Abstract
SET domain group 8 (SDG8) serves as multifunctional H3 methyltransferase to be involved in various processes in plants. To better understand its functions, an EMS mutagenesis of sdg8-2 seeds was performed for the enhancers of sdg8-2, and an allele of CURLY LEAF (clf100) was identified in the study, which enhanced the phenotype of sdg8-2, such as early flower, abortion, and more shoot branches. Real-time PCR analysis indicated that the simultaneous disruption of SDG8 and CLF can lead to synergistic or antagonistic effect on transcriptional accumulation of shoot branching regulatory genes. Among the 16 genes examined in the study, the transcriptional accumulation of LATERAL SUPPRESSOR (LAS) and UDP-GLYCOSYLTRANSFERASE 74E2 (UGT74E2) displayed most significant enhancement in double mutant. Furthermore, the chromatin immunoprecipitation assay indicated that the excess expressions of LAS and UGT74E2 in double mutant were associated with the state of H3K trimethylation marks at their locus, showing the reduction of H3K27me3 level, as well as an elevated enrichment of H3K36me3 at LAS locus and H3K4me3 at UGT74E2 locus. These results indicated that CLF and SDG8 can play a combinatorial role in regulation of shoot branching via maintaining proper histone markers for appropriate gene expression.
Similar content being viewed by others
References
Aguilar-Martinez JA, Poza-Carrion C, Cubas P (2007) Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19:458–472. doi:10.1105/tpc.106.048934
Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447:407–412. doi:10.1038/nature05915
Berr A, McCallum EJ, Alioua A, Heintz D, Heitz T, Shen WH (2010) Arabidopsis histone methyltransferase SET DOMAIN GROUP8 mediates induction of the jasmonate/ethylene pathway genes in plant defense response to necrotrophic fungi. Plant Physiol 154:1403–1414. doi:10.1104/pp.110.161497
Booker J, Sieberer T, Wright W, Williamson L, Willett B, Stirnberg P, Turnbull C, Srinivasan M, Goddard P, Leyser O (2005) MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev Cell 8:443–449. doi:10.1016/j.devcel.2005.01.009
Catterou M, Dubois F, Smets R, Vaniet S, Kichey T, Van Onckelen H, Sangwan-Norreel BS, Sangwan RS (2002) hoc: an Arabidopsis mutant overproducing cytokinins and expressing high in vitro organogenic capacity. Plant J 30(3):273–287. doi:10.1046/j.1365-313X.2002.01286.x
Cazzonelli CI, Cuttriss AJ, Cossetto SB, Pye W, Crisp P, Whelan J, Finnegan EJ, Turnbull C, Pogson BJ (2009) Regulation of carotenoid composition and shoot branching in Arabidopsis by a chromatin modifying histone methyltransferase, SDG8. Plant Cell 21(1):39–53. doi:10.1105/tpc.108.063131
Cazzonelli CI, Roberts AC, Carmody ME, Pogson BJ (2010) Transcriptional control of SET DOMAIN GROUP 8 and CAROTENOID ISOMERASE during Arabidopsis development. Mol Plant 3:174–191. doi:10.1093/mp/ssp092
Challis RJ, Hepworth J, Mouchel C, Waites R, Leyser O (2013) A role for MORE AXILLARY GROWTH1 (MAX1) in evolutionary diversity in strigolactone signaling upstream of MAX2. Plant Physiol 161(4):1885–1902. doi:10.1104/pp.112.211383
Dong G, Ma DP, Li J (2008) The histone methyltransferase SDG8 regulates shoot branching in Arabidopsis. Biochem Biophys Res Commun 373(4):659–664. doi:10.1016/j.bbrc.2008.06.096
Gendrel AV, Lippman Z, Martienssen R, Colot V (2005) Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods 2:213–218. doi:10.1038/nmeth0305-213
Goodrich J, Puangsomlee P, Martin M, Long D, Meyerowitz EM, Coupland G (1997) A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386(6620):44–51. doi:10.1038/386044a0
Greb T, Clarenz O, Schafer E, Muller D, Herrero R, Schmitz G, Theres K (2003) Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes Dev 17(9):1175–1187. doi:10.1101/gad.260703
Grini PE, Thorstensen T, Alm V, Vizcay-Barrena G, Windju SS, Jorstad TS, Wilson ZA, Aalen RB (2009) The ASH1 HOMOLOG 2 (ASHH2) histone H3 methyltransferase is required for ovule and anther development in Arabidopsis. PLoS One 4(11):e7817. doi:10.1371/journal.pone.0007817
Guo Y, Gan SS (2011) AtMYB2 regulates whole plant senescence by inhibiting cytokinin-mediated branching at late stages of development in Arabidopsis. Plant Physiol 156(3):1612–1619. doi:10.1104/pp.111.177022
Hibara K, Karim MR, Takada S, Taoka K, Furutani M, Aida M, Tasaka M (2006) Arabidopsis CUP-SHAPED COTYLEDON3 regulates postembryonic shoot meristem and organ boundary formation. Plant Cell 18(11):2946–2957. doi:10.1105/tpc.106.045716
Hwang I, Kim SY, Kim CS, Park Y, Tripathi GR, Kim SK, Cheong H (2010) Over-expression of the IGI1 leading to altered shoot-branching development related to MAX pathway in Arabidopsis. Plant Mol Biol 73(6):629–641. doi:10.1007/s11103-010-9645-0
Keller T, Abbott J, Moritz T, Doerner P (2006) Arabidopsis REGULATOR OF AXILLARY MERISTEMS1 controls a leaf axil stem cell niche and modulates vegetative development. Plant Cell 18(3):598–611. doi:10.1105/tpc.105.038588
Kim SY, He Y, Jacob Y, Noh YS, Michael S, Amasino R (2005) Establishment of the vernalization-responsive, winter-annual habit in Arabidopsis requires a putative histone H3 methyl transferase. Plant Cell 17(12):3301–3310. doi:10.1105/tpc.105.034645
Lopez-Vernaza M, Yang S, Müller R, Thorpe F, de Leau E, Goodrich J (2012) Antagonistic roles of SEPALLATA3, FT and FLC genes as targets of the polycomb group gene CURLY LEAF. PLoS One 7(2):e30715. doi:10.1371/journal.pone.0030715
Lukowitz W, Gillmor CS, Scheible WR (2000) Positional cloning in Arabidopsis. Why it feels good to have a genome initiative working for you. Plant Physiol 123(3):795–805
Mimasu S, Umezawa N, Sato S, Higuchi T, Umehara T, Yokoyama S (2010) Structurally designed trans-2-phenylcyclopropylamine derivatives potently inhibit histone demethylase LSD1/KDM1. Biochemistry 49(30):6494–6503. doi:10.1021/bi100299r
Muller D, Schmitz G, Theres K (2006) Blind homologous R2R3 Myb genes control the pattern of lateral meristem initiation in Arabidopsis. Plant Cell 18(3):586–597. doi:10.1105/tpc.105.038745
Niwa M, Daimon Y, Kurotani K, Higo A, Pruneda-Paz JL, Breton G, Mitsuda N, Kay SA, Ohme-Takagi M, Endo M, Araki T (2013) BRANCHED1 interacts with FLOWERING LOCUS T to repress the floral transition of the axillary meristems in Arabidopsis. Plant Cell 25(4):1228–1242. doi:10.1105/tpc.112.109090
Otsuga D, DeGuzman B, Prigge MJ, Drews GN, Clark SE (2001) REVOLUTA regulates meristem initiation at lateral positions. Plant J 25(2):223–236. doi:10.1111/j.1365-313X.2001.00959.x
Pfluger J, Wagner D (2007) Histone modifications and dynamic regulation of genome accessibility in plants. Curr Opin Plant Biol 10(6):645–652. doi:10.1016/j.pbi.2007.07.013
Raman S, Greb T, Peaucelle A, Blein T, Laufs P, Theres K (2008) Interplay of miR164, CUP-SHAPED COTYLEDON genes and LATERAL SUPPRESSOR controls axillary meristem formation in Arabidopsis thaliana. Plant J 55(1):65–76. doi:10.1111/j.1365-313X.2008.03483.x
Rameau C (2010) Strigolactones, a novel class of plant hormone controlling shoot branching. C R Biol 333(4):344–349. doi:10.1016/j.crvi.2010.01.012
Saleh A, Al-Abdallat A, Ndamukong I, Alvarez-Venegas R, Avramova Z (2007) The Arabidopsis homologs of trithorax (ATX1) and enhancer of zeste (CLF) establish ‘bivalent chromatin marks’ at the silent AGAMOUS locus. Nucleic Acids Res 35(18):6290–6296. doi:10.1093/nar/gkm464
Schulze S, Schafer BN, Parizotto EA, Voinnet O, Theres K (2010) LOST MERISTEMS genes regulate cell differentiation of central zone descendants in Arabidopsis shoot meristems. Plant J 64(4):668–678. doi:10.1111/j.1365-313X.2010.04359.x
Shafiq S, Berr A, Shen WH (2014) Combinatorial functions of diverse histone methylations in Arabidopsis thaliana flowering time regulation. New Phytol 201(1):312–322. doi:10.1111/nph.12493
Shen H, Luong P, Huq E (2007) The F-box protein MAX2 functions as a positive regulator of photomorphogenesis in Arabidopsis. Plant Physiol 145(4):1471–1483. doi:10.1104/pp.107.107227
Sorefan K, Booker J, Haurogne K, Goussot M, Bainbridge K, Foo E, Chatfield S, Ward S, Beveridge C, Rameau C, Leyser O (2003) MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Dev 17:1469–1474. doi:10.1101/gad.256603
Stirnberg P, van De Sande K, Leyser HM (2002) MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129(5):1131–1141
Tang X, Lim MH, Pelletier J, Tang M, Nguyen V, Keller WA, Tsang EW, Wang A, Rothstein SJ, Harada JJ, Cui Y (2012) Synergistic repression of the embryonic programme by SET DOMAIN GROUP 8 and EMBRYONIC FLOWER 2 in Arabidopsis seedlings. J Exp Bot 63(3):1391–1404. doi:10.1093/jxb/err383
Tantikanjana T, Yong JW, Letham DS, Griffith M, Hussain M, Ljung K, Sandberg G, Sundaresan V (2001) Control of axillary bud initiation and shoot architecture in Arabidopsis through the SUPERSHOOT gene. Genes Dev 15(12):1577–1588. doi:10.1101/gad.887301
Tognetti VB, Van Aken O, Morreel K, Vandenbroucke K, van de Cotte B, De Clercq I, Chiwocha S, Fenske R, Prinsen E, Boerjan W, Genty B, Stubbs KA, Inzé D, Van Breusegem F (2010) Perturbation of indole-3-butyric acid homeostasis by the UDP-glucosyltransferase UGT74E2 modulates Arabidopsis architecture and water stress tolerance. Plant Cell 22(8):2660–2679. doi:10.1105/tpc.109.071316
Tsuchiya Y, McCourt P (2009) Strigolactones: a new hormone with a past. Curr Opin Plant Biol 12(5):556–561. doi:10.1016/j.pbi.2009.07.018
Vernoux T, Kronenberger J, Grandjean O, Laufs P, Traas J (2000) PIN-FORMED 1 regulates cell fate at the periphery of the shoot apical meristem. Development 127(23):5157–5165
Vidaurre DP, Ploense S, Krogan NT, Berleth T (2007) AMP1 and MP antagonistically regulate embryo and meristem development in Arabidopsis. Development 134(14):2561–2567. doi:10.1242/dev.006759
Wang Y, Sun S, Zhu W, Jia K, Yang H, Wang X (2013) Strigolactone/MAX2-induced degradation of brassinosteroid transcriptional effector BES1 regulates shoot branching. Dev Cell 27(6):681–688. doi:10.1016/j.devcel.2013.11.010
Weigel D, Glazebrook J (2002) EMS mutagenesis of seed. In: Weigel D, Glazebrook J (eds) Arabidopsis, a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 24–26
Xu L, Zhao Z, Dong A, Soubigou-Taconnat L, Renou JP, Steinmetz A, Shen WH (2008) Di- and tri- but not monomethylation on histone H3 lysine 36 marks active transcription of genes involved in flowering time regulation and other processes in Arabidopsis thaliana. Mol Cell Biol 28(4):1348–1360. doi:10.1128/MCB.01607-07
Yaginuma H, Hirakawa Y, Kondo Y, Ohashi-Ito K, Fukuda H (2011) A novel function of TDIF-related peptides: promotion of axillary bud formation. Plant Cell Physiol 52(8):1354–1364. doi:10.1093/pcp/pcr081
Yuan W, Xu M, Huang C, Liu N, Chen S, Zhu B (2011) H3K36 methylation antagonizes PRC2-mediated H3K27 methylation. J Biol Chem 286(10):7983–7989. doi:10.1074/jbc.M110.194027
Zhang X, Clarenz O, Cokus S, Bernatavichute YV, Pellegrini M, Goodrich J, Jacobsen SE (2007a) Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol 5(5):e129. doi:10.1371/journal.pbio.0050129
Zhang ZB, Yang G, Arana F, Chen Z, Li Y, Xia HJ (2007b) Arabidopsis inositol polyphosphate 6-/3-kinase (AtIpk2beta) is involved in axillary shoot branching via auxin signaling. Plant Physiol 144(2):942–951. doi:10.1104/pp.106.092163
Zhao Z, Yu Y, Meyer D, Wu C, Shen WH (2005) Prevention of early flowering by expression of FLOWERING LOCUS C requires methylation of histone H3 K36. Nat Cell Biol 7(12):1256–1260. doi:10.1038/ncb1329
Acknowledgments
We are grateful to the Arabidopsis Biological Resource Center for seeds of T-DNA insertion lines. The work was supported by the Grant from the National Natural Science Foundation of China (31370340).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Y. Wang.
S. Bian and J. Li equally contributed to the work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bian, S., Li, J., Tian, G. et al. Combinatorial regulation of CLF and SDG8 during Arabidopsis shoot branching. Acta Physiol Plant 38, 173 (2016). https://doi.org/10.1007/s11738-016-2188-5
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-016-2188-5