Post-translational regulation of rice MADS29 function: Homodimerization or binary interactions with other seedexpressed MADS proteins modulate its translocation into the nucleus

Journal of Experimental Botany

Volumn 65, Issue 18, 2014, Pages 5339-5350

  Nayar, Saraswati ^a   Kapoor, Meenu ^b   Kapoor, Sanjay ^a  

^a UNIVERSITY OF DELHI   (India)

^b GURU GOBIND SINGH INDRAPRASTHA UNIVERSITY   (India)

Author keywords

MADS box; Nuclear localization; Protein protein interaction; Rice; Seed; Transcription factor

Indexed keywords

VEGETABLE PROTEIN;

CELL NUCLEUS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PLANT SEED; PROTEIN TRANSPORT; RICE;

CELL NUCLEUS; GENE EXPRESSION REGULATION, PLANT; ORYZA SATIVA; PLANT PROTEINS; PROTEIN TRANSPORT; SEEDS;

EID: 84921307799     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru296     Document Type: Article

References (57)

1. Agrawal GK, Abe K, Yamazaki M, Miyao A, Hirochika H. 2005. Conservation of the E-function for floral organ identity in rice revealed by the analysis of tissue culture-induced loss-of-function mutants of the OsMADS1 gene. Plant Molecular Biology 59, 125-135.
2. Arora R, Agarwal P, Ray S, Singh AK, Singh VP, Tyagi AK, Kapoor S. 2007. MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8, 242.
3. Baisamy L. 2005. Leucine zipper-mediated homo-oligomerization regulates the rho-GEF activity of AKAP-Lbc. Journal of Biological Chemistry 280, 15405-15412.
4. Becker A, Theißen G. 2003. The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Molecular Phylogenetics and Evolution 29, 464-489.
5. Chida K, Nagamori S, Kuroki T. 1999. Nuclear translocation of Fos is stimulated by interaction with Jun through the leucine zipper. Cellular and Molecular Life Sciences 55, 297-302.
6. Cui R, Han J, Zhao S, Su K, Wu F, Du X, Xu Q, Chong K, Theißen G, Meng Z. 2010. Functional conservation and diversification of class E floral homeotic genes in rice (Oryza sativa). The Plant Journal 61, 767-781.
7. De Folter S, Immink RGH, Kieffer M, et al. 2005. Comprehensive interaction map of the Arabidopsis MADS box transcription factors. The Plant Cell 17, 1424-1433.
8. Duan Y, Xing Z, Diao Z, et al. 2012. Characterization of Osmads6-5, a null allele, reveals that OsMADS6 is a critical regulator for early flower development in rice (Oryza sativa L.). Plant Molecular Biology 80, 429-442.
9. Ferrario S, Busscher J, Franken J, Gerats T, Vandenbussche M, Angenent GC, Immink RGH. 2004. Ectopic expression of the petunia MADS box gene UNSHAVEN accelerates flowering and confers leaf-like characteristics to floral organs in a dominant-negative manner. The Plant Cell 16, 1490-1505.
10. Gao X, Liang W, Yin C, Ji S, Wang H, Su X, Guo C, Kong H, Xue H, Zhang D. 2010. The SEPALLATA-like gene OsMADS34 is required for rice inflorescence and spikelet development. Plant Physiology 153, 728-740.
11. Gramzow L, Theissen G. 2010. A hitchhiker's guide to the MADS world of plants. Genome Biology 11, 214.
12. Gu H, Zhu P, Jiao Y, Meng Y, Chen M. 2011. PRIN: A predicted rice interactome network. BMC Bioinformatics 12, 161.
13. Ho C-L, Wu Y, Shen H-B, Provart NJ, Geisler M. 2012. A predicted protein interactome for rice. Rice 5, 15-14.
14. Horton P, Park K-J, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K. 2007. WoLF PSORT: Protein localization predictor. Nucleic Acids Research 35, W585-W587.
15. Howell JM, Winstone TL, Coorssen JR, Turner RJ. 2006. An evaluation of in vitro protein-protein interaction techniques: Assessing contaminating background proteins. Proteomics 6, 2050-2069.
16. Immink RGH, Gadella TWJ, Ferrario S, Busscher M, Angenent GC. 2002. Analysis of MADS box protein-protein interactions in living plant cells. Proceedings of the National Academy of Sciences, USA 99, 2416-2421.
17. Immink RGH, Kaufmann K, Angenent GC. 2010. The 'ABC'of MADS domain protein behaviour and interactions. Seminars in Cell and Developmental Biology 21, 87-93.
18. Immink RGH, Tonaco IAN, de Folter S, Shchennikova A, van Dijk ADJ, Busscher-Lange J, Borst JW, Angenent GC. 2009. SEPALLATA3: The 'glue' for MADS box transcription factor complex formation. Genome Biology 10, R24.
19. Jeon JS, Jang S, Lee S, et al. 2000. leafy hull sterile1 is a homeotic mutation in a rice MADS box gene affecting rice flower development. The Plant Cell 12, 871-884.
20. Jia H, Chen R, Cong B, Cao K, Sun C, Luo D. 2000. Characterization and transcriptional profiles of two rice MADS-box genes. Plant Science 155, 115-122.
21. Jiang CJ, Shoji K, Matsuki R, et al. 2001. Molecular cloning of a novel importin alpha homologue from rice, by which constitutive photomorphogenic 1 (COP1) nuclear localization signal (NLS)-protein is preferentially nuclear imported. The Journal of Biological Chemistry 276, 9322-9329.
22. Kang HG, Jang S, Chung JE, Cho YG, An G. 1997. Characterization of two rice MADS box genes that control flowering time. Molecules and Cells 7, 559-566.
23. Kater MM, Dreni L, Colombo L. 2006. Functional conservation of MADS-box factors controlling floral organ identity in rice and Arabidopsis. Journal of Experimental Botany 57, 3433-3444.
24. Kobayashi K, Maekawa M, Miyao A, Hirochika H, Kyozuka J. 2010. PANICLE PHYTOMER2 (PAP2), encoding a SEPALLATA subfamily MADSbox protein, positively controls spikelet meristem identity in rice. Plant and Cell Physiology 51, 47-57.
25. Lange A, Mills RE, Lange CJ, Stewart M, Devine SE, Corbett AH. 2007. Classical nuclear localization signals: definition, function, and interaction with importin alpha. The Journal of Biological Chemistry 282, 5101-5105.
26. Lee J, Oh M, Park H, Lee I. 2008a. SOC1 translocated to the nucleus by interaction with AGL24 directly regulates leafy. The Plant Journal 55, 832-843.
27. Lee JH, Park SH, Ahn JH. 2012. Functional conservation and diversification between rice OsMADS22/OsMADS55 and Arabidopsis SVP proteins. Plant Science 185-186, 97-104.
28. Lee L-Y, Fang M-J, Kuang L-Y, Gelvin SB. 2008b. Vectors for multicolor bimolecular fluorescence complementation to investigate protein- protein interactions in living plant cells. Plant Methods 4, 24.
29. Lee S, Woo YM, Ryu SI, Shin YD, Kim WT, Park KY, Lee IJ, An G. 2008c. Further Characterization of a Rice AGL12 Group MADS-Box Gene, OsMADS26. Plant Physiology 147, 156-168.
30. Li H, Liang W, Jia R, Yin C, Zong J, Kong H, Zhang D. 2010. The AGL6-like gene OsMADS6 regulates floral organ and meristem identities in rice. Cell Research 20, 299-313.
31. Li H, Liang W, Yin C, Zhu L, Zhang D. 2011. Genetic interaction of OsMADS3, DROOPING LEAF, and OsMADS13 in specifying rice floral organ identities and meristem determinacy. Plant Physiology 156, 263-274.
32. Lim J, Moon YH, An G, Jang SK. 2000. Two rice MADS domain proteins interact with OsMADS1. Plant Molecular Biology 44, 513-527.
33. Marchler-Bauer A, Lu S, Anderson JB, et al. 2011. CDD: A conserved domain database for the functional annotation of proteins. Nucleic Acids Research 39, 225-9.
34. McGonigle B, Bouhidel K, Irish VF. 1996. Nuclear localization of the Arabidopsis APETALA3 and PISTILLATA homeotic gene products depends on their simultaneous expression. Genes and Development 10, 1812-1821.
35. Miernyk JA, Thelen JJ. 2008. Biochemical approaches for discovering protein-protein interactions. The Plant Journal 53, 597-609.
36. Moon YH, Kang HG, Jung JY, Jeon JS, Sung SK, An G. 1999. Determination of the motif responsible for interaction between the rice APETALA1/AGAMOUS-LIKE9 family proteins using a yeast two-hybrid system. Plant Physiology 120, 1193-1204.
37. Nagoshi E, Yoneda Y. 2001. Dimerization of sterol regulatory elementbinding protein 2 via the helix-loop-helix-leucine zipper domain is a prerequisite for its nuclear localization mediated by importin beta. Molecular and Cellular Biology 21, 2779-2789.
38. Nayar S, Sharma R, Tyagi AK, Kapoor S. 2013. Functional delineation of rice MADS29 reveals its role in embryo and endosperm development by affecting hormone homeostasis. Journal of Experimental Botany 64, 4239-4253.
39. Ohmori S, Kimizu M, Sugita M, Miyao A, Hirochika H, Uchida E, Nagato Y, Yoshida H. 2009. MOSAIC FLORAL ORGANS1, an AGL6-like MADS box gene, regulates floral organ identity and meristem fate in rice. The Plant Cell 21, 3008-3025.
40. Pawson T, Nash P. 2003. Assembly of cell regulatory systems through protein interaction domains. Science Signaling 300, 445.
41. Piehler J. 2005. New methodologies for measuring protein interactions in vivo and in vitro. Current Opinion in Structural Biology 15, 4-14.
42. Prasad K, P S, Kumar S, Kushalappa K, Vijayraghavan U. 2001. Ectopic expression of rice OsMADS1 reveals a role in specifying the lemma and palea, grass floral organs analogous to sepals. Development Genes and Evolution 211, 281-290.
43. Prasad K, Parameswaran S, Vijayraghavan U. 2005. OsMADS1, a rice MADS-box factor, controls differentiation of specific cell types in the lemma and palea and is an early-acting regulator of inner floral organs. The Plant Journal 43, 915-928.
44. Roy A, Kucukural A, Zhang Y. 2010. I-TASSER: A unified platform for automated protein structure and function prediction. Nature Protocols 5, 725-738.
45. Roy A, Yang J, Zhang Y. 2012. COFACTOR: An accurate comparative algorithm for structure-based protein function annotation. Nucleic Acids Research 40, 471-7.
46. Ryu C-H, Lee S, Cho L-H, et al. 2009. OsMADS50 and OsMADS56 function antagonistically in regulating long day (LD)-dependent flowering in rice. Plant, Cell and Environment 32, 1412-1427.
47. Sridhar VV, Surendrarao A, Liu Z. 2006. APETALA1 and SEPALLATA3 interact with SEUSS to mediate transcription repression during flower development. Development 133, 3159-3166.
48. Theißen G, Saedler H. 2001. Plant biology: floral quartets. Nature 409, 469-471.
49. Tonaco IAN, Borst JW, de Vries SC, Angenent GC, Immink RGH. 2006. In vivo imaging of MADS-box transcription factor interactions. Journal of Experimental Botany 57, 33-42.
50. van Dijk, ADJ, Morabito G, Fiers M, van Ham, RCHJ, Angenent GC, Immink RGH. 2010. Sequence motifs in MADS transcription factors responsible for specificity and diversification of protein-protein interaction (C Ouzounis, Ed.). PLoS Computational Biology 6, e1001017.
51. Yang X, Wu F, Lin X, Du X, Chong K, Gramzow L, Schilling S, Becker A, Theißen G, Meng Z. 2012. Live and let die-the B(sister) MADS-box gene OsMADS29 controls the degeneration of cells in maternal tissues during seed development of rice (Oryza sativa). PLoS One 7, e51435.
52. Yang Y, Jack T. 2004. Defining subdomains of the K domain important for protein-protein interactions of plant MADS proteins. Plant Molecular Biology 55, 45-59.
53. Yang Y, Fanning L, Jack T. 2003. The K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3 and PISTILLATA. The Plant Journal 33, 47-59.
54. Yin L-L, Xue H-W. 2012. The MADS29 transcription factor regulates the degradation of the nucellus and the nucellar projection during rice seed development. The Plant Cell 24, 1049-1065.
55. Zhang D, Yuan Z, An G, Dreni L, Hu J, Kater MM. 2013. Panicle development. In: Zhang Q, Wing R, eds. Genetics and genomics of rice . New York: Springer, 279-295.
56. Zhang J, Nallamilli BR, Mujahid H, Peng Z. 2010. OsMADS6 plays an essential role in endosperm nutrient accumulation and is subject to epigenetic regulation in rice (Oryza sativa). The Plant Journal 64, 604-617.
57. Zhong S, Lin Z, Fray RG, Grierson D. 2008. Improved plant transformation vectors for fluorescent protein tagging. Transgenic Research 17, 985-989.