A gibberellin methyltransferase modulates the timing of floral transition at the Arabidopsis shoot meristem.
Journal
Physiologia plantarum
ISSN: 1399-3054
Titre abrégé: Physiol Plant
Pays: Denmark
ID NLM: 1256322
Informations de publication
Date de publication:
Dec 2020
Dec 2020
Historique:
received:
15
03
2020
revised:
26
05
2020
accepted:
29
05
2020
pubmed:
3
6
2020
medline:
25
11
2020
entrez:
3
6
2020
Statut:
ppublish
Résumé
The transition from vegetative to reproductive growth is a key event in the plant life cycle. Plants therefore use a variety of environmental and endogenous signals to determine the optimal time for flowering to ensure reproductive success. These signals are integrated at the shoot apical meristem (SAM), which subsequently undergoes a shift in identity and begins producing flowers rather than leaves, while still maintaining pluripotency and meristematic function. Gibberellic acid (GA), an important hormone associated with cell growth and differentiation, has been shown to promote flowering in many plant species including Arabidopsis thaliana, but the details of how spatial and temporal regulation of GAs in the SAM contribute to floral transition are poorly understood. In this study, we show that the gene GIBBERELLIC ACID METHYLTRANSFERASE 2 (GAMT2), which encodes a GA-inactivating enzyme, is significantly upregulated at the SAM during floral transition and contributes to the regulation of flowering time. Loss of GAMT2 function leads to early flowering, whereas transgenic misexpression of GAMT2 in specific regions around the SAM delays flowering. We also found that GAMT2 expression is independent of the key floral regulator LEAFY but is strongly increased by the application of exogenous GA. Our results indicate that GAMT2 is a repressor of flowering that may act as a buffer of GA levels at the SAM to help prevent premature flowering.
Substances chimiques
Arabidopsis Proteins
0
Gibberellins
0
Methyltransferases
EC 2.1.1.-
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
474-487Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : SCHM 1560/10-1
Organisme : Knut och Alice Wallenbergs Stiftelse
ID : 2016.0025
Informations de copyright
© 2020 The Authors. Physiologia Plantarum published by John Wiley & Sons Ltd on behalf of Scandinavian Plant Physiology Society.
Références
An H, Roussot C, Suárez-López P, Corbesier L, Vincent C, Piñeiro M, Hepworth S, Mouradov A, Justin S, Turnbull C, Coupland G (2004) CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131: 3615-3626
Andres F, Porri A, Torti S, Mateos J, Romera-Branchat M, Garcia-Martinez JL, Fornara F, Gregis V, Kater MM, Coupland G (2014) SHORT VEGETATIVE PHASE reduces gibberellin biosynthesis at the Arabidopsis shoot apex to regulate the floral transition. Proc Natl Acad Sci USA 111: 2760-2769
Bao S, Hua C, Shen L, Yu H (2020) New insights into gibberellin signaling in regulating flowering in Arabidopsis. J Integr Plant Biol 62: 118-131
Blazquez MA, Weigel D (2000) Integration of floral inductive signals in Arabidopsis. Nature 404: 889-892
Blazquez MA, Soowal LN, Lee I, Weigel D (1997) LEAFY expression and flower initiation in Arabidopsis. Development 124: 3835-3844
Blazquez MA, Green R, Nilsson O, Sussman MR, Weigel D (1998) Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. Plant Cell 10: 791-800
Bolduc N, Hake S (2009) The maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene ga2ox1. Plant Cell 21: 1647-1658
Clough SJ, Bent AF (1998) Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
Collani S, Neumann M, Yant L, Schmid M (2019) FT modulates genome-wide DNA-binding of the bZIP transcription factor FD. Plant Physiol 180: 367-380
Deplancke B., Vermeirssen V., Arda H.E., Martinez N.J., Walhout A.J.M. (2006) Gateway-Compatible Yeast One-Hybrid Screens. Cold Spring Harbor Protocols, 2006 (28), pdb.prot4590-pdb.prot4590. http://dx.doi.org/10.1101/pdb.prot4590.
Eriksson S, Bohlenius H, Moritz T, Nilsson O (2006) GA4 is the active gibberellin in the regulation of LEAFY transcription and Arabidopsis floral initiation. Plant Cell 18: 2172-2181
Fornara F, de Montaigu A, Coupland G (2010) SnapShot: control of flowering in Arabidopsis. Cell 141 550: e1-e2
Fukazawa J, Mori M, Watanabe S, Miyamoto C, Ito T, Takahashi Y (2017) DELLA-GAF1 complex is a main component in gibberellin feedback regulation of GA20 oxidase 2. Plant Physiol 175: 1395-1406
Galvao VC, Horrer D, Kuttner F, Schmid M (2012) Spatial control of flowering by DELLA proteins in Arabidopsis thaliana. Development 139: 4072-4082
Gocal GF, King RW, Blundell CA, Schwartz OM, Andersen CH, Weigel D (2001) Evolution of floral meristem identity genes. Analysis of Lolium temulentum genes related to APETALA1 and LEAFY of Arabidopsis. Plant Physiol 125: 1788-1801
Griffiths J, Murase K, Rieu I, Zentella R, Zhang ZL, Powers SJ, Gong F, Phillips AL, Hedden P, Sun TP, Thomas SG (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18: 3399-3414
Hay A, Tsiantis M (2010) KNOX genes: versatile regulators of plant development and diversity. Development 137: 3153-3165
Hay A, Kaur H, Phillips A, Hedden P, Hake S, Tsiantis M (2002) The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Curr Biol 12: 1557-1565
Hu J, Mitchum MG, Barnaby N, Ayele BT, Ogawa M, Nam E, Lai WC, Hanada A, Alonso LM, Ecker LR, Swain SM, Yamaguchi S, Kamiya Y, Sun TP (2008) Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis. Plant Cell 20: 320-336
Immink RGH, Pose D, Ferrario S, Ott F, Kaufmann K, Valentim FL, de Folter S, van der Wal F, van Dijk ADJ, Schmid M, Angenent GC (2012) Characterization of SOC1's central role in flowering by the identification of its upstream and downstream regulators. Plant Physiol 160: 433-449
Jasinski S, Piazza P, Craft J, Hay A, Woolley L, Rieu I, Phillips A, Hedden P, Tsiantis M (2005) KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol 15: 1560-1565
Lampropoulos A, Sutikovic Z, Wenzl C, Maegele I, Lohmann JU, Forner J (2013) GreenGate - a novel, versatile, and efficient cloning system for plant transgenesis. PLoS One 8: e83043
Lincoln C, Long J, Yamaguchi J, Serikawa K, Hake S (1994) A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell 6: 1859-1876
Moon J, Suh SS, Lee H, Choi KR, Hong CB, Paek NC, Kim SG, Lee I (2003) The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J 35: 613-623
Nam YJ, Herman D, Blomme J, Chae E, Kojima M, Coppens F, Storme V, Van Daele T, Dhondt S, Sakakibara H, Weigel D, Inze D, Gonzalez N (2017) Natural variation of molecular and morphological gibberellin responses. Plant Physiol 173: 703-714
Ng M, Yanofsky MF (2001) Activation of the Arabidopsis B class homeotic genes by APETALA1. Plant Cell 13: 739-753
Nomura T, Magome H, Hanada A, Takeda-Kamiya N, Mander LN, Kamiya Y, Yamaguchi S (2013) Functional analysis of Arabidopsis CYP714A1 and CYP714A2 reveals that they are distinct gibberellin modification enzymes. Plant Cell Physiol 54: 1837-1851
Olszewski N, Sun TP, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14: S61-S80
Parcy F, Nilsson O, Busch MA, Lee I, Weigel D (1998) A genetic framework for floral patterning. Nature 395: 561-566
Porri A, Torti S, Romera-Branchat M, Coupland G (2012) Spatially distinct regulatory roles for gibberellins in the promotion of flowering of Arabidopsis under long photoperiods. Development 139: 2198-2209
Raatz B, Eicker A, Schmitz G, Fuss E, Muller D, Rossmann S, Theres K (2011) Specific expression of LATERAL SUPPRESSOR is controlled by an evolutionarily conserved 3′ enhancer. Plant J 68: 400-412
Ratcliffe OJ, Bradley DJ, Coen ES (1999) Separation of shoot and floral identity in Arabidopsis. Development 126: 1109-1120
Richter R, Bastakis E, Schwechheimer C (2013) Cross-repressive interactions between SOC1 and the GATAs GNC and GNL/CGA1 in the control of greening, cold tolerance, and flowering time in Arabidopsis. Plant Physiol 162: 1992-2004
Rieu I, Eriksson S, Powers SJ, Gong F, Griffiths J, Woolley L, Benlloch R, Nilsson O, Thomas SG, Hedden P, Phillips AL (2008) Genetic analysis reveals that C19-GA 2-oxidation is a major gibberellin inactivation pathway in Arabidopsis. Plant Cell 20: 2420-2436
Sakamoto T, Kamiya N, Ueguchi-Tanaka M, Iwahori S, Matsuoka M (2001) KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev 15: 581-590
Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37: 501-506
Scofield S, Murison A, Jones A, Fozard J, Aida M, Band LR, Bennett M, Murray JAH (2018) Coordination of meristem and boundary functions by transcription factors in the SHOOT MERISTEMLESS regulatory network. Development 145: dev157081
Srikanth A, Schmid M (2011) Regulation of flowering time: all roads lead to Rome. Cell Mol Life Sci 68: 2013-2037
Varbanova M, Yamaguchi S, Yang Y, McKelvey K, Hanada A, Borochov R, Yu F, Jikumaru Y, Ross J, Cortes D, Ma CJ, Noel JP, Mander L, Shulaev V, Kamiya Y, Rodermel S, Weiss D, Pichersky E (2007) Methylation of gibberellins by Arabidopsis GAMT1 and GAMT2. Plant Cell 19: 32-45
Veit B (2009) Hormone mediated regulation of the shoot apical meristem. Plant Mol Biol 69: 397-408
Wang JW, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138: 738-749
Weigel D, Jurgens G (2002) Stem cells that make stems. Nature 415: 751-754
Wilczek AM, Roe JL, Knapp MC, Cooper MD, Lopez-Gallego C, Martin LJ, Muir CD, Sim S, Walker A, Anderson J, Egan JF, Moyers BT, Petipas R, Giakountis A, Charbit E, Coupland G, Welch SM, Schmitt J (2009) Effects of genetic perturbation on seasonal life history plasticity. Science 323: 930-934
Winter CM, Austin RS, Blanvillain-Baufume S, Reback MA, Monniaux M, Wu MF, Sang Y, Yamaguchi A, Yamaguchi N, Parker JE, Parcy F, Jensen ST, Li H, Wagner D (2011) LEAFY target genes reveal floral regulatory logic, cis motifs, and a link to biotic stimulus response. Dev Cell 20: 430-443
Winter CM, Yamaguchi N, Wu MF, Wagner D (2015) Transcriptional programs regulated by both LEAFY and APETALA1 at the time of flower formation. Physiol Plant 155: 55-73
Xing SF, Qin GJ, Shi Y, Ma ZQ, Chen ZL, Gu HY, Qu LJ (2007) GAMT2 encodes a methyltransferase of gibberellic acid that is involved in seed maturation and germination in Arabidopsis. J Integr Plant Biol 49: 368-381
Yamaguchi N, Winter CM, Wu MF, Kanno Y, Yamaguchi A, Seo M, Wagner D (2014) Gibberellin acts positively then negatively to control onset of flower formation in Arabidopsis. Science 344: 638-641
Yanai O, Shani E, Dolezal K, Tarkowski P, Sablowski R, Sandberg G, Samach A, Ori N (2005) Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr Biol 15: 1566-1571
You Y, Sawikowska A, Neumann M, Pose D, Capovilla G, Langenecker T, Neher RA, Krajewski P, Schmid M (2017) Temporal dynamics of gene expression and histone marks at the Arabidopsis shoot meristem during flowering. Nat Commun 8: 15120
You Y, Sawikowska A, Lee JE, Benstein RM, Neumann M, Krajewski P, Schmid M (2019) Phloem companion cell-specific transcriptomic and epigenomic analyses identify MRF1, a regulator of flowering. Plant Cell 31: 325-345
Zentella R, Zhang ZL, Park M, Thomas SG, Endo A, Murase K, Fleet CM, Jikumaru Y, Nambara E, Kamiya Y, Sun TP (2007) Global analysis of della direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19: 3037-3057