Tomato MBD5, a methyl CpG binding domain protein, physically interacting with UV-damaged DNA binding protein-1, functions in multiple processes

New Phytologist

Volumn 210, Issue 1, 2016, Pages 208-226

  Li, Yuxiang ^a   Deng, Heng ^a   Miao, Min ^b   Li, Huirong ^a   Huang, Shengxiong ^b   Wang, Songhu ^c   Liu, Yongsheng ^a,b  

^a SICHUAN UNIVERSITY   (China)

^b HEFEI UNIVERSITY OF TECHNOLOGY   (China)

^c CHENGDU INSTITUTE OF BIOLOGY   (China)

Author keywords

MBD; Cullin4 (CUL4); De etiolated 1 (DET1); Fruit quality; High pigment; Plastid biogenesis; Tomato (Solanum lycopersicum); UV damaged DNA binding protein 1 (DDB1)

Indexed keywords

BIOASSAY; ELECTROKINESIS; FRUIT; GENE EXPRESSION; METHYLATION; MOBILITY; PIGMENT; PLASTID; PROTEIN;

LYCOPERSICON ESCULENTUM;

BENZYLOXYCARBONYLLEUCYL-LEUCYL-LEUCINE ALDEHYDE; DNA BINDING PROTEIN; LEUPEPTIN; PLANT PROTEIN; PROTEIN BINDING;

AMINO ACID SEQUENCE; CELL FRACTIONATION; CHEMISTRY; CPG ISLAND; DRUG EFFECTS; FRUIT; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; LIGHT; METABOLISM; METHYL-CPG-BINDING DOMAIN; PHENOTYPE; PIGMENTATION; PLANT DEVELOPMENT; PLASTID; PLEIOTROPY; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; RADIATION RESPONSE; SACCHAROMYCES CEREVISIAE; TOMATO; TRANSGENIC PLANT; UBIQUITINATION;

AMINO ACID SEQUENCE; CPG ISLANDS; DNA-BINDING PROTEINS; FRUIT; GENE EXPRESSION REGULATION, PLANT; GENETIC PLEIOTROPY; LEUPEPTINS; LIGHT; LYCOPERSICON ESCULENTUM; METHYL CPG BINDING DOMAIN; PHENOTYPE; PIGMENTATION; PLANT DEVELOPMENT; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PLASTIDS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; SUBCELLULAR FRACTIONS; TRANSCRIPTION, GENETIC; UBIQUITINATION;

EID: 84959091666     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13745     Document Type: Article

References (77)

1. Angers S, Li T, Yi X, MacCoss MJ, Moon RT, Zheng N. 2006. Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery. Nature 443: 590-593.
2. Azari R, Reuveni M, Evenor D, Nahon S, Shlomo H, Chen L, Levin I. 2010. Overexpression of UV-DAMAGED DNA BINDING PROTEIN 1 links plant development and phytonutrient accumulation in high pigment-1 tomato. Journal of Experimental Botany 61: 3627-3637.
3. Baubec T, Ivanek R, Lienert F, Schubeler D. 2013. Methylation-dependent and -independent genomic targeting principles of the MBD protein family. Cell 153: 480-492.
4. Benvenuto G, Formiggini F, Laflamme P, Malakhov M, Bowler C. 2002. The photomorphogenesis regulator DET1 binds the amino-terminal tail of histone H2B in a nucleosome context. Current Biology 12: 1529-1534.
5. Berg A, Meza TJ, Mahić M, Thorstensen T, Kristiansen K, Aalen RB. 2003. Ten members of the Arabidopsis gene family encoding methyl-CpG-binding domain proteins are transcriptionally active and at least one, AtMBD11, is crucial for normal development. Nucleic Acids Research 31: 5291-5304.
6. Bernhardt A, Lechner E, Hano P, Schade V, Dieterle M, Anders M, Dubin MJ, Benvenuto G, Bowler C, Genschik P. 2006. CUL4 associates with DDB1 and DET1 and its downregulation affects diverse aspects of development in Arabidopsis thaliana. Plant Journal 47: 591-603.
7. Caspi N, Levin I, Chamovitz DA, Reuveni M. 2014. A mutation in the tomato DDB1gene affects cell and chloroplast compartment size and CDT1 transcript. Plant Signaling & Behavior 3: 641-649.
8. Chahrour M, Jung SY, Shaw C, Zhou X, Wong ST, Qin J, Zoghbi HY. 2008. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320: 1224-1229.
9. Chen H, Shen Y, Tang X, Yu L, Wang J, Guo L, Zhang Y, Zhang H, Feng S, Strickland E. 2006. Arabidopsis CULLIN4 forms an E3 ubiquitin ligase with RBX1 and the CDD complex in mediating light control of development. Plant Cell 18: 1991-2004.
10. Chen J, Yang L, Gu J, Bai X, Ren Y, Fan T, Han Y, Jiang L, Xiao F, Liu Y. 2015. MAN3 gene regulates cadmium tolerance through the glutathione-dependent pathway in Arabidopsis thaliana. New Phytologist 205: 570-582.
11. Chen T, Lv Y, Zhao T, Li N, Yang Y, Yu W, He X, Liu T, Zhang B. 2013. Comparative transcriptome profiling of a resistant vs. susceptible tomato (Solanum lycopersicum) cultivar in response to infection by tomato yellow leaf curl virus. PLoS ONE 8: e80816.
12. Chinnusamy V, Zhu J-K. 2009. Epigenetic regulation of stress responses in plants. Current Opinion in Plant Biology 12: 133-139.
13. Uniprot Consortium. 2013. Update on activities at the Universal Protein Resource (UniProt) in 2013. Nucleic Acids Research 41: D43-D47.
14. Cookson P, Kiano J, Shipton C, Fraser P, Romer S, Schuch W, Bramley P, Pyke K. 2003. Increases in cell elongation, plastid compartment size and phytoene synthase activity underlie the phenotype of the high pigment-1 mutant of tomato. Planta 217: 896-903.
15. Davuluri GR, Van Tuinen A, Fraser PD, Manfredonia A, Newman R, Burgess D, Brummell DA, King SR, Palys J, Uhlig J. 2005. Fruit-specific RNAi-mediated suppression of DET1 enhances carotenoid and flavonoid content in tomatoes. Nature Biotechnology 23: 890-895.
16. Dhasarathy A, Wade PA. 2008. The MBD protein family-reading an epigenetic mark? Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 647: 39-43.
17. Dumbliauskas E, Lechner E, Jaciubek M, Berr A, Pazhouhandeh M, Alioua M, Cognat V, Brukhin V, Koncz C, Grossniklaus U. 2011. The Arabidopsis CUL4-DDB1 complex interacts with MSI1 and is required to maintain MEDEA parental imprinting. EMBO Journal 30: 731-743.
18. Enfissi EM, Barneche F, Ahmed I, Lichtle 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.
19. Fillatti JJ, Kiser J, Rose R, Comai L. 1987. Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector. Nature Biotechnology 5: 726-730.
20. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J. 2014. Pfam: the protein families database. Nucleic Acids Research 42: 222-230.
21. 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 Journal 53: 717-730.
22. He YJ, McCall CM, Hu J, Zeng Y, Xiong Y. 2006. DDB1 functions as a linker to recruit receptor WD40 proteins to CUL4-ROC1 ubiquitin ligases. Genes Development 20: 2949-2954.
23. Hu H, Yang Y, Ji Q, Zhao W, Jiang B, Liu R, Yuan J, Liu Q, Li X, Zou Y et al. 2012. CRL4B catalyzes H2AK119 monoubiquitination and coordinates with PRC2 to promote tumorigenesis. Cancer Cell 22: 781-795.
24. Huang W, Miao M, Kud J, Niu X, Ouyang B, Zhang J, Ye Z, Kuhl JC, Liu Y, Xiao F. 2013. SlNAC1, a stress-related transcription factor, is fine-tuned on both the transcriptional and the post-translational level. New Phytologist 197: 1214-1224.
25. Inamdar NM, Ehrlich KC, Ehrlich M. 1991. CpG methylation inhibits binding of several sequence-specific DNA-binding proteins from pea, wheat, soybean and cauliflower. Plant Molecular Biology 17: 111-123.
26. Ito M, Koike A, Koizumi N, Sano H. 2003. Methylated DNA-binding proteins from Arabidopsis. Plant Physiology 133: 1747-1754.
27. Jeltsch A. 2002. Beyond Watson and Crick: DNA methylation and molecular enzymology of DNA methyltransferases. ChemBioChem 3: 274-293.
28. Jin J, Arias EE, Chen J, Harper JW, Walter JC. 2006. A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Molecular Cell 23: 709-721.
29. Kilambi HV, Kumar R, Sharma R, Sreelakshmi Y. 2013. Chromoplast-specific carotenoid-associated protein appears to be important for enhanced accumulation of carotenoids in hp1 tomato fruits. Plant Physiology 161: 2085-2101.
30. Klose RJ, Bird AP. 2006. Genomic DNA methylation: the mark and its mediators. Trends in Biochemical Sciences 31: 89-97.
31. Koenig D, Jimenez-Gomez JM, Kimura S, Fulop D, Chitwood DH, Headland LR, Kumar R, Covington MF, Devisetty UK, Tat AV et al. 2013. Comparative transcriptomics reveals patterns of selection in domesticated and wild tomato. Proceedings of the National Academy of Sciences, USA 110: 2655-2662.
32. dg tomato mutant links early fruit plastid biogenesis with its overproduction of phytonutrients. Plant Physiology 145: 389-401.
33. Kosugi S, Hasebe M, Tomita M, Yanagawa H. 2009. Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proceedings of the National Academy of Sciences, USA 106: 10 171-10 176.
34. Lau OS, Huang X, Charron JB, Lee JH, Li G, Deng XW. 2011. Interaction of Arabidopsis DET1 with CCA1 and LHY in mediating transcriptional repression in the plant circadian clock. Molecular Cell 43: 703-712.
35. Lau OS, Deng XW. 2012. The photomorphogenic repressors COP1 and DET1: 20 years later. Trends in Plant Science 17: 584-593.
36. Lavi N, Tadmor Y, Meir A, Bechar A, Oren-Shamir M, Ovadia R, Reuveni M, Nahon S, Shlomo H, Chen L. 2009. Characterization of the intense pigment tomato genotype emphasizing targeted fruit metabolites and chloroplast biogenesis. Journal of Agricultural and Food Chemistry 57: 4818-4826.
37. Lee J-H, Yoon H-J, Terzaghi W, Martinez C, Dai M, Li J, Byun M-O, Deng XW. 2010. DWA1 and DWA2, two Arabidopsis DWD protein components of CUL4-based E3 ligases, act together as negative regulators in ABA signal transduction. Plant Cell 22: 1716-1732.
38. Letunic I, Doerks T, Bork P. 2012. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Research 40: 302-305.
39. Li T, Chen X, Garbutt KC, Zhou P, Zheng N. 2006. Structure of DDB1 in complex with a paramyxovirus V protein: viral hijack of a propeller cluster in ubiquitin ligase. Cell 124: 105-117.
40. Liu J, Tang X, Gao L, Gao Y, Li Y, Huang S, Sun X, Miao M, Zeng H, Tian X et al. 2012. A role of tomato UV-damaged DNA binding protein 1 (DDB1) in organ size control via an epigenetic manner. PLoS ONE 7: e42621.
41. Liu Y, Roof S, Ye Z, 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. Proceedings of the National Academy of Sciences, USA 101: 9897-9902.
42. Miao M, Zhu Y, Qiao M, Tang X, Zhao W, Xiao F, Liu Y. 2014. The tomato DWD motif-containing protein DDI1 interacts with the CUL4-DDB1-based ubiquitin ligase and plays a pivotal role in abiotic stress responses. Biochemical and Biophysical Research Communication 450: 1439-1445.
43. Moes D, Himmelbach A, Korte A, Haberer G, Grill E. 2008. Nuclear localization of the mutant protein phosphatase abi1 is required for insensitivity towards ABA responses in Arabidopsis. Plant Journal 54: 806-819.
44. 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.
45. Nadakuduti SS, Holdsworth WL, Klein CL, Barry CS. 2014. KNOX genes influence a gradient of fruit chloroplast development through regulation of GOLDEN2-LIKE expression in tomato. Plant Journal 78: 1022-1033.
46. Nguyen CV, Vrebalov JT, Gapper NE, Zheng Y, Zhong S, Fei Z, Giovannoni JJ. 2014. Tomato GOLDEN2-LIKE transcription factors reveal molecular gradients that function during fruit development and ripening. Plant Cell 26: 585-601.
47. Pazhouhandeh M, Molinier J, Berr A, Genschik P. 2011. MSI4/FVE interacts with CUL4-DDB1 and a PRC2-like complex to control epigenetic regulation of flowering time in Arabidopsis. Proceedings of the National Academy of Sciences, USA 108: 3430-3435.
48. Powell AL, 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.
49. Preuss SB, Costa-Nunes P, Tucker S, Pontes O, Lawrence RJ, Mosher R, Kasschau KD, Carrington JC, Baulcombe DC, Viegas W et al. 2008. Multimegabase silencing in nucleolar dominance involves siRNA-directed DNA methylation and specific methylcytosine-binding proteins. Molecular Cell 32: 673-684.
50. 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 Journal 68: 999-1013.
51. Scebba F, Bernacchia G, De Bastiani M, Evangelista M, Cantoni RM, Cella R, Locci MT, Pitto L. 2003. Arabidopsis MBD proteins show different binding specificities and nuclear localization. Plant Molecular Biology 53: 755-771.
52. Scebba F, De Bastiani M, Bernacchia G, Andreucci A, Galli A, Pitto L. 2007. PRMT11: a new Arabidopsis MBD7 protein partner with arginine methyltransferase activity. Plant Journal 52: 210-222.
53. Scrima A, Konickova R, Czyzewski BK, Kawasaki Y, Jeffrey PD, Groisman R, Nakatani Y, Iwai S, Pavletich NP, Thoma NH. 2008. Structural basis of UV DNA-damage recognition by the DDB1-DDB2 complex. Cell 135: 1213-1223.
54. Seymour GB, Ostergaard L, Chapman NH, Knapp S, Martin C. 2013. Fruit development and ripening. Annual Review of Plant Biology 64: 219-241.
55. Shi X, Gupta S, Lindquist IE, Cameron CT, Mudge J, Rashotte AM. 2013. Transcriptome analysis of cytokinin response in tomato leaves. PLoS ONE 8: e55090.
56. Springer NM, Kaeppler SM. 2005. Evolutionary divergence of monocot and dicot methyl-CpG-binding domain proteins. Plant Physiology 138: 92-104.
57. Tamura K, Peterson D, Peterson N, Stecher G. 2011. Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology & Evolution 28: 2731-2739.
58. Tang X, Tang Z, Huang S, Liu J, Liu J, Shi W, Tian X, Li Y, Zhang D, Yang J et al. 2013. Whole transcriptome sequencing reveals genes involved in plastid/chloroplast division and development are regulated by the HP1/DDB1 at an early stage of tomato fruit development. Planta 238: 923-936.
59. Voinnet O, Rivas S, Mestre P, Baulcombe D. 2003. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant Journal 33: 949-956.
60. Walter M, Chaban C, Schütze K, Batistic O, Weckermann K, Näke C, Blazevic D, Grefen C, Schumacher K, Oecking C. 2004. Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant Journal 40: 428-438.
61. Wang F, Zhu D, Huang X, Li S, Gong Y, Yao Q, Fu X, Fan L-M, Deng XW. 2009. Biochemical insights on degradation of Arabidopsis DELLA proteins gained from a cell-free assay system. Plant Cell 21: 2378-2390.
62. Wang H, Zhai L, Xu J, Joo HY, Jackson S, Erdjument-Bromage H, Tempst P, Xiong Y, Zhang Y. 2006. Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Molecular Cell 22: 383-394.
63. Wang S, Liu J, Feng Y, Niu X, Giovannoni J, Liu Y. 2008. Altered plastid levels and potential for improved fruit nutrient content by downregulation of the tomato DDB1-interacting protein CUL4. Plant Journal 55: 89-103.
64. Wang Y, Tao X, Tang X-M, Xiao L, J-l Sun, Yan X-F, Li D, Deng H-Y, Ma X-R. 2013. Comparative transcriptome analysis of tomato (Solanum lycopersicum) in response to exogenous abscisic acid. BMC Genomics 14: 841.
65. Wertz IE, O'Rourke KM, Zhang Z, Dornan D, Arnott D, Deshaies RJ, Dixit VM. 2004. Human De-etiolated-1 regulates c-Jun by assembling a CUL4A ubiquitin ligase. Science 303: 1371-1374.
66. Yaish MW, Peng M, Rothstein SJ. 2009. AtMBD9 modulates Arabidopsis development through the dual epigenetic pathways of DNA methylation and histone acetylation. Plant Journal 59: 123-135.
67. Yang Y, Liu R, Qiu R, Zheng Y, Huang W, Hu H, Ji Q, He H, Shang Y, Gong Y et al. 2015. CRL4B promotes tumorigenesis by coordinating with SUV39H1/HP1/DNMT3A in DNA methylation-based epigenetic silencing. Oncogene 34: 104-118.
68. Yoo SD, Cho YH, Sheen J. 2007. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature Protocols 2: 1565-1572.
69. Zemach A, Gaspan O, Grafi G. 2008. The three methyl-CpG-binding domains of AtMBD7 control its subnuclear localization and mobility. Journal of Biological Chemistry 283: 8406-8411.
70. Zemach A, Grafi G. 2003. Characterization of Arabidopsis thaliana methyl-CpG-binding domain (MBD) proteins. Plant Journal 34: 565-572.
71. Zemach A, Grafi G. 2007. Methyl-CpG-binding domain proteins in plants: interpreters of DNA methylation. Trends in Plant Science 12: 80-85.
72. Zemach A, Li Y, Wayburn B, Ben-Meir H, Kiss V, Avivi Y, Kalchenko V, Jacobsen SE, Grafi G. 2005. DDM1 binds Arabidopsis methyl-CpG binding domain proteins and affects their subnuclear localization. Plant Cell 17: 1549-1558.
73. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW-L, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE. 2006. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126: 1189-1201.
74. Zhang Y, Feng S, Chen F, Chen H, Wang J, McCall C, Xiong Y, Deng XW. 2008. Arabidopsis DDB1-CUL4 ASSOCIATED FACTOR1 forms a nuclear E3 ubiquitin ligase with DDB1 and CUL4 that is involved in multiple plant developmental processes. Plant Cell 20: 1437-1455.
75. Zhao R, Han C, Eisenhauer E, Kroger J, Zhao W, Yu J, Selvendiran K, Liu X, Wani AA, Wang QE. 2014. DNA damage-binding complex recruits HDAC1 to repress Bcl-2 transcription in human ovarian cancer cells. Molecular Cancer Research 12: 370-380.
76. Zhong S, Fei Z, Chen YR, Zheng Y, Huang M, Vrebalov J, McQuinn R, Gapper N, Liu B, Xiang J et al. 2013. Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nature Biotechnology 31: 154-159.
77. Zouari I, Salvioli A, Chialva M, Novero M, Miozzi L, Tenore GC, Bagnaresi P, Bonfante P. 2014. From root to fruit: RNA-Seq analysis shows that arbuscular mycorrhizal symbiosis may affect tomato fruit metabolism. BMC Genomics 15: 221.