Coordination of shoot apical meristem shape and identity by APETALA2 during floral transition in Arabidopsis.
Arabidopsis
/ genetics
Meristem
/ metabolism
Arabidopsis Proteins
/ metabolism
Flowers
/ genetics
Gene Expression Regulation, Plant
Homeodomain Proteins
/ metabolism
MADS Domain Proteins
/ metabolism
Transcription Factors
/ metabolism
Gene Expression Regulation, Developmental
Plants, Genetically Modified
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
13 Aug 2024
13 Aug 2024
Historique:
received:
03
09
2023
accepted:
06
08
2024
medline:
14
8
2024
pubmed:
14
8
2024
entrez:
13
8
2024
Statut:
epublish
Résumé
Plants flower in response to environmental signals. These signals change the shape and developmental identity of the shoot apical meristem (SAM), causing it to form flowers and inflorescences. We show that the increases in SAM width and height during floral transition correlate with changes in size of the central zone (CZ), defined by CLAVATA3 expression, and involve a transient increase in the height of the organizing center (OC), defined by WUSCHEL expression. The APETALA2 (AP2) transcription factor is required for the rapid increases in SAM height and width, by maintaining the width of the OC and increasing the height and width of the CZ. AP2 expression is repressed in the SAM at the end of floral transition, and extending the duration of its expression increases SAM width. Transcriptional repression by SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1) represents one of the mechanisms reducing AP2 expression during floral transition. Moreover, AP2 represses SOC1 transcription, and we find that reciprocal repression of SOC1 and AP2 contributes to synchronizing precise changes in meristem shape with floral transition.
Identifiants
pubmed: 39138172
doi: 10.1038/s41467-024-51341-6
pii: 10.1038/s41467-024-51341-6
doi:
Substances chimiques
Arabidopsis Proteins
0
Homeodomain Proteins
0
APETALA2 protein, Arabidopsis
0
MADS Domain Proteins
0
WUSCHEL protein, Arabidopsis
0
Transcription Factors
0
AT2G27250 protein, Arabidopsis
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
6930Subventions
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : CO 318/14-1
Informations de copyright
© 2024. The Author(s).
Références
Fuchs, M. & Lohmann, J. U. Aiming for the top: non-cell autonomous control of shoot stem cells in Arabidopsis. J. Plant Res 133, 297–309 (2020).
pubmed: 32146616
pmcid: 7214502
doi: 10.1007/s10265-020-01174-3
Uchida, N. & Torii, K. U. Stem cells within the shoot apical meristem: identity, arrangement and communication. Cell. Mol. Life Sci. 76, 1067–1080 (2019).
Landrein, B. et al. Nitrate modulates stem cell dynamics in Arabidopsis shoot meristems through cytokinins. Proc. Natl Acad. Sci. USA 115, 1382–1387 (2018).
pubmed: 29363596
pmcid: 5819446
doi: 10.1073/pnas.1718670115
Pfeiffer, A. et al. Integration of light and metabolic signals for stem cell activation at the shoot apical meristem. Elife https://doi.org/10.7554/eLife.17023 (2016).
doi: 10.7554/eLife.17023
pubmed: 27400267
pmcid: 4969040
Kinoshita, A. et al. Regulation of shoot meristem shape by photoperiodic signaling and phytohormones during floral induction of arabidopsis. Elife 9, e60661 (2020).
Tal, L. et al. Coordination of meristem doming and the floral transition by late termination, a kelch repeat protein. Plant Cell 29, 681–696 (2017).
pubmed: 28389586
pmcid: 5435437
doi: 10.1105/tpc.17.00030
Jacqmard, A., Gadisseur, I. & Bernier, G. Cell division and morphological changes in the shoot apex of Arabidopsis thaliana during floral transition. Ann. Bot. 91, 571–576 (2003).
pubmed: 12646501
pmcid: 4242243
doi: 10.1093/aob/mcg053
Sang, Q. et al. MicroRNA172 controls inflorescence meristem size through regulation of APETALA2 in Arabidopsis. N. Phytologist 235, 356–371 (2022).
doi: 10.1111/nph.18111
Xu, C. et al. A cascade of arabinosyltransferases controls shoot meristem size in tomato. Nat. Genet 47, 784–792 (2015).
pubmed: 26005869
doi: 10.1038/ng.3309
Bommert, P., Nagasawa, N. S. & Jackson, D. Quantitative variation in maize kernel row number is controlled by the FASCIATED EAR2 locus. Nat. Genet 45, 334–337 (2013).
pubmed: 23377180
doi: 10.1038/ng.2534
Schmid, M. et al. Dissection of floral induction pathways using global expression analysis. Development 130, 6001–6012 (2003).
pubmed: 14573523
doi: 10.1242/dev.00842
Torti, S. et al. Analysis of the Arabidopsis shoot meristem transcriptome during floral transition identifies distinct regulatory patterns and a leucine-rich repeat protein that promotes flowering. Plant Cell 24, 444–462 (2012).
pubmed: 22319055
pmcid: 3315226
doi: 10.1105/tpc.111.092791
Samach, A. et al. Distinct roles of constans target genes in reproductive development of Arabidopsis. Science 288, 1613–1616 (2000).
pubmed: 10834834
doi: 10.1126/science.288.5471.1613
Lee, H. et al. The AGAMOUS-lIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev. 14, 2366–2376 (2000).
pubmed: 10995392
pmcid: 316936
doi: 10.1101/gad.813600
Borner, R. et al. A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J. 24, 591–599 (2000).
pubmed: 11123798
doi: 10.1046/j.1365-313x.2000.00906.x
Kwiatkowska, D. Flowering and apical meristem growth dynamics. J. Exp. Bot. 59, 187–201 (2008).
pubmed: 18256052
doi: 10.1093/jxb/erm290
Hempel, F. D. & Feldman, L. J. Bi-directional inflorescence development in Arabidopsis thaliana: Acropetal initiation of flowers and basipetal initiation of paraclades. Planta https://doi.org/10.1007/BF01089045 (1994)
Miksche, J. P. & Brown, J. A. M. Development of vegetative and floral meristems of Arabidopsis thaliana. Am. J. Bot. 52, 533–537 (1965).
doi: 10.1002/j.1537-2197.1965.tb06818.x
Vaughan, J. G. The morphology and growth of the vegetative and reproductive apices of Arabidopsis thaliana (L.) Heynh., Capsella bursa-pastoris (L.) Medic. and Anagallis arvensis L. Botanical. J. Linn. Soc. 55, 279–301 (1951).
doi: 10.1111/j.1095-8339.1955.tb00014.x
Immink, R. G. H. et al. Characterization of SOC1’s central role in flowering by the identification of its upstream and downstream regulators. Plant Physiol. 160, 433–449 (2012).
pubmed: 22791302
pmcid: 3440217
doi: 10.1104/pp.112.202614
Tao, Z. et al. Genome-wide identification of SOC1 and SVP targets during the floral transition in Arabidopsis. Plant J. 70, 549–561 (2012).
pubmed: 22268548
doi: 10.1111/j.1365-313X.2012.04919.x
Clark, S. E., Running, M. P. & Meyerowitz, E. M. CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121, 2057–2067 (1995).
doi: 10.1242/dev.121.7.2057
Würschum, T., Groß-Hardt, R. & Laux, T. APETALA2 regulates the stem cell niche in the Arabidopsis shoot meristem. Plant Cell 18, 295–307 (2006).
pubmed: 16387832
pmcid: 1356540
doi: 10.1105/tpc.105.038398
Schlegel, J. et al. Control of arabidopsis shoot stem cell homeostasis by two antagonistic cle peptide signalling pathways. Elife https://doi.org/10.7554/eLife.70934 (2021).
Mayer, K. F. X. et al. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95, 805–815 (1998).
pubmed: 9865698
doi: 10.1016/S0092-8674(00)81703-1
Mandel, T.et al. Differential regulation of meristem size, morphology and organization by the ERECTA, CLAVATA and class III HD-ZIP pathways. Development 143, 1612–1622 (2016).
Kosentka, P. Z., Overholt, A., Maradiaga, R., Mitoubsi, O. & Shpak, E. D. EPFL signals in the boundary region of the SAM restrict its size and promote leaf initiation. Plant Physiol. 179, 265–279 (2019).
pubmed: 30409857
doi: 10.1104/pp.18.00714
Zhang, L., De Gennaro, D., Lin, G., Chai, J. & Shpak, E. D. ERECTA family signaling constrains CLAVATA3 and WUSCHEL to the center of the shoot apical meristem. Development 148, dev189753 (2021)
Bartrina, I., Otto, E., Strnad, M., Werner, T. & Schmülling, T. Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. Plant Cell 23, 69–80 (2011).
pubmed: 21224426
pmcid: 3051259
doi: 10.1105/tpc.110.079079
Chickarmane, V. S., Gordon, S. P., Tarr, P. T., Heisler, M. G. & Meyerowitz, E. M. Cytokinin signaling as a positional cue for patterning the apical-basal axis of the growing Arabidopsis shoot meristem. Proc. Natl Acad. Sci. USA 109, 4002–4007 (2012).
pubmed: 22345559
pmcid: 3309735
doi: 10.1073/pnas.1200636109
Leibfried, A. et al. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438, 1172–1175 (2005).
pubmed: 16372013
doi: 10.1038/nature04270
Brand, U., Fletcher, J. C., Hobe, M., Meyerowitz, E. M. & Simon, R. Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science (1979) 289, 617–619 (2000).
Fletcher, J. C. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science (1979) 283, 1911–1914 (1999).
Schoof, H. et al. The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100, 635–644 (2000).
pubmed: 10761929
doi: 10.1016/S0092-8674(00)80700-X
Rojo, E., Sharma, V. K., Kovaleva, V., Raikhel, N. V. & Fletcher, J. C. CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. Plant Cell 14, 969–977 (2002).
pubmed: 12034890
pmcid: 150600
doi: 10.1105/tpc.002196
Balanzà, V. et al. Genetic control of meristem arrest and life span in Arabidopsis by a FRUITFULL-APETALA2 pathway. Nat. Commun. 9, 565 (2018).
pubmed: 29422669
pmcid: 5805735
doi: 10.1038/s41467-018-03067-5
Lenhard, M., Bohnert, A., Jürgens, G. & Laux, T. Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between Wuschel and Agamous. Cell 105, 805–814 (2001).
pubmed: 11440722
doi: 10.1016/S0092-8674(01)00390-7
Lohmann, J. U. et al. A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105, 793–803 (2001).
pubmed: 11440721
doi: 10.1016/S0092-8674(01)00384-1
Wollmann, H., Mica, E., Todesco, M., Long, J. A. & Weigel, D. On reconciling the interactions between APETALA2, miR172 and AGAMOUS with the ABC model of flower development. Development 137, 3633–3642 (2010).
pubmed: 20876650
pmcid: 2964095
doi: 10.1242/dev.036673
Ó’Maoiléidigh, D. S. et al. Systematic analyses of the MIR172 family members of Arabidopsis define their distinct roles in regulation of APETALA2 during floral transition. PLoS Biol. 19, e3001043 (2021).
pubmed: 33529186
pmcid: 7853530
doi: 10.1371/journal.pbio.3001043
Bowman, J. L., Alvarez, J., Weigel, D., Meyerowitz, E. M. & Smyth, D. R. Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Development 119, 721–743 (1993).
doi: 10.1242/dev.119.3.721
Jofuku, K. D., Den Boer, B. G. W., Van Montagu, M. & Okamuro, J. K. Control of arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6, 1211–1225 (1994).
pubmed: 7919989
pmcid: 160514
Yant, L. et al. Orchestration of the floral transition and floral development in arabidopsis by the bifunctional transcription factor APETALA2. Plant Cell 22, 2156–2170 (2010).
pubmed: 20675573
pmcid: 2929098
doi: 10.1105/tpc.110.075606
Gruel, J. et al. An epidermis-driven mechanism positions and scales stem cell niches in plants. Sci Adv, 2, e1500989 (2016).
Laufs, P., Grandjean, O., Jonak, C., Kiêu, K. & Traas, J. Cellular parameters of the shoot apical meristem in Arabidopsis. Plant Cell 10, 1375–1389 (1998).
pubmed: 9707536
pmcid: 144064
doi: 10.1105/tpc.10.8.1375
Hartmann, U. et al. Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J. 21, 351–360 (2000).
pubmed: 10758486
doi: 10.1046/j.1365-313x.2000.00682.x
Yoo, S. K. et al. CONSTANS activates SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 through FLOWERING LOCUS T to promote flowering in Arabidopsis. Plant Physiol. 139, 770–778 (2005).
pubmed: 16183837
pmcid: 1255994
doi: 10.1104/pp.105.066928
Liu, C. et al. Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis. Development 135, 1481–1491 (2008).
pubmed: 18339670
doi: 10.1242/dev.020255
Chen, X. A MicroRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science (1979) 303, 2022–2025 (2004).
Huang, Z. et al. APETALA2 antagonizes the transcriptional activity of AGAMOUS in regulating floral stem cells in Arabidopsis thaliana. N. Phytologist 215, 1197–1209 (2017).
doi: 10.1111/nph.14151
Liu, X. et al. AUXIN RESPONSE FACTOR 3 integrates the functions of AGAMOUS and APETALA 2 in floral meristem determinacy. Plant J. 80, 629–641 (2014).
pubmed: 25187180
pmcid: 4215321
doi: 10.1111/tpj.12658
Chang, W., Guo, Y., Zhang, H., Liu, X. & Guo, L. Same actor in different stages: genes in shoot apical meristem maintenance and floral meristem determinacy in arabidopsis. Front. Ecol. Evol. 8, 89 (2020).
Schwab, R. et al. Specific effects of microRNAs on the plant transcriptome. Dev. Cell 8, 517–527 (2005).
pubmed: 15809034
doi: 10.1016/j.devcel.2005.01.018
Clyde, D. E. et al. A self-organizing system of repressor gradients establishes segmental oomplexity in Drosophila. Nature 426, 849–853 (2003).
pubmed: 14685241
doi: 10.1038/nature02189
Briscoe, J. & Small, S. Morphogen rules: design principles of gradient-mediated embryo patterning. Development 142, 3996–4009 (2015).
Briscoe, J., Pierani, A., Jessell, T. M. & Ericson, J. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101, 435–445 (2000).
pubmed: 10830170
doi: 10.1016/S0092-8674(00)80853-3
Sokolowski, T. R., Erdmann, T. & ten Wolde, P. R. Mutual repression enhances the steepness and precision of gene expression boundaries. PLoS Comput Biol. 8, e1002654 (2012).
pubmed: 22956897
pmcid: 3431325
doi: 10.1371/journal.pcbi.1002654
Kurihara, D., Mizuta, Y., Sato, Y. & Higashiyama, T. ClearSee: a rapid optical clearing reagent for whole-plant fluorescence imaging. Development 142, 4168–4179 (2015).
Musielak, T. J., Schenkel, L., Kolb, M., Henschen, A. & Bayer, M. A simple and versatile cell wall staining protocol to study plant reproduction. Plant Reprod. 28, 161–169 (2015).
pubmed: 26454832
pmcid: 4623088
doi: 10.1007/s00497-015-0267-1
Barbier de Reuille, P. et al. MorphoGraphX: a platform for quantifying morphogenesis in 4D. Elife 4, 1–20 (2015).
doi: 10.7554/eLife.05864
Kierzkowski, D. et al. Elastic domains regulate growth and organogenesis in the plant shoot apical meristem. Science (1979) 335, 1096–1099 (2012).
Formosa-Jordan, P. & Landrein, B. Quantifying gene expression domains in plant shoot apical meristems. In Flower Development: Methods and Protocols, 537–551, (Springer, 2023).
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
pubmed: 24695404
pmcid: 4103590
doi: 10.1093/bioinformatics/btu170
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10 (2011).
doi: 10.14806/ej.17.1.200
Patro, R., Duggal, G., Love, M. I., Irizarry, R. A. & Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14, 417–419 (2017).
pubmed: 28263959
pmcid: 5600148
doi: 10.1038/nmeth.4197
Zhang, R. et al. A high quality Arabidopsis transcriptome for accurate transcript-level analysis of alternative splicing. Nucleic Acids Res. 45, 5061–5073 (2017).
pubmed: 28402429
pmcid: 5435985
doi: 10.1093/nar/gkx267
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 25516281
pmcid: 4302049
doi: 10.1186/s13059-014-0550-8