-24.
44. Qin G., Wang Y., Cao B., Wang W., Tian S. Unraveling the regulatory network of the MADS box transcription factor RIN in fruit ripening. Plant J 2012, 70:243-255.
45. Reid K.R., Olsson N., Schlosser J., Peng F.Y., Lund S.T. An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biol 2006, 6:27.
46. Ruokolainen S., Ng Y.P., Albert V.A., Elomaa P., Teeri T.H. Large scale interaction analysis predicts that the Gerbera hybrida floral E function is provided both by general and specialized proteins. BMC Plant Biol 2010, 10:129.
47. Seymour G.B., Ryder C.D., Cevik V., Hammond J.P., Popovich A., King G.J., et al. A SEPALLATA gene is involved in the development and ripening of strawberry (Fragaria x ananassa Duch.) fruit, a non-climacteric tissue. J Exp Bot 2011, 62:1179-1188.
48. Slimestad R., Fossen T., Verheul M.J. The flavonoids of tomatoes. J Agric Food Chem 2008, 56:2436-2441.
49. Tadiello A., Pavanello A., Zanin D., Caporali E., Colombo L., Rotino G.L., et al. PLENA-like gene of peach is involved in carpel formation and subsequent transformation into a fleshy fruit. J Exp Bot 2009, 60:651-661.
50. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
51. Theissen G., Sedler H. Plant biology: floral quartets. Nature 2001, 409:469-471.
52. Vrebalov J., Pan I.L., Arroyo A.J., McQuinn R., Chung M., Poole M., et al. Fleshy fruit expansion and ripening are regulated by the tomato SHATTERPROOF gene TAGL1. Plant Cell 2009, 21:3041-3062.
53. Vrebalov J., Ruezinsky D., Padmanabhan V., White R., Medrano D., Drake R., et al. A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 2002, 296:343-346.
54. Yanofsky M.F., Ma H., Bowman J.L., Drews G.N., Feldmann K.A., Meyerowitz E.M. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 1990, 346:35-39.
55. Zahn L.M., Kong H., Leebens-Mack J.H., Kim S., Soltis P.S., Landherr L.L., et al. The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history. Genetics 2005, 169:2209-2223.
56. Zenoni S., Ferrarini A., Giacomelli E., Xumerle L., Fasoli M., Malerba G., et al. Characterization of transcriptional complexity during berry development in Vitis vinifera using RNA-Seq. Plant Physiol 2010, 152:1787-1795.
57. Zhu H.L., Zhu B.Z., Li Y.C., Shao Y., Wang X.G., Xie Y.H., et al. Expression and DNA binding activity of the tomato transcription factor RIN (ripening inhibitor). Biosci Biotechnol Biochem 2008, 72:250-252.