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Cell type-specific attenuation of brassinosteroid signaling precedes stomatal asymmetric cell division

Kim Eunji (UGent) , Cheng Zhang, Boyu Guo (UGent) , Thomas Eekhout (UGent) , Anaxi Houbaert, Jos Wendrich (UGent) , Niels Vandamme (UGent) , Manish Tiwari (UGent) , Claire Simon--Vezo (UGent) , Isabelle Vanhoutte (UGent) , et al.
(2023) PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 120(36).
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Abstract
In Arabidopsis thaliana, brassinosteroid (BR) signaling and stomatal development are connected through the SHAGGY/GSK3-like kinase BR INSENSITIVE2 (BIN2). BIN2 is a key negative regulator of BR signaling but it plays a dual role in stomatal development. BIN2 promotes or restricts stomatal asymmetric cell division (ACD) depending on its subcellular localization, which is regulated by the stomatal lineage-specific scaffold protein POLAR. BRs inactivate BIN2, but how they govern stomatal development remains unclear. Mapping the single-cell transcriptome of stomatal lineages after triggering BR signaling with either exogenous BRs or the specific BIN2 inhibitor, bikinin, revealed that the two modes of BR signaling activation generate spatiotemporally distinct transcriptional responses. We established that BIN2 is always sensitive to the inhibitor but, when in a complex with POLAR and its closest homolog POLAR-LIKE1, it becomes protected from BR-mediated inactivation. Subsequently, BR signaling in ACD precursors is attenuated, while it remains active in epidermal cells devoid of scaffolds and undergoing differentiation. Our study demonstrates how scaffold proteins contribute to cellular signal specificity of hormonal responses in plants.
Keywords
Arabidopsis, asymmetric cell division, brassinosteroids, single-cell RNA sequencing, stomatal development, TRANSCRIPTION FACTOR, GSK3-LIKE KINASES, GENE-EXPRESSION, ARABIDOPSIS, LINEAGE, DIFFERENTIATION, TERMINATION, INHIBITION, SPEECHLESS, COMPONENT

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MLA
Eunji, Kim, et al. “Cell Type-Specific Attenuation of Brassinosteroid Signaling Precedes Stomatal Asymmetric Cell Division.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 120, no. 36, 2023, doi:10.1073/pnas.2303758120.
APA
Eunji, K., Zhang, C., Guo, B., Eekhout, T., Houbaert, A., Wendrich, J., … Russinova, E. (2023). Cell type-specific attenuation of brassinosteroid signaling precedes stomatal asymmetric cell division. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 120(36). https://doi.org/10.1073/pnas.2303758120
Chicago author-date
Eunji, Kim, Cheng Zhang, Boyu Guo, Thomas Eekhout, Anaxi Houbaert, Jos Wendrich, Niels Vandamme, et al. 2023. “Cell Type-Specific Attenuation of Brassinosteroid Signaling Precedes Stomatal Asymmetric Cell Division.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 120 (36). https://doi.org/10.1073/pnas.2303758120.
Chicago author-date (all authors)
Eunji, Kim, Cheng Zhang, Boyu Guo, Thomas Eekhout, Anaxi Houbaert, Jos Wendrich, Niels Vandamme, Manish Tiwari, Claire Simon--Vezo, Isabelle Vanhoutte, Yvan Saeys, Kun Wang, Yuxian Zhu, Bert De Rybel, and Eugenia Russinova. 2023. “Cell Type-Specific Attenuation of Brassinosteroid Signaling Precedes Stomatal Asymmetric Cell Division.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 120 (36). doi:10.1073/pnas.2303758120.
Vancouver
1.
Eunji K, Zhang C, Guo B, Eekhout T, Houbaert A, Wendrich J, et al. Cell type-specific attenuation of brassinosteroid signaling precedes stomatal asymmetric cell division. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2023;120(36).
IEEE
[1]
K. Eunji et al., “Cell type-specific attenuation of brassinosteroid signaling precedes stomatal asymmetric cell division,” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 120, no. 36, 2023.
@article{01H9ZV257FJR5CBFFZ2Q6RYG0F,
  abstract     = {{In Arabidopsis thaliana, brassinosteroid (BR) signaling and stomatal development are connected through the SHAGGY/GSK3-like kinase BR INSENSITIVE2 (BIN2). BIN2 is a key negative regulator of BR signaling but it plays a dual role in stomatal development. BIN2 promotes or restricts stomatal asymmetric cell division (ACD) depending on its subcellular localization, which is regulated by the stomatal lineage-specific scaffold protein POLAR. BRs inactivate BIN2, but how they govern stomatal development remains unclear. Mapping the single-cell transcriptome of stomatal lineages after triggering BR signaling with either exogenous BRs or the specific BIN2 inhibitor, bikinin, revealed that the two modes of BR signaling activation generate spatiotemporally distinct transcriptional responses. We established that BIN2 is always sensitive to the inhibitor but, when in a complex with POLAR and its closest homolog POLAR-LIKE1, it becomes protected from BR-mediated inactivation. Subsequently, BR signaling in ACD precursors is attenuated, while it remains active in epidermal cells devoid of scaffolds and undergoing differentiation. Our study demonstrates how scaffold proteins contribute to cellular signal specificity of hormonal responses in plants.}},
  articleno    = {{e2303758120}},
  author       = {{Eunji, Kim and Zhang, Cheng and Guo, Boyu and Eekhout, Thomas and Houbaert, Anaxi and Wendrich, Jos and Vandamme, Niels and Tiwari, Manish and Simon--Vezo, Claire and Vanhoutte, Isabelle and Saeys, Yvan and Wang, Kun and Zhu, Yuxian and De Rybel, Bert and Russinova, Eugenia}},
  issn         = {{0027-8424}},
  journal      = {{PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA}},
  keywords     = {{Arabidopsis,asymmetric cell division,brassinosteroids,single-cell RNA sequencing,stomatal development,TRANSCRIPTION FACTOR,GSK3-LIKE KINASES,GENE-EXPRESSION,ARABIDOPSIS,LINEAGE,DIFFERENTIATION,TERMINATION,INHIBITION,SPEECHLESS,COMPONENT}},
  language     = {{eng}},
  number       = {{36}},
  pages        = {{12}},
  title        = {{Cell type-specific attenuation of brassinosteroid signaling precedes stomatal asymmetric cell division}},
  url          = {{http://doi.org/10.1073/pnas.2303758120}},
  volume       = {{120}},
  year         = {{2023}},
}
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