Abstract
Key message
PvMADS56 may regulate the flowering time, the identity of floral organs, and the development of leaves.
Abstract
As a floral activator, SUPPRESSOR OF OVEREXPRESSION OF CO1/AGAMOUS-LIKE 20 (SOC1/AGL20) gene plays a key role in the flowering pathway of Arabidopsis. Bamboo MADS box gene PvMADS56, a homolog of SOC1/AGL20, was cloned from Phyllostachys violascens. Sequence comparison and phylogenetic analysis showed that PvMADS56 was closely related to MADS56-like proteins, which are the members of SOC1-like family. PvMADS56 was widely expressed in all the tested tissues of flowering and non-flowering bamboo plants, and its function was investigated by ectopic expression in transgenic Arabidopsis plants. The results showed that the overexpression promoted flowering in wild-type Arabidopsis and complemented the delayed flowering phenotype of soc1 Arabidopsis. Meanwhile the transgenic plants displayed abnormal floral organs and leaves, low fertility and dwarfism. Overexpression of PvMADS56 in the wild-type Arabidopsis not only caused early flowering by upregulating Flowering Locus T and downregulating Flowering Locus C expression, but also led to abnormal floral organs by downregulating APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Furthermore, PvMADS56 might be a nuclear protein, and interacted with PvAP1 and PvSEP3 from P. violascens in the yeast two-hybrid assay. In addition, the activity of PvMADS56 promoter was enhanced by exogenous abscisic acid (ABA) and methyl jasmonate (MeJA). Taken together, PvMADS56 may be a multifunctional gene that not only regulates the flowering time but also involves in the identity of floral organs in response to ABA and MeJA.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Borner R, Kampmann G, Chandler J, Gleißner R, Wisman E, Apel K, Melzer S (2000) A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J 24:591–599. doi:10.1046/j.1365-313x.2000.00906.x
Bowman JL, Alvarez J, Weigel D, Meyerowitz EM, Smyth DR (1993) Control of flower development in Arabidopsis thaliana by APETALA 1 and interacting genes. Development 119:721–743
Brambilla V, Fornara F (2013) Molecular control of flowering in response to day length in rice. J Integr Plant Biol 55:410–418. doi:10.1111/jipb.12033
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. doi:10.1046/j.1365-313x.1998.00343.x
Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37
Conti L, Galbiati M, Tonelli C (2014) ABA and the floral transition. In: Zhang DP (ed) Abscisic acid: metabolism, transport and signaling. Springer, The Netherlands, pp 365–384
Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033. doi:10.1126/science.1141752
Cseke LJ, Zheng J, Podila GK (2003) Characterization of PTM5 in aspen trees: a MADS-box gene expressed during woody vascular development. Gene 318:55–67. doi:10.1016/S0378-1119(03)00765-0
de Folter S, Immink RG, Kieffer M, Pařenicová L, Henz SR, Weigel D et al (2005) Comprehensive interaction map of the Arabidopsis MADS box transcription factors. Plant Cell 17:1424–1433. doi:10.1105/tpc.105.031831
Diallo AO, Agharbaoui Z, Badawi MA, Ali-Benali MA, Moheb A, Houde M, Sarhan F (2014) Transcriptome analysis of an mvp mutant reveals important changes in global gene expression and a role for methyl jasmonate in vernalization and flowering in wheat. J Exp Bot 65:2271–2286. doi:10.1093/jxb/eru102
Ding L, Wang Y, Yu H (2013) Overexpression of DOSOC1, an ortholog of Arabidopsis SOC1, promotes flowering in the orchid Dendrobium Chao Parya Smile. Plant Cell Physiol 54:595–608. doi:10.1093/pcp/pct026
Ferrario S, Busscher J, Franken J, Gerats T, Vandenbussche M, Angenent GC, Immink RG (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. Plant Cell 16:1490–1505. doi:10.1105/tpc.019679
Fu J, Qi S, Yang L, Dai Y, Dai S (2014) Characterization of chrysanthemum ClSOC1-1 and ClSOC1-2, homologous genes of SOC1. Plant Mol Biol Rep 32:740–749. doi:10.1007/s11105-013-0679-8
Gao J, Zhang Y, Zhang C, Qi F, Li X, Mu S, Peng Z (2014) Characterization of the floral transcriptome of Moso bamboo (Phyllostachys edulis) at different flowering developmental stages by transcriptome sequencing and RNA-seq analysis. PLoS One 9:e98910. doi:10.1371/journal.pone.0098910
Gao J, Ge W, Zhang Y, Cheng ZC, Li L, Hou D (2015) Identification and characterization of micrornas at different flowering developmental stages in moso bamboo (Phyllostachys edulis) by high-throughput sequencing. MGG 290:1–19. doi:10.1007/s00438-015-1069-8
Gietz D, St Jean A, Woods RA, Schiestl RH (1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res 20:1425
Helliwell CA, 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. Plant J 46:183–192. doi:10.1111/j.1365-313X.2006.02686.x
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. EMBO J 21:4327–4337. doi:10.1093/emboj/cdf432
Hong SM, Bahn SC, Lyu A, Jung HS, Ahn JH (2010) Identification and testing of superior reference genes for a starting pool of transcript normalization in Arabidopsis. Plant Cell Physiol 51:1694–1706. doi:10.1093/pcp/pcq128
Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409:525–529. doi:10.1038/35054083
Jack T (2004) Molecular and genetic mechanisms of floral control. Plant Cell 16(suppl 1):S1–S17. doi:10.1105/tpc.017038
Janzen DH (1976) Why bamboos wait so long to flower? Ann Rev Ecol Syst 7:347–391
Jarillo JA, Piñeiro M (2011) Timing is everything in plant development. The central role of floral repressors. Plant science 181:364–378. doi:10.1016/j.plantsci.2011.06.011
Keeley JE, Bond WJ (1999) Mast flowering and semelparity in bamboos: the bamboo fire cycle hypothesis. Am Nat 154:383–391. doi:10.1086/303243
Kimura Y, Aoki S, Ando E, Kitatsuji A, Watanabe A, Ohnishi M et al (2015) A flowering integrator, SOC1, affects stomatal opening in Arabidopsis thaliana. Plant Cell Physiol 56:640–649. doi:10.1093/pcp/pcu214
Lee J, Lee I (2010) Regulation and function of SOC1, a flowering pathway integrator. J Exp Bot 61:2247–2254. doi:10.1093/jxb/erq098
Lee H, Suh SS, Park E, Cho E, Ahn JH, Kim SG et al (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev 14:2366–2376. doi:10.1101/gad.813600
Lee S, Kim J, Han JJ, Han MJ, An G (2004) Functional analyses of the flowering time gene OsMADS50, the putative SUPPRESSOR OF OVEREXPRESSION OF CO 1/AGAMOUS-LIKE 20 (SOC1/AGL20) ortholog in rice. Plant J 38:754–764. doi:10.1111/j.1365-313X.2004.02082.x
Lee J, Oh M, Park H, Lee I (2008) SOC1 translocated to the nucleus by interaction with AGL24 directly regulates LEAFY. Plant J 55:832–843. doi:10.1111/j.1365-313X.2008.03552.x
Lei HJ, Yuan HZ, Liu Y, Guo XW, Liao X, Liu LL et al (2013) Identification and characterization of FaSOC1, a homolog of SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 from strawberry. Gene 531:158–167. doi:10.1016/j.gene.2013.09.036
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y et al (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327. doi:10.1093/nar/30.1.325
Lin EP, Peng HZ, Jin QY, Deng MJ, Li T, Xiao XC et al (2009) Identification and characterization of two Bamboo (Phyllostachys praecox) AP1/SQUA-like MADS-box genes during floral transition. Planta 231:109–120. doi:10.1007/s00425-009-1033-0
Lin XC, Chow TY, Chen HH, Liu CC, Chou SJ, Huang BL et al (2010) Understanding bamboo flowering based on large-scale analysis of expressed sequence tags. Genet Mol Res 9:1085–1093. doi:10.4238/vol9-2gmr804
Lin XC, Yuan XL, Lin R, Lou YF, Fang W (2012) Morphogenesis of indefinite inflorescence of Phyllostachys violascens (In Chinese). J Fujian Coll For 32:141–145
Liu C, Zhou J, Bracha-Drori K, Yalovsky S, Ito T, Yu H (2007) Specification of Arabidopsis floral meristem identity by repression of flowering time genes. Development 134:1901–1910. doi:10.1242/dev.003103
Liu C, Xi WY, Shen LS, Tan CP, Yu H (2009) Regulation of floral patterning by flowering time genes. Dev Cell 16:711–722. doi:10.1016/j.devcel.2009.03.011
Liu C, Teo ZWN, Bi Y, Song S, Xi W, Yang X et al (2013) A conserved genetic pathway determines inflorescence architecture in Arabidopsis and rice. Dev Cell 24:612–622. doi:10.1016/j.devcel.2013.02.013
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. doi:10.1006/meth.2001.1262
Louis B, Waikhom SD, Goyari S, Jose RC, Roy P, Talukdar NC (2015) First proteome study of sporadic flowering in bamboo species (Bambusa vulgaris and Dendrocalamus manipureanus) reveal the boom is associated with stress and mobile genetic elements. Gene 574:255–264. doi:10.1016/j.gene.2015.08.010
Lu YT, Yuan XL, Lin XC, Fang W (2012) Endogenous hormone changes during floral bud morphological differentiation of Phyllostachys violascens (In Chinese). J Zhejiang A F Univ 29:161–165
Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277
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. Nat Genet 40:1489–1492. doi:10.1038/ng.253
Moon J, Suh SS, Lee H, Choi KR, Hong CB, Paek NC et al (2003) The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J 35:613–623. doi:10.1046/j.1365-313X.2003.01833.x
Onouchi H, Igeño MI, Périlleux C, Graves K, Coupland G (2000) Mutagenesis of plants overexpressing CONSTANS demonstrates novel interactions among Arabidopsis flowering-time genes. Plant Cell 12:885–900. doi:10.1105/tpc.12.6.885
Papaefthimiou D, Kapazoglou A, Tsaftaris AS (2012) Cloning and characterization of SOC1 homologs in barley (Hordeum vulgare) and their expression during seed development and in response to vernalization. Physiol Plant 146:71–85. doi:10.1111/j.1399-3054.2012.01610.x
Pelaz S, Gustafson-Brown C, Kohalmi SE, Crosby WL, Yanofsky MF (2001) APETALA1 and SEPALLATA3 interact to promote flower development. Plant J 26:385–394. doi:10.1046/j.1365-313X.2001.2641042.x
Peng ZH, Lu Y, Li L, Zhao Q, Feng Q et al (2013) The draft genome of the fast-growing non-timber forest species moso bamboo (Phyllostachys heterocycla). Nat Genet 45:456–461. doi:10.1038/ng.2569
Putterill J, Laurie R, Macknight R (2004) It’s time to flower: the genetic control of flowering time. Bioessays 26:363–373. doi:10.1002/bies.20021
Qi FY, Hu T, Peng ZH, Gao J (2013) Screening of reference genes used in qRT-PCR and expression analysis of PheTFL1 gene in Moso Bamboo (In Chinese). Acta Bot Boreal 33:0048–0052
Ruokolainen S, Ng YP, Albert VA, Elomaa P, Teeri TH (2011) Over-expression of the Gerbera hybrida At-SOC1-like1 gene Gh-SOC1 leads to floral organ identity deterioration. Ann Bot Lond 107:1491–1499. doi:10.1093/aob/mcr112
Rusconi F, Simeoni F, Francia P, Cominelli E, Conti L, Riboni M et al (2013) The Arabidopsis thaliana MYB60 promoter provides a tool for the spatio-temporal control of gene expression in stomatal guard cells. J Exp Bot 64:3361–3371. doi:10.1093/jxb/ert180
Ryu CH, Lee S, Cho LH, Kim SL, Lee YS, Choi SC et al (2009) OsMADS50 and OsMADS56 function antagonistically in regulating long day (LD)-dependent flowering in rice. Plant Cell Environ 32:1412–1427. doi:10.1111/j.1365-3040.2009.02008.x
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 288:1613–1616. doi:10.1126/science.288.5471.1613
Sharma ML (1994) The flowering of bamboo: fallacies and facts. In: Proceedings 4th international bamboo workshop, pp 68–70
Shih MC, Chou ML, Yue JJ, Hsu CT, ChangWJ Ko SS et al (2014) BeMADS1 is a key to delivery MADSs into nucleus in reproductive tissues-De novo characterization of Bambusa edulis transcriptome and study of MADS genes in bamboo floral development. BMC Plant Biol 14:1. doi:10.1186/1471-2229-14-179
Tadege M, Sheldon CC, Helliwell CA, Upadhyaya NM, Dennis ES, Peacock WJ (2003) Reciprocal control of flowering time by OsSOC1 in transgenic Arabidopsis and by FLC in transgenic rice. Plant Biotechnol J 1:361–369. doi:10.1046/j.1467-7652.2003.00034.x
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121
Tan FC, Swain SM (2007) Functional characterization of AP3, SOC1 and WUS homologues from citrus (Citrus sinensis). Physiol Plant 131:481–495. doi:10.1111/j.1399-3054.2007.00971.x
Tian B, Chen Y, Li D, Yan Y (2006) Cloning and characterization of a bamboo leafy hull sterile1 homologous gene. DNA Seq 17:143–151. doi:10.1080/10425170600699877
Wang YC, Klein TM, Fromm M, Cao J, Sanford JC, Wu R (1988) Transient expression of foreign genes in rice, wheat and soybean cells following particle bombardment. Plant Mol Biol 11:433–439. doi:10.1007/BF00039024
Wu HY, Liu KH, Wang YC, Wu JF, Chiu WL, Chen CY et al (2014) AGROBEST: an efficient Agrobacterium-mediated transient expression method for versatile gene function analyses in Arabidopsis seedlings. Plant methods 10:1–16. doi:10.1186/1746-4811-10-19
Wuest SE, O’Maoileidigh DS, Rae L, Kwasniewska K, Raganelli A, Hanczaryk K et al (2012) Molecular basis for the specification of floral organs by APETALA3 and PISTILLATA. PNAS 109:13452–13457. doi:10.1073/pnas.1207075109
Xie HP (2004) Study on the senescence mechanism of leaf in bamboo plants (In Chinese). Doctoral dissertation, Nanjing, Nanjing Forestry University
Yoo SK, Chung KS, Kim J, Lee JH, Hong SM, Yoo SJ et al (2005) Constans activates suppressor of overexpression of CONSTANS 1 through Flowering Locus T to promote flowering in Arabidopsis. Plant Physiol 139:770–778. doi:10.1104/pp.105.066928
Zhang XM, Zhao L, Larson-Rabin Z, Li DZ, Guo ZH (2012) De novo sequencing and characterization of the floral transcriptome of Dendrocalamus latiflorus (Poaceae: Bambusoideae). PLoS One 7:e42082. doi:10.1371/journal.pone.0042082
Zhao H, Peng Z, Fei B, Li L, Hu T, Gao Z, Jiang Z (2014) BambooGDB: a bamboo genome database with functional annotation and an analysis platform. Database 2014:bau006. doi:10.1093/database/bau006
Zhao XY, Wang XY, Zhao L, Zhang XM, Chen SY, Ma PF et al (2015) Investigating the microRNA-omes of two developmental phases of Dendrocalamus latiflorus (poaceae: bambusoideae) inflorescences. Plant Mol Biol Rep 33:1–15. doi:10.1007/s11105-014-0808-z
Zhong X, Dai X, Xv J, Wu H, Liu B, Li H (2012) Cloning and expression analysis of GmGAL1, SOC1 homolog gene in soybean. Mol Biol Rep 39:6967–6974. doi:10.1007/s11033-012-1524-0
Acknowledgments
We are grateful to Professor Erh-min Lai (Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan) for supplying the efr-1 Arabidopsis seeds and Agrobacterium tumefaciens strain C58C1. This study was funded by the National Natural Science Foundation of China [Grant Nos. 31000295 and 31270715] and the China Scholarship Council to X Lin.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by F. Canovas.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Liu, S., Qi, T., Ma, J. et al. Ectopic expression of a SOC1 homolog from Phyllostachys violascens alters flowering time and identity of floral organs in Arabidopsis thaliana . Trees 30, 2203–2215 (2016). https://doi.org/10.1007/s00468-016-1445-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-016-1445-y