Arabidopsis LATERAL ORGAN BOUNDARIES negatively regulates brassinosteroid accumulation to limit growth in organ boundaries
Open accessAbstract
Leaves and flowers begin life as outgrowths from the edges of shoot apical meristems. Stem cell divisions in the meristem center replenish cells that are incorporated into organ primordia at the meristem periphery and leave the meristem. Organ boundaries, regions of limited growth that separate forming organs from the meristem, serve to isolate these two domains and are critical for coordination of organogenesis and meristem maintenance. Boundary formation and maintenance are poorly understood processes, despite the identification of a number of boundary-specific transcription factors. Here we provide genetic and biochemical evidence that the Arabidopsis thaliana transcription factor LATERAL ORGAN BOUNDARIES (LOB) negatively regulates accumulation of the plant steroid hormone brassinosteroid (BR) in organ boundaries. We found that ectopic expression of LOB results in reduced BR responses. We identified BAS1 , which encodes a BR-inactivating enzyme, as a direct target of LOB transcriptional activation. Loss-of-function lob mutants exhibit organ fusions, and this phenotype is suppressed by expression of BAS1 under the LOB promoter, indicating that BR hyperaccumulation contributes to the lob mutant phenotype. In addition, LOB expression is BR regulated; therefore, LOB and BR form a feedback loop to modulate local BR accumulation in organ boundaries to limit growth in the boundary domain.
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Low brassinosteroid activity in the boundary zone allows the induction of CUC genes.
“Thus, low brassinosteroid activity in the boundary zone not only reduces cell expansion and division as described above, but also allows the induction of CUC genes (Bell et al., 2012; Gendron et al., 2012).”
From Shaping plant architecture (2015) · cites this paper as Bell et al., 2012
LOB1-mediated decrease of brassinosteroid activity causes a reduction of cell size and cell division rate in the boundary zone compared to neighboring zones.
“The LOB1-mediated decrease of brassinosteroid activity causes a reduction of cell size and cell division rate in the boundary zone compared to neighboring zones (Bell et al., 2012; Gendron et al., 2012).”
From Shaping plant architecture (2015) · cites this paper as Bell et al., 2012
CUC genes are down-regulated by brassinosteroids.
“CUC genes are down-regulated by brassinosteroids.”
From Shaping plant architecture (2015) · cites this paper as Bell et al., 2012
LOB1 induces the expression of BAS1, which encodes a brassinosteroid-inactivating protein.
“A key factor during establishment of the boundary zone is the transcription factor LATERAL ORGAN BOUNDARIES1 (LOB1) that induces the expression of BAS1, encoding a protein that has brassinosteroid inactivating activity (Bell et al., 2012).”
From Shaping plant architecture (2015) · cites this paper as Bell et al., 2012
LOB expression is regulated by BRs.
“Furthermore, LOB expression is regulated by BRs (Bell et al., 2012).”
From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Bell et al., 2012
Cites
Smyth, G. K. (2004) · Statistical Applications in Genetics and Molecular Biology · doi:10.2202/1544-6115.1027 · Cited by 11,829 · see citing works
Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant.
Aida, M., Ishida, T., Fukaki, H., Fujisawa, H., & Tasaka, M. (1997) · The Plant Cell · doi:10.1105/tpc.9.6.841 · Cited by 1,486 · see citing works
Greb, T., Clarenz, O., Schäfer, E., Müller, D., Herrero, R., Schmitz, G., & Theres, K. (2003) · Genes & Development · doi:10.1101/gad.260703 · Cited by 541 · see citing works
Gendron, J. M., Liu, J.-S., Fan, M., Bai, M.-Y., Wenkel, S., Springer, P. S., Barton, M. K., & Wang, Z.-Y. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210799110 · Cited by 205 · see citing works
Self-citationBorghi, L., Bureau, M., & Simon, R. (2007) · The Plant Cell · doi:10.1105/tpc.106.047159 · Cited by 161 · see citing works
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Teichmann, T., & Muhr, M. (2015) · Frontiers in Plant Science · doi:10.3389/fpls.2015.00233 · Cited by 228 · see citing works
“The LOB1-mediated decrease of brassinosteroid activity causes a reduction of cell size and cell division rate in the boundary zone compared to neighboring zones (Bell et al., 2012; Gendron et al., 2012).”
BackgroundGendron, J. M., Liu, J.-S., Fan, M., Bai, M.-Y., Wenkel, S., Springer, P. S., Barton, M. K., & Wang, Z.-Y. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210799110 · Cited by 205 · see citing works
Self-citationHow boundaries control plant development
Žádníková, P., & Simon, R. (2014) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2013.11.013 · Cited by 121 · see citing works
<i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems
Wang, Q., Hasson, A., Rossmann, S., & Theres, K. (2016) · New Phytologist · doi:10.1111/nph.13641 · Cited by 106 · see citing works
- Authors
- Bell, E. M., Lin, W.-C., Husbands, A. Y., Yu, L., Jaganatha, V., Jablonska, B., Mangeon, A., Neff, M. M., Girke, T., & Springer, P. S.
- Affiliations
- University of California, Riverside (US)
- Department of Botany and Plant Sciences, Center for Plant Cell Biology, University of California, Riverside, CA 92521; and
- Washington State University (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-12-04
- Volume
- 109
- Issue
- 51
- Pages
- 21146-21151
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3529045
- OpenAlex
- W2029822970
- Cited by
- 194
- References
- 5
- Citations by year
- 2026: 5 · 2025: 13 · 2024: 12 · 2023: 12 · 2022: 10 · 2021: 22 · 2020: 14 · 2019: 19 · 2018: 10 · 2017: 16 · 2016: 12 · 2015: 22 · 2014: 11 · 2013: 15 · 2012: 1
- FWCI
- 17.91
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- Funders
- National Science Foundation (0420202)
- U.S. Department of Energy (DE‐FG02‐, FG02-05ER15649)
- Basic Energy Sciences (DE-FG02)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Parasitism and Resistance
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant tissue culture and regeneration
- Keywords
- brassinosteroids, organ boundaries, BAS1, transcriptional regulation, shoot apical meristem, organogenesis, feedback loops, Arabidopsis thaliana
- MeSH terms
- Alleles, Models, Genetic, Mutation, Phenotype, Plants, Promoter Regions, Genetic, Time Factors, Transcription, Genetic, Genes, Plant, Arabidopsis, Gene Expression Regulation, Plant, Arabidopsis Proteins, Brassinosteroids
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