Network inference analysis identifies an APRR2-like gene linked to pigment accumulation in tomato and pepper fruits

Plant Physiology

Volumn 161, Issue 3, 2013, Pages 1476-1485

  Pan, Yu ^a   Bradley, Glyn ^a   Pyke, Kevin ^a   Ball, Graham ^c   Lu, Chungui ^a   Fray, Rupert ^a   Marshall, Alexandra ^a   Jayasuta, Subhalai ^a   Baxter, Charles ^b   van Wijk, Rik ^d   Boyden, Laurie ^e   Cade, Rebecca ^f   Chapman, Natalie H ^a   Fraser, Paul D ^g   Hodgman, Charlie ^a   Seymour, Graham B ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b NOTTINGHAM TRENT UNIVERSITY   (United Kingdom)

^c JEALOTT S HILL RESEARCH STATION   (United Kingdom)

^d Syngenta Seeds SAS   (France)

^e SYNGENTA CROP PROTECTION   (United States)

^f NATIONAL INSTITUTES OF HEALTH   (United States)

^g UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84874607142     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.212654     Document Type: Article

References (42)

1. Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot 53: 2039-2055
2. Barry CS, Aldridge GM, Herzog G, Ma Q, McQuinn RP, Hirschberg J, Giovannoni JJ (2012) Altered chloroplast development and delayed fruit ripening caused by mutations in a zinc metalloprotease at the lutescent2 locus of tomato. Plant Physiol 159: 1086-1098
3. Brand A, Borovsky Y, Meir S, Rogachev I, Aharoni A, Paran I (2012) pc8.1, a major QTL for pigment content in pepper fruit, is associated with variation in plastid compartment size. Planta 235: 579-588
4. Carvalho RF, Campos ML, Pino LE, Crestana SL, Zsögön A, Lima JE, Benedito VA, Peres LE (2011) Convergence of developmental mutants into a single tomato model system: 'Micro-Tom' as an effective toolkit for plant development research. Plant Methods 7: 18
5. 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
6. Davuluri GR, van Tuinen A, Mustilli AC, Manfredonia A, Newman R, Burgess D, Brummell DA, King SR, Palys J, Uhlig J, et al (2004) Manipulation of DET1 expression in tomato results in photomorphogenic phenotypes caused by post-transcriptional gene silencing. Plant J 40: 344-354
7. Enfissi EMA, Barneche F, Ahmed I, Lichtlé C, Gerrish C, McQuinn RP, Giovannoni JJ, Lopez-Juez E, Bowler C, Bramley PM, et al (2010) Integrative transcript and metabolite analysis of nutritionally enhanced DE-ETIOLATED1 downregulated tomato fruit. Plant Cell 22: 1190-1215
8. Fitter DW, Martin DJ, Copley MJ, Scotland RW, Langdale JA (2002) GLK gene pairs regulate chloroplast development in diverse plant species. Plant J 31: 713-727
9. Forth D, Pyke KA (2006) The suffulta mutation in tomato reveals a novel method of plastid replication during fruit ripening. J Exp Bot 57: 1971-1979
10. Fraser PD, Bramley PM (2004) The biosynthesis and nutritional uses of carotenoids. Prog Lipid Res 43: 228-265
11. Fraser PD, Pinto MES, Holloway DE, Bramley PM (2000) Technical advance: application of high-performance liquid chromatography with photodiode array detection to the metabolic profiling of plant isoprenoids. Plant J 24: 551-558
12. 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
13. Goff SA, Klee HJ (2006) Plant volatile compounds: sensory cues for health and nutritional value? Science 311: 815-819
14. 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
15. 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
16. Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45: 41-59
17. Kurup S, Jones HD, Holdsworth MJ (2000) Interactions of the developmental regulator ABI3 with proteins identified from developing Arabidopsis seeds. Plant J 21: 143-155
18. Lanahan MB, Yen HC, Giovannoni JJ, Klee HJ (1994) The never ripe mutation blocks ethylene perception in tomato. Plant Cell 6: 521-530
19. Lancashire L, Ugurel S, Creaser C, Schadendorf D, Rees R, Ball G (2005) Utilizing artificial neural networks to elucidate serum biomarker patterns which discriminate between clinical stages in melanoma. In Proceedings of the 2005 IEEE Symposium on Computational Intelligence in Bioinformatics and Computational Biology. pp 455-460
20. Lancashire LJ, Powe DG, Reis-Filho JS, Rakha E, Lemetre C, Weigelt B, Abdel-Fatah TM, Green AR, Mukta R, Blamey R, et al (2010) A validated gene expression profile for detecting clinical outcome in breast cancer using artificial neural networks. Breast Cancer Res Treat 120: 83-93
21. Lancashire LJ, Rees RC, Ball GR (2008) Identification of gene transcript signatures predictive for estrogen receptor and lymph node status using a stepwise forward selection artificial neural network modelling approach. Artif Intell Med 43: 99-111
22. Langley KR, Martin A, Stenning R, Murray AJ, Hobson GE, Schuch WW, Bird CR (1994) Mechanical and optical assessment of the ripening of tomato fruit with reduced polygalacturonase activity. J Sci Food Agric 66: 547-554
23. Lee JM, Joung JG, McQuinn R, Chung MY, Fei ZJ, 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. Plant J 70: 191-204
24. Lieberman M, Segev O, Gilboa N, Lalazar A, Levin I (2004) The tomato homolog of the gene encoding UV-damaged DNA binding protein 1 (DDB1) underlined as the gene that causes the high pigment-1 mutant phenotype. Theor Appl Genet 108: 1574-1581
25. Lin ZF, Hong YG, YinMG, Li CY, Zhang K, Grierson D (2008) A tomato HD-Zip homeobox protein, LeHB-1, plays an important role in floral organogenesis and ripening. Plant J 55: 301-310
26. Lippman ZB, Semel Y, Zamir D (2007) An integrated view of quantitative trait variation using tomato interspecific introgression lines. Curr Opin Genet Dev 17: 545-552
27. Liu YS, Gur A, Ronen G, Causse M, Damidaux R, Buret M, Hirschberg J, Zamir D (2003) There is more to tomato fruit colour than candidate carotenoid genes. Plant Biotechnol J 1: 195-207
28. Liu YS, Roof S, Ye ZB, Barry C, van Tuinen A, Vrebalov J, Bowler C, Giovannoni J (2004) Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc Natl Acad Sci USA 101: 9897-9902
29. 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. Nat Genet 38: 948-952
30. Matharoo-Ball B, Hughes C, Lancashire L, Tooth D, Ball G, Creaser C, Elgasim M, Rees R, Layfield R, Atiomo W (2007) Characterization of biomarkers in polycystic ovary syndrome (PCOS) using multiple distinct proteomic platforms. J Proteome Res 6: 3321-3328
31. Mustilli AC, Fenzi F, Ciliento R, Alfano F, Bowler C (1999) Phenotype of the tomato high pigment-2 mutant is caused by a mutation in the tomato homolog of DEETIOLATED1. Plant Cell 11: 145-157
32. Perochon A, Dieterle S, Pouzet C, Aldon D, Galaud JP, Ranty B (2010) Interaction of a plant pseudo-response regulator with a calmodulin-like protein. Biochem Biophys Res Commun 398: 747-751
33. Powell ALT, Nguyen CV, Hill T, Cheng KL, Figueroa-Balderas R, Aktas H, Ashrafi H, Pons C, Fernández-Muñoz R, Vicente A, et al (2012) Uniform ripening encodes a Golden 2-like transcription factor regulating tomato fruit chloroplast development. Science 336: 1711-1715
34. Rohrmann J, Tohge T, Alba R, Osorio S, Caldana C, McQuinn R, Arvidsson S, van der Merwe MJ, Riano-Pachon DM, Mueller-Roeber B, et al (2011) Combined transcription factor profiling, microarray analysis and metabolite profiling reveals the transcriptional control of metabolic shifts occurring during tomato fruit development. Plant J 68: 999-1013
35. Sun HJ, Uchii S, Watanabe S, Ezura H (2006) A highly efficient transformation protocol for Micro-Tom, a model cultivar for tomato functional genomics. Plant Cell Physiol 47: 426-431
36. Thorup TA, Tanyolac B, Livingstone KD, Popovsky S, Paran I, Jahn M (2000) Candidate gene analysis of organ pigmentation loci in the Solanaceae. Proc Natl Acad Sci USA 97: 11192-11197
37. Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635-641
38. Vrebalov J, Pan IL, Arroyo AJM, McQuinn R, Chung M, Poole M, Rose JKC, 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
39. 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
40. Wang SH, Liu JK, Feng YY, Niu XL, Giovannoni J, Liu YS (2008) Altered plastid levels and potential for improved fruit nutrient content by downregulation of the tomato DDB1-interacting protein CUL4. Plant J 55: 89-103
41. Waters MT, Moylan EC, Langdale JA (2008) GLK transcription factors regulate chloroplast development in a cell-autonomous manner. Plant J 56: 432-444
42. Waters MT, Wang P, Korkaric M, Capper RG, Saunders NJ, Langdale JA (2009) GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell 21: 1109-1128