Post-Embryonic Lateral Organ Development and Adaxial-Abaxial Polarity Are Regulated by the Combined Effect of ENHANCER OF SHOOT REGENERATION 1 and WUSCHEL in Arabidopsis Shoots
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
17-23702S
Grantová Agentura České Republiky
18-23972Y
Grantová Agentura České Republiky
CZ.02.1.01/0.0/0.0/16_019/0000827
European Regional Development Fund
FY2019
IROAST research unit plant stem cells and regeneration
PubMed
34638958
PubMed Central
PMC8508843
DOI
10.3390/ijms221910621
PII: ijms221910621
Knihovny.cz E-zdroje
- Klíčová slova
- Arabidopsis thaliana, ENHANCER OF SHOOT REGENERATION 1, REVOLTA, SHOOTMERISTEMLESS, WUSCHEL, adaxial–abaxial polarity, lateral organ, shoot apical meristem,
- MeSH
- Arabidopsis genetika růst a vývoj MeSH
- fenotyp MeSH
- homeodoménové proteiny genetika MeSH
- listy rostlin genetika růst a vývoj MeSH
- meristém genetika růst a vývoj MeSH
- mutace MeSH
- organogeneze rostlin genetika MeSH
- proteiny huseníčku genetika MeSH
- regulace genové exprese u rostlin * MeSH
- rostlinné geny * MeSH
- transkripční faktory genetika MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- ESR1 protein, Arabidopsis MeSH Prohlížeč
- homeodoménové proteiny MeSH
- proteiny huseníčku MeSH
- transkripční faktory MeSH
- WUSCHEL protein, Arabidopsis MeSH Prohlížeč
The development of above-ground lateral organs is initiated at the peripheral zone of the shoot apical meristem (SAM). The coordination of cell fate determination and the maintenance of stem cells are achieved through a complex regulatory network comprised of transcription factors. Two AP2/ERF transcription factor family genes, ESR1/DRN and ESR2/DRNL/SOB/BOL, regulate cotyledon and flower formation and de novo organogenesis in tissue culture. However, their roles in post-embryonic lateral organ development remain elusive. In this study, we analyzed the genetic interactions among SAM-related genes, WUS and STM, two ESR genes, and one of the HD-ZIP III members, REV, whose protein product interacts with ESR1 in planta. We found that esr1 mutations substantially enhanced the wus and stm phenotypes, which bear a striking resemblance to those of the wus rev and stm rev double mutants, respectively. Aberrant adaxial-abaxial polarity is observed in wus esr1 at relatively low penetrance. On the contrary, the esr2 mutation partially suppressed stm phenotypes in the later vegetative phase. Such complex genetic interactions appear to be attributed to the distinct expression pattern of two ESR genes because the ESR1 promoter-driving ESR2 is capable of rescuing phenotypes caused by the esr1 mutation. Our results pose the unique genetic relevance of ESR1 and the SAM-related gene interactions in the development of rosette leaves.
Zobrazit více v PubMed
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. 2000;289:617–619. doi: 10.1126/science.289.5479.617. PubMed DOI
Schoof H., Lenhard M., Haecker A., Mayer K.F.X., Jürgens G., Laux T. The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell. 2000;100:635–644. doi: 10.1016/S0092-8674(00)80700-X. PubMed DOI
Laux T., Mayer K.F.X., Berger J., Jürgens G. The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development. 1996;122:87–96. doi: 10.1242/dev.122.1.87. PubMed DOI
Lee C., Clark S.E. A WUSCHEL-independent stem cell specification pathway is repressed by PHB, PHV and CNA in arabidopsis. PLoS ONE. 2015;10:1–19. doi: 10.1371/journal.pone.0126006. PubMed DOI PMC
Huang W., Pitorre D., Poretska O., Marizzi C., Winter N., Poppenberger B., Sieberer T. Altered meristem programSuppresses ectopic stem cell niche formation in the shoot apical meristem in a largely cytokinin-independent manner. Plant Physiol. 2015;167:1471–1486. doi: 10.1104/pp.114.254623. PubMed DOI PMC
Jung J.H., Park C.M. MIR166/165 genes exhibit dynamic expression patterns in regulating shoot apical meristem and floral development in Arabidopsis. Planta. 2007;225:1327–1338. doi: 10.1007/s00425-006-0439-1. PubMed DOI
Williams L., Grigg S.P., Xie M., Christensen S., Fletcher J.C. Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development. 2005;132:3657–3668. doi: 10.1242/dev.01942. PubMed DOI
Otsuga D., DeGuzman B., Prigge M.J., Drews G.N., Clark S.E. REVOLUTA regulates meristem initiation at lateral positions. Plant J. 2001;25:223–236. doi: 10.1046/j.1365-313x.2001.00959.x. PubMed DOI
Emery J.F., Floyd S.K., Alvarez J., Eshed Y., Hawker N.P., Izhaki A., Baum S.F., Bowman J.L. Radial Patterning of Arabidopsis Shoots by Class III HD-ZIP and KANADI Genes. Curr. Biol. 2003;13:1768–1774. doi: 10.1016/j.cub.2003.09.035. PubMed DOI
Prigge M.J., Otsuga D., Alonso J.M., Ecker J.R., Drews G.N., Clark S.E. Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell. 2005;17:61–76. doi: 10.1105/tpc.104.026161. PubMed DOI PMC
Banno H., Ikeda Y., Niu Q.W., Chua N.H. Overexpression of Arabidopsis ESR1 induces initiation of Shoot Regeneration. Plant Cell. 2001;13:2609–2618. doi: 10.1105/tpc.010234. PubMed DOI PMC
Kirch T., Simon R., Grünewald M., Werr W. The Dornröschen/enhancer of shoot regeneration1: Gene of Arabidopsis acts in the control of meristem cell fate and lateral organ development. Plant Cell. 2003;15:694–705. doi: 10.1105/tpc.009480. PubMed DOI PMC
Ikeda Y., Banno H., Niu Q.-W., Howell S.H., Chua N.-H. The enhancer of shoot regeneration 2 gene in Arabidopsis regulates cup-shaped cotyledon 1 at the transcriptional level and controls cotyledon development. Plant Cell Physiol. 2006;47:1443–1456. doi: 10.1093/pcp/pcl023. PubMed DOI
Ward J.M., Smith A.M., Shah P.K., Galanti S.E., Yi H., Demianski A.J., Van Der Graaff E., Keller B., Neff M.M. A new role for the Arabidopis AP2 transcription factor, leafy petiole, in gibberellin-induced germination is revealed by the misexpression of a homologous gene SOB2/DRN-LIKE. Plant Cell. 2006;18:29–39. doi: 10.1105/tpc.105.036707. PubMed DOI PMC
Marsch-Martinez N., Greco R., Becker J.D., Dixit S., Bergervoet J.H.W., Karaba A., De Folter S., Pereira A. BOLITA, an Arabidopsis AP2/ERF-like transcription factor that affects cell expansion and proliferation/differentiation pathways. Plant Mol. Biol. 2006;62:825–843. doi: 10.1007/s11103-006-9059-1. PubMed DOI
Capua Y., Eshed Y. Coordination of auxin-triggered leaf initiation by tomato LEAFLESS. Proc. Natl. Acad. Sci. USA. 2017;114:3246–3251. doi: 10.1073/pnas.1617146114. PubMed DOI PMC
Chandler J.W., Cole M., Flier A., Grewe B., Werr W. The AP2 transcription factors DORNRÖSCHEN and Dornröschen-like redundantly control Arabidopsis embryo patterning via interaction with PHAVOLUTA. Development. 2007;134:1653–1662. doi: 10.1242/dev.001016. PubMed DOI
Durán-Medina Y., Serwatowska J., Reyes-Olalde J.I., De Folter S., Marsch-Martínez N. The AP2/ERF transcription factor DRNL modulates gynoecium development and affects its response to Cytokinin. Front. Plant Sci. 2017;8:1–13. doi: 10.3389/fpls.2017.01841. PubMed DOI PMC
Nag A., Yang Y., Jack T. DORNRÖSCHEN-LIKE, an AP2 gene, is necessary for stamen emergence in Arabidopsis. Plant Mol. Biol. 2007;65:219–232. doi: 10.1007/s11103-007-9210-7. PubMed DOI
Matsuo N., Makino M., Banno H. Arabidopsis ENHANCER OF SHOOT REGENERATION (ESR)1 and ESR2 regulate in vitro shoot regeneration and their expressions are differentially regulated. Plant Sci. 2011;181:39–46. doi: 10.1016/j.plantsci.2011.03.007. PubMed DOI
Matsuo N., Mase H., Makino M., Takahashi H., Banno H. Identification of enhancer of shoot regeneration 1-upregulated genes during in vitro shoot regeneration. Plant Biotechnol. 2009;26:385–393. doi: 10.5511/plantbiotechnology.26.385. DOI
Tian C., Zhang X., He J., Yu H., Wang Y., Shi B., Han Y., Wang G., Feng X., Zhang C., et al. An organ boundary-enriched gene regulatory network uncovers regulatory hierarchies underlying axillary meristem initiation. Mol. Syst. Biol. 2014;10:755. doi: 10.15252/msb.20145470. PubMed DOI PMC
Zhang C., Wang J., Wenkel S., Chandler J.W., Werr W., Jiao Y. Spatiotemporal control of axillary meristem formation by interacting transcriptional regulators. Development. 2018;145:dev158352. doi: 10.1242/dev.158352. PubMed DOI PMC
Kubalová I., Zalabák D., Mičúchová A., Ikeda Y. Mutations in tetrapyrrole biosynthesis pathway uncouple nuclear WUSCHEL expression from de novo shoot development in Arabidopsis. Plant Cell Tissue Organ Cult. 2019;139:395–401. doi: 10.1007/s11240-019-01680-w. DOI
Magnani E., Barton M.K. A Per-ARNT-sim-like sensor domain uniquely regulates the activity of the homeodomain leucine zipper transcription factor REVOLUTA in Arabidopsis. Plant Cell. 2011;23:567–582. doi: 10.1105/tpc.110.080754. PubMed DOI PMC
Takano S., Niihama M., Smith H.M.S., Tasaka M., Aida M. Gorgon, a novel missense mutation in the shoot meristemless gene, impairs shoot meristem homeostasis in arabidopsis. Plant Cell Physiol. 2010;51:621–634. doi: 10.1093/pcp/pcq028. PubMed DOI
Campisi L., Yang Y., Yi Y., Heilig E., Herman B., Cassista A.J., Allen D.W., Xiang H., Jack T. Generation of enhancer trap lines in Arabidopsis and characterization of expression patterns in the inflorescence. Plant J. 1999;17:699–707. doi: 10.1046/j.1365-313X.1999.00409.x. PubMed DOI
Glowa D., Comelli P., Chandler J.W., Werr W. Clonal sector analysis and cell ablation confirm a function for DORNROESCHEN-LIKE in founder cells and the vasculature in Arabidopsis. Planta. 2021;253:1–16. doi: 10.1007/s00425-020-03545-5. PubMed DOI PMC
Caggiano M.P., Yu X., Bhatia N., Larsson A., Ram H., Ohno C.K., Sappl P., Meyerowitz E.M., Jönsson H., Heisler M.G. Cell type boundaries organize plant development. Elife. 2017;6:1–32. doi: 10.7554/eLife.27421. PubMed DOI PMC
Su Y.H., Zhou C., Li Y.J., Yu Y., Tang L.P., Zhang W.J., Yao W.J., Huang R., Laux T., Zhang X.S. Integration of pluripotency pathways regulates stem cell maintenance in the arabidopsis shoot meristem. Proc. Natl. Acad. Sci. USA. 2020;117:22561–22571. doi: 10.1073/pnas.2015248117. PubMed DOI PMC
Heisler M.G., Ohno C., Das P., Sieber P., Reddy G.V., Long J.A., Meyerowitz E.M. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr. Biol. 2005;15:1899–1911. doi: 10.1016/j.cub.2005.09.052. PubMed DOI
Luo L., Zeng J., Wu H., Tian Z., Zhao Z. A Molecular Framework for Auxin-Controlled Homeostasis of Shoot Stem Cells in Arabidopsis. Mol. Plant. 2018;11:899–913. doi: 10.1016/j.molp.2018.04.006. PubMed DOI
Fu Y., Xu L., Xu B., Yang L., Ling Q., Wang H., Huang H. Genetic interactions between leaf polarity-controlling genes and ASYMMETRIC LEAVES1 and 2 in Arabidopsis leaf patterning. Plant Cell Physiol. 2007;48:724–735. doi: 10.1093/pcp/pcm040. PubMed DOI
Xu L., Xu Y., Dong A., Sun Y., Pi L., Xu Y., Huang H. Novel as1 and as2 defects in leaf adaxial-abaxial polarity reveal the requirement for ASYMMETRIC LEAVES1 and 2 and ERECTA functions in specifying leaf adaxial identity. Development. 2003;130:4097–4107. doi: 10.1242/dev.00622. PubMed DOI
Qi Y., Sun Y., Xu L., Xu Y., Huang H. ERECTA is required for protection against heat-stress in the AS1/AS2 pathway to regulate adaxial-abaxial leaf polarity in Arabidopsis. Planta. 2004;219:270–276. doi: 10.1007/s00425-004-1248-z. PubMed DOI
Xu M., Du Q., Tian C., Wang Y., Jiao Y. Stochastic gene expression drives mesophyll protoplast regeneration. Sci. Adv. 2021;7:eabg8466. doi: 10.1126/sciadv.abg8466. PubMed DOI PMC
Xiang D., Yang H., Venglat P., Cao Y., Wen R., Ren M., Stone S., Wang E., Wang H., Xiao W., et al. POPCORN functions in the auxin pathway to regulate embryonic body plan and meristem organization in Arabidopsis. Plant Cell. 2011;23:4348–4367. doi: 10.1105/tpc.111.091777. PubMed DOI PMC
Mayer K.F., Schoof H., Haecker A., Lenhard M., Jurgens G., Laux T. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell. 1998;95:805–815. doi: 10.1016/S0092-8674(00)81703-1. PubMed DOI
Turchi L., Carabelli M., Ruzza V., Possenti M., Sassi M., Peñalosa A., Sessa G., Salvi S., Forte V., Morelli G., et al. Arabidopsis HD-Zip II transcription factors control apical embryo development and meristem function. Development. 2013;140:2118–2129. doi: 10.1242/dev.092833. PubMed DOI
Aida M., Ishida T., Fukaki H., Fujisawa H., Tasaka M. Genes involved in organ separation in Arabidopsis: An analysis of the cup-shaped cotyledon mutant. Plant Cell. 1997;9:841–857. doi: 10.1105/tpc.9.6.841. PubMed DOI PMC