BdRCN4, a Brachypodium distachyon TFL1 homologue, is involved in regulation of apical meristem fate.
Brachypodium distachyon
BdRCN4
Inflorescence meristem regulation
TFL1 homologs
Journal
Plant molecular biology
ISSN: 1573-5028
Titre abrégé: Plant Mol Biol
Pays: Netherlands
ID NLM: 9106343
Informations de publication
Date de publication:
28 Jun 2024
28 Jun 2024
Historique:
received:
04
09
2023
accepted:
13
05
2024
medline:
28
6
2024
pubmed:
28
6
2024
entrez:
28
6
2024
Statut:
epublish
Résumé
In higher plants, the shift from vegetative to reproductive development is governed by complex interplay of internal and external signals. TERMINALFLOWER1 (TFL1) plays a crucial role in the regulation of flowering time and inflorescence architecture in Arabidopsis thaliana. This study aimed to explore the function of BdRCN4, a homolog of TFL1 in Brachypodium distachyon, through functional analyses in mutant and transgenic plants. The results revealed that overexpression of BdRCN4 in B. distachyon leads to an extended vegetative phase and reduced production of spikelets. Similar results were found in A. thaliana, where constitutive expression of BdRCN4 promoted a delay in flowering time, followed by the development of hypervegetative shoots, with no flowers or siliques produced. Our results suggest that BdRCN4 acts as a flowering repressor analogous to TFL1, negatively regulating AP1, but no LFY expression. To further validate this hypothesis, a 35S::LFY-GR co-transformation approach on 35::BdRCN4 lines was performed. Remarkably, AP1 expression levels and flower formation were restored to normal in co-transformed plants when treated with dexamethasone. Although further molecular studies will be necessary, the evidence in B. distachyon support the idea that a balance between LFY and BdRCN4/TFL1 seems to be essential for activating AP1 expression and initiating floral organ identity gene expression. This study also demonstrates interesting conservation through the molecular pathways that regulate flowering meristem transition and identity across the evolution of monocot and dicot plants.
Identifiants
pubmed: 38940986
doi: 10.1007/s11103-024-01467-4
pii: 10.1007/s11103-024-01467-4
doi:
Substances chimiques
Plant Proteins
0
Arabidopsis Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
81Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Nature B.V.
Références
Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science (1979) 309:1052–1056. https://doi.org/10.1126/science.1115983
Ahn JH, Miller D, Winter VJ, Banfield MJ, Jeong HL, So YY, Henz SR, Brady RL, Weigel D (2006) A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO J 25:605–614. https://doi.org/10.1038/sj.emboj.7600950
doi: 10.1038/sj.emboj.7600950
pubmed: 16424903
pmcid: 1383534
Barton MK (2010) Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. Dev Biol 341:95–113. https://doi.org/10.1016/j.ydbio.2009.11.029
doi: 10.1016/j.ydbio.2009.11.029
pubmed: 19961843
Benlloch R, Berbel A, Serrano-Mislata A, Madueño F (2007) Floral initiation and inflorescence architecture: a comparative view. Ann Bot 100:659–676. https://doi.org/10.1093/aob/mcm146
doi: 10.1093/aob/mcm146
pubmed: 17679690
pmcid: 2533596
Bi Z, Tahir AT, Huang H, Hua Y (2019) Cloning and functional analysis of five TERMINAL FLOWER 1/CENTRORADIALIS-like genes from Hevea brasiliensis. Physiol Plant 166:612–627. https://doi.org/10.1111/ppl.12808
doi: 10.1111/ppl.12808
pubmed: 30069883
Blümel M, Dally N, Jung C (2015) Flowering time regulation in crops-what did we learn from Arabidopsis? Curr Opin Biotechnol 32:121–129. https://doi.org/10.1016/j.copbio.2014.11.023
doi: 10.1016/j.copbio.2014.11.023
pubmed: 25553537
Bowman JL, Eshed Y (2000) Formation and maintenance of the shoot apical meristem. Trends Plant Sci 5:110–115. https://doi.org/10.1016/S1360-1385(00)01569-7
doi: 10.1016/S1360-1385(00)01569-7
pubmed: 10707076
Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13:1499–1510. https://doi.org/10.1105/tpc.13.7.1499
doi: 10.1105/tpc.13.7.1499
pubmed: 11449047
pmcid: 139543
Bradley D, Carpenter R, Copsey L, Vincent C, Rothstein S, Coen E (1996) Control of inflorescence architecture in Antirrhinum
Bragg JN, Wu J, Gordon SP, Guttman ME, Thilmony R, Lazo GR, Gu YQ, Vogel JP (2012) Generation and characterization of the Western Regional Research Center Brachypodium T-DNA Insertional Mutant Collection. PLoS ONE 7. https://doi.org/10.1371/journal.pone.0041916
Chardon F, Damerval C (2005) Phylogenomic analysis of the PEBP gene family in cereals. J Mol Evol 61:579–590. https://doi.org/10.1007/s00239-004-0179-4
doi: 10.1007/s00239-004-0179-4
pubmed: 16170456
Charrier B, Champion A, Henry Y, Kreis M (2002) Expression profiling of the whole Arabidopsis Shaggy- Like kinase Multigene Family by Real-Time Reverse. Plant Physiol 130:577–590. https://doi.org/10.1104/pp.009175.In
doi: 10.1104/pp.009175.In
pubmed: 12376626
pmcid: 166588
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. https://doi.org/10.1046/j.1365-313X.1998.00343.x
doi: 10.1046/j.1365-313X.1998.00343.x
pubmed: 10069079
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 (1979) 316:1030–1033. https://doi.org/10.1126/science.1141752
D’Aloia M, Bonhomme D, Bouché F, Tamseddak K, Ormenese S, Torti S, Coupland G, Périlleux C (2011) Cytokinin promotes flowering of Arabidopsis via transcriptional activation of the FT paralogue TSF. Plant J 65:972–979. https://doi.org/10.1111/j.1365-313X.2011.04482.x
doi: 10.1111/j.1365-313X.2011.04482.x
pubmed: 21205031
Danilevskaya ON, Meng X, Hou Z, Ananiev EV, Simmons CR (2008) A genomic and expression compendium of the expanded PEBP gene family from maize. Plant Physiol 146:250–264. https://doi.org/10.1104/pp.107.109538
doi: 10.1104/pp.107.109538
pubmed: 17993543
pmcid: 2230559
Danilevskaya ON, Meng X, Ananiev EV (2010) Concerted modification of flowering time and inflorescence architecture by ectopic expression of TFL1-like genes in maize. Plant Physiol 153:238–251. https://doi.org/10.1104/pp.110.154211
doi: 10.1104/pp.110.154211
pubmed: 20200067
pmcid: 2862429
Darriba D, Taboada GL, Doallo R, Posada D (2012) JModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
doi: 10.1038/nmeth.2109
pubmed: 22847109
pmcid: 4594756
Derbyshire P, Byrne ME (2013) MORE SPIKELETS1 is required for spikelet fate in the inflorescence of Brachypodium. Plant Physiol 161:1291–1302. https://doi.org/10.1104/pp.112.212340
doi: 10.1104/pp.112.212340
pubmed: 23355632
pmcid: 3585597
Draper J, Mur LAJ, Jenkins G, Ghosh-Biswas GC, Bablak P, Hasterok R, Routledge APM (2001) Brachypodium distachyon. A new model system for functional genomics in grasses. Plant Physiol 127:1539–1555. https://doi.org/10.1104/pp.010196
doi: 10.1104/pp.010196
pubmed: 11743099
pmcid: 133562
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
doi: 10.1093/nar/gkh340
pubmed: 15034147
pmcid: 390337
Ferrándiz C, Gu Q, Martienssen R, Yanofsky MF (2000) Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127:725–734. https://doi.org/10.1242/dev.127.4.725
doi: 10.1242/dev.127.4.725
pubmed: 10648231
Fornara F, de Montaigu A, Coupland G (2010) SnapShot: control of flowering in arabidopsis. Cell 141:3–5. https://doi.org/10.1016/j.cell.2010.04.024
doi: 10.1016/j.cell.2010.04.024
Goslin K, Zheng B, Serrano-Mislata A, Rae L, Ryan PT, Kwaśniewska K, Thomson B, Ó’Maoiléidigh DS, Madueño F, Wellmer F, Graciet E (2017) Transcription factor interplay between LEAFY and APETALA1/CAULIFLOWER during floral initiation. Plant Physiol 174:1097–1109. https://doi.org/10.1104/pp.17.00098
doi: 10.1104/pp.17.00098
pubmed: 28385730
pmcid: 5462026
Hanano S, Goto K (2011) Arabidopsis terminal flower1 is involved in the regulation of flowering time and inflorescence development through transcriptional repression. Plant Cell 23:3172–3184. https://doi.org/10.1105/tpc.111.088641
doi: 10.1105/tpc.111.088641
pubmed: 21890645
pmcid: 3203435
Hanzawa Y, Money T, Bradley D (2005) A single amino acid converts a repressor to an activator of flowering. Proc Natl Acad Sci U S A 102:7748–7753. https://doi.org/10.1073/pnas.0500932102
doi: 10.1073/pnas.0500932102
pubmed: 15894619
pmcid: 1140427
Ho WWH, Weigel D (2014) Structural features determining flower-promoting activity of Arabidopsis FLOWERING LOCUS T. Plant Cell 26:552–564. https://doi.org/10.1105/tpc.113.115220
doi: 10.1105/tpc.113.115220
pubmed: 24532592
pmcid: 3967025
Hong SY, Seo PJ, Yang MS, Xiang F, Park CM (2008) Exploring valid reference genes for gene expression studies in Brachypodium distachyon by real-time PCR. BMC Plant Biol 8:1–11. https://doi.org/10.1186/1471-2229-8-112
doi: 10.1186/1471-2229-8-112
Huang NC, Jane WN, Chen J, Yu TS (2012) Arabidopsis thaliana CENTRORADIALIS homologue (ATC) acts systemically to inhibit floral initiation in Arabidopsis. Plant J 72:175–184. https://doi.org/10.1111/j.1365-313X.2012.05076.x
doi: 10.1111/j.1365-313X.2012.05076.x
pubmed: 22702636
Huelsenbeck JP, Ronquist F (2001) MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17:754–755. https://doi.org/10.1093/bioinformatics/17.8.754
doi: 10.1093/bioinformatics/17.8.754
pubmed: 11524383
Jensen CS, Salchert K, Nielsen KK (2001) A TERMINAL FLOWER1-like gene from perennial ryegrass involved in floral transition and axillary meristem identity. Plant Physiol 125:1517–1528. https://doi.org/10.1104/pp.125.3.1517
doi: 10.1104/pp.125.3.1517
pubmed: 11244130
pmcid: 65629
Jensen CS, Salchert K, Gao C, Andersen C, Didion T, Nielsen KK (2004) Floral inhibition in red fescue (Festuca rubra L.) through expression of a heterologous flowering repressor from Lolium. Mol Breeding 13:37–48. https://doi.org/10.1023/B:MOLB.0000012327.47625.23
doi: 10.1023/B:MOLB.0000012327.47625.23
Jin H, Tang X, Xing M, Zhu H, Sui J, Cai C, Li S (2019) Molecular and transcriptional characterization of phosphatidyl ethanolamine-binding proteins in wild peanuts Arachis duranensis and Arachis Ipaensis. BMC Plant Biol 19:1–16. https://doi.org/10.1186/s12870-019-2113-3
doi: 10.1186/s12870-019-2113-3
Jin S, Nasim Z, Susila H, Ahn JH (2021) Evolution and functional diversification of FLOWERING LOCUS T/TERMINAL FLOWER 1 family genes in plants. Semin Cell Dev Biol 109:20–30. https://doi.org/10.1016/j.semcdb.2020.05.007
doi: 10.1016/j.semcdb.2020.05.007
pubmed: 32507412
Krylova EA (2020) The role of TFL1 orthologs in determining of Plant Architectonics. Russ J Genet 56:1308–1322. https://doi.org/10.1134/S1022795420110058
doi: 10.1134/S1022795420110058
Lee C, Kim SJ, Jin S, Susila H, Youn G, Nasim Z, Alavilli H, Chung KS, Yoo SJ, Ahn JH (2019) Genetic interactions reveal the antagonistic roles of FT/TSF and TFL1 in the determination of inflorescence meristem identity in Arabidopsis. Plant J 99:452–464. https://doi.org/10.1111/tpj.14335
doi: 10.1111/tpj.14335
pubmed: 30943325
Lenth RV (2023) Emmeans: estimated marginal means. aka Least-Squares Means
Lv B, Nitcher R, Han X, Wang S, Ni F, Li K, Pearce S, Wu J, Dubcovsky J, Fu D (2014) Characterization of FLOWERING LOCUS T1 (FT1) gene in Brachypodium and wheat. PLoS ONE 9(4):e94171. https://doi.org/10.1371/journal.pone.0094171 PMID: 24718312; PMCID: PMC3981775
doi: 10.1371/journal.pone.0094171
pubmed: 24718312
pmcid: 3981775
Mimida N, Goto K, Kobayashi Y, Araki T, Ahn JH, Weigel D, Murata M, Motoyoshi F, Sakamoto W (2001) Functional divergence of the TFL1-like gene family in Arabidopsis revealed by characterization of a novel homologue. Genes Cells 6:327–336. https://doi.org/10.1046/j.1365-2443.2001.00425.x
doi: 10.1046/j.1365-2443.2001.00425.x
pubmed: 11318875
Nakagawa M, Shimamoto K, Kyozuka J (2002) Overexpression of RCN1 and RCN2, rice Terminal Flower 1/Centroradialis homologs, confers delay of phase transition and altered panicle morphology in rice. Plant J 29:743–750. https://doi.org/10.1046/j.1365-313X.2002.01255.x
doi: 10.1046/j.1365-313X.2002.01255.x
pubmed: 12148532
Notaguchi M, Abe M, Kimura T, Daimon Y, Kobayashi T, Yamaguchi A, Tomita Y, Dohi K, Mori M, Araki T (2008) Long-distance, graft-transmissible action of Arabidopsis FLOWERING LOCUS T protein to promote flowering. Plant Cell Physiol 49:1645–1658. https://doi.org/10.1093/pcp/pcn154
doi: 10.1093/pcp/pcn154
pubmed: 18849573
Peer LA, Bhat MY, Ahmad N, Mir BA (2021) Floral induction pathways: decision making and determination in plants to flower-a comprehensive review. J Appl Biol Biotechnol 9:7–17. https://doi.org/10.7324/JABB.2021.9201
doi: 10.7324/JABB.2021.9201
Pin PA, Benlloch R, Bonnet D, Wremerth-Weich E, Kraft T, Gielen JJL, Nilsson O (2010) An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science (1979) 330:1397–1400. https://doi.org/10.1126/science.1197004
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2021) nlme: Linear and Nonlinear Mixed Effects Models
R Core Team (2023) R: a Language and. Environment for Statistical Computing
Ratcliffe OJ, Amaya I, Vincent CA, Rothstein S, Carpenter R, Coen ES, Bradley DJ (1998) A common mechanism controls the life cycle and architecture of plants. Development 125:1609–1615. https://doi.org/10.1242/dev.125.9.1609
doi: 10.1242/dev.125.9.1609
pubmed: 9521899
Ryu JY, Lee HJ, Seo PJ, Jung JH, Ahn JH, Park CM (2014) The arabidopsis floral repressor BFT delays flowering by competing with FT for FD binding under high salinity. Mol Plant 7:377–387. https://doi.org/10.1093/mp/sst114
doi: 10.1093/mp/sst114
pubmed: 23935007
Schubert D, Lechtenberg B, Forsbach A, Gils M, Bahadur S, Schmidt R (2004) Silencing in Arabidopsis T-DNA transformants: the predominant role of a gene-specific RNA sensing mechanism versus position effects. Plant Cell 16:2561–2572. https://doi.org/10.1105/tpc.104.024547
doi: 10.1105/tpc.104.024547
pubmed: 15367719
pmcid: 520955
Shannon S, Meeks-Wagner DR (1991) A mutation in the arabidopsis TFL1 gene affects inflorescence meristem development. Plant Cell 3:877–892. https://doi.org/10.2307/3869152
doi: 10.2307/3869152
pubmed: 12324621
pmcid: 160057
Simpson GG, Dean C (2002) Arabidopsis, the Rosetta Stone of. Science (1979) 285:285–290
Wagner D, Sablowski RWM, Meyerowitz EM (1999) Transcriptional activation of APETALA1 by LEAFY. Sci (1979) 285:582–584. https://doi.org/10.1126/science.285.5427.582
doi: 10.1126/science.285.5427.582
Wei B et al. (2014) Genome-Wide analysis of the MADS-Box Gene Family in Brachypodium distachyon. PLOS One https://doi.org/10.1371/journal.pone.0084781
Wickland DP, Hanzawa Y (2015) The FLOWERING LOCUS T/TERMINAL FLOWER 1 Gene Family: functional evolution and molecular mechanisms. Mol Plant 8:983–997. https://doi.org/10.1016/j.molp.2015.01.007
doi: 10.1016/j.molp.2015.01.007
pubmed: 25598141
Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science (1979) 309:1056–1059. https://doi.org/10.1126/science.1114358
Yamaguchi A, Kobayashi Y, Goto K, Abe M, Araki T (2005) TWIN SISTER of FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol 46:1175–1189. https://doi.org/10.1093/pcp/pci151
doi: 10.1093/pcp/pci151
pubmed: 15951566
Yoo SJ, Chung KS, Jung SH, Yoo SY, Lee JS, Ahn JH (2010) BROTHER OF FT AND TFL1 (BFT) has TFL1 -like activity and functions redundantly with TFL1 in inflorescence meristem development in Arabidopsis. 1:241–253. https://doi.org/10.1111/j.1365-313X.2010.04234.x
Zeng HY, Lu YT, Yang XM, Xu YH, Lin XC (2015) Ectopic expression of the BoTFL1-like gene of Bambusa oldhamii delays blossoming in Arabidopsis thaliana and rescues the tfl1 mutant phenotype. Genet Mol Res 14:9306–9317. https://doi.org/10.4238/2015.August.10.11
doi: 10.4238/2015.August.10.11
pubmed: 26345864
Zhang S, Hu W, Wang L, Lin C, Cong B, Sun C, Luo D (2005) TFL1/CEN-like genes control intercalary meristem activity and phase transition in rice. Plant Sci 168:1393–1408. https://doi.org/10.1016/j.plantsci.2004.10.022
doi: 10.1016/j.plantsci.2004.10.022