BBX32 Interacts with AGL24 Involved in Flowering Time Control in Chinese Cabbage (Brassica rapa L. ssp. pekinensis)
B-box (BBX) zinc finger proteins play critical roles in both vegetative and reproductive development in plants. Many BBX proteins have been identified in Arabidopsis thaliana as floral transition regulatory factors, such as CO, BBX7 (COL9), BBX19, and BBX32. BBX32 is involved in flowering time control through repression of COL3 in Arabidopsis thaliana, but it is still elusive that whether and how BBX32 directly interacts with flowering signal integrators of AGAMOUS-LIKE 24 (AGL24) and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) in Chinese cabbage (Brassica rapa L. ssp. pekinensis) or other plants. In this study, B-box-32(BBX32), a transcription factor in this family with one B-box motif was cloned from B. rapa, acted as a circadian clock protein, showing expression changes during the circadian period. Additional experiments using GST pull-down and yeast two-hybrid assays indicated that BrBBX32 interacts with BrAGL24 and does not interact with BrSOC1, while BrAGL24 does interact with BrSOC1. To investigate the domains involved in these protein-protein interactions, we tested three regions of BrBBX32. Only the N-terminus interacted with BrAGL24, indicating that the B-box domain may be the key region for protein interaction. Based on these data, we propose that BrBBX32 may act in the circadian clock pathway and relate to the mechanism of flowering time regulation by binding to BrAGL24 through the B-box domain. This study will provide valuable information for unraveling the molecular regulatory mechanisms of BrBBX32 in flowering time of B. rapa.
Andrés F, Coupland G (2012). The genetic basis of flowering responses to seasonal cues. Nature Reviews Genetics 13(9):627.
Bluemel M, Dally N, Jung C (2015). Flowering time regulation in crops – what did we learn from Arabidopsis?. Current Opinion in Biotechnology 32:121-129.
Boss PK, Bastow RM, Mylne JS, Dean C (2004). Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16(Suppl 1): S18-S31.
Cao S, Kumimoto RW, Gnesutta N, Calogero AM, Mantovani R, Holt BF (2014). A distal CCAAT/NUCLEAR FACTOR Y complex promotes chromatin looping at the FLOWERING LOCUS T promoter and regulates the timing of flowering in Arabidopsis. Plant Cell 26(3):1009-1017.
Cheng XF, Wang ZY (2005). Overexpression of COL9, a CONSTANS-LIKE gene, delays flowering by reducing expression of CO and FT in Arabidopsis thaliana. The Plant Journal 43(5):758-768.
Crocco CD, Botto JF (2013). BBX proteins in green plants: Insights into their evolution, structure, feature and functional diversification. Gene 531(1):44-52.
Datta S, Hettiarachchi GH, Deng XW, Holm M (2006). Arabidopsis CONSTANS-LIKE3 is a positive regulator of red light signaling and root growth. Plant Cell 18(1):70-84.
de Folter S, Immink RG, Kieffer M, Pa?enicová L, Henz SR, Weigel D, … Davies B (2005). Comprehensive interaction map of the Arabidopsis MADS box transcription factors. Plant Cell 17(5):1424-1433.
Gangappa SN, Botto JF (2014). The BBX family of plant transcription factors. Trends in Plant Science 19(7):460-470.
Hassidim M, Harir Y, Yakir E, Kron I, Green RM (2009). Over-expression of CONSTANS-LIKE 5 can induce flowering in short-day grown Arabidopsis. Planta 230(3):481-491.
Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K (2003). Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422(6933):719-722.
He Y, Amasino RM (2005). Role of chromatin modification in flowering-time control. Trends in Plant Science 10:30-35.
Helliwell C A, Wood CC, Robertson M, James Peacock W, Dennis ES (2006). The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex. The Plant Journal 46(2):183-192.
Hepworth SR, Valverde F, Ravenscroft D, Mouradov A, Coupland G (2002). Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. The EMBO Journal 21(16):4327-4337.
Holtan HE, Bandong S, Marion CM, Adam L, Tiwari S, Shen Y, . . . Meister R (2011). BBX32, An Arabidopsis B-box protein, functions in light signaling by suppressing HY5-regulated gene expression and interacting with STH2/BBX21. Plant Physiology 156(4):2109-2123.
Huang J, Zhao X, Weng X, Wang L, Xie W (2012). The rice B-box zinc finger gene family: Genomic identification, characterization, expression profiling and diurnal analysis. PLoS One 7(10):e48242.
Huang XY, Tao P, Li BY, Wang WH, Yue, ZC, Lei JL, … Zhong XM (2015). Genome-wide identification, classification, and analysis of heat shock transcription factor family in Chinese cabbage (Brassica rapa pekinensis). Genetics and Molecular Research 14(1):2189-2204.
Khanna R, Kronmiller B, Maszle DR, Coupland G, Holm M, Mizuno T, … Wu SH (2009). The Arabidopsis B-box zinc finger family. Plant Cell 21(11):3416-3420.
Lee H, Suh SS, Park E, Cho E, Ahn JH, Kim SG, Lee JS, Kwon YM, Lee I (2000). The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes & Development 14(18):2366-2376.
Lee J, Lee I (2010). Regulation and function of SOC1, a flowering pathway integrator. Journal of Experimental Botany 61(9):2247-2254.
Li F, Sun J, Wang D, Bai S, Clarke AK, Holm M (2014). The B-box family gene STO (BBX24) in Arabidopsis thaliana regulates flowering time in different pathways. PLoS One 9(2):e87544.
Liu C, Chen H, Er HL, Soo HM, Kumar PP, Han JH, Liou YC, Yu H (2008). Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis. Development 135(8):1481-1491.
Liu J, Zhang H, Lian X, Converse R, Zhu L (2016). Identification of interacting motifs between armadillo repeat containing 1 (ARC1) and Exocyst 70 A1 (Exo70A1) proteins in Brassica oleracea. The Protein Journal 35(1):34-43.
Liu J, Liu B, Cheng F, Liang J, Wang X, … Wu J (2016). A high density linkage map facilitates QTL mapping of flowering time in Brassica rapa. Horticultural Plant Journal 2(4):217-223.
Mateos JL, Madrigal P, Tsuda K, Rawat V, Richter R, Romera-Branchat M, … Coupland G (2015). Combinatorial activities of SHORT VEGETATIVE PHASE and FLOWERING LOCUS C define distinct modes of flowering regulation in Arabidopsis. Genome Biology 16(1):31.
Melzer S, Lens F, Gennen J, Vanneste S, Rohde A, Beeckman T (2008). Flowering-time genes modulate meristem determinacy and growth form in Arabidopsis thaliana. Nature Genetics 40(12):1489.
Michaels SD, Ditta G, Gustafson-Brown C, Pelaz S, Yanofsky M, Amasino RM (2003). AGL24 acts as a promoter of flowering in Arabidopsis and is positively regulated by vernalization. The Plant Journal 33(5):867-874.
Moon J, Suh SS, Lee H, Choi KR, Hong CB, Paek NC, … Lee I (2003). The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. The Plant Journal 35(5):613-623.
Parcy F (2004). Flowering: a time for integration. International Journal of Developmental Biology 49(5-6):585-593.
Park HY, Lee SY, Seok HY, Kim SH, Sung ZR, Moon YH (2011). EMF1 interacts with EIP1, EIP6 or EIP9 involved in the regulation of flowering time in Arabidopsis. Plant and Cell Physiology 52(8):1376-1388.
Preuss SB, Meister R, Xu Q, Urwin CP, Tripodi FA, Screen SE, … Ratcliffe OJ (2012). Expression of the Arabidopsis thaliana BBX32 gene in soybean increases grain yield. PLoS One 7(2):e30717.
Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000). Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288(5471):1613-1616.
Sasaki E, Frommlet F, Nordborg M (2017). The genetic architecture of the network underlying flowering time variation in Arabidopsis thaliana. BioRxiv 175430.
Seo E, Lee H, Jeon J, Park H, Kim J, Noh YS, Lee I (2009). Crosstalk between cold response and flowering in Arabidopsis is mediated through the flowering-time gene SOC1 and its upstream negative regulator FLC. Plant Cell 21:3185-3197.
Shore P, Sharrocks AD (1995). The MADS-box family of transcription factors. European Journal of Biochemistry 229(1):1-13.
Song YH, Shim JS, Kinmonth-Schultz HA, Imaizumi T (2015a). Photoperiodic flowering: time measurement mechanisms in leaves. Annual Review of Plant Biology 66:441-464.
Song MF, Zhang S, Hou P, Shang HZ, Gu HK, Li JJ, … Yang JP (2015b). Ectopic expression of a phytochrome B gene from Chinese cabbage (Brassica rapa L. ssp. pekinensis) in Arabidopsis thaliana promotes seedling de-etiolation, dwarfing in mature plants, and delayed flowering. Plant Molecular Biology 87(6):633-643.
Suárez-López P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001). CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410(6832):1116.
Theißen G, Melzer R, Rümpler F (2016). MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution. Development 143(18):3259-3271.
Tripathi P, Carvallo M, Hamilton EE, Preuss S, Kay SA (2017). Arabidopsis B-BOX32 interacts with CONSTANS-LIKE3 to regulate flowering. Proceedings of the National Academy of Sciences 114(1):172-177.
Valverde F (2011). CONSTANS and the evolutionary origin of photoperiodic timing of flowering. Journal of Experimental Botany 62(8):2453-2463.
Valentim FL, van Mourik S, Posé D, Kim MC, Schmid M, van Ham RC, … Immink RG (2015). A quantitative and dynamic model of the Arabidopsis flowering time gene regulatory network. PLoS One 10(2):e0116973.
Wang CQ, Guthrie C, Sarmast MK, Dehesh, K (2014). BBX19 interacts with CONSTANS to repress FLOWERING LOCUS T transcription, defining a flowering time checkpoint in Arabidopsis. Plant Cell 26(9):3589-3602.
Weller JL, Hecht V, Vander Schoor JK, Davidson SE, Ross JJ (2009). Light regulation of gibberellin biosynthesis in pea is mediated through the COP1/HY5 pathway. Plant Cell 21(1):800-813.
Yoo SK, Chung KS, Kim J, Lee JH, Hong SM, Yoo SJ, . . . Ahn JH (2005). CONSTANS activates SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 through FLOWERING LOCUS T to promote flowering in Arabidopsis. Plant Physiology 139(2):770-778.
Yu H, Xu Y, Tan EL, Kumar PP (2002). AGAMOUS-LIKE 24, a dosage-dependent mediator of the flowering signals. Proceedings of the National Academy of Sciences 99(25):16336-16341.
Yu H, Ito T, Wellmer F, Meyerowitz EM (2004). Repression of AGAMOUS-LIKE 24 is a crucial step in promoting flower development. Nature Genetics 36(2):157.
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