Handling Editor: Ykä Helariutta
ABSTRACT
The differentiation of distinct cell types in appropriate patterns is a fundamental process in the development of multicellular organisms. In Arabidopsis thaliana, protoderm/epidermis differentiates as a single cell layer at the outermost position. However, little is known about the molecular nature of the positional signals that achieve correct epidermal cell differentiation. Here, we propose that very-long-chain fatty acid-containing ceramides (VLCFA-Cers) mediate positional signals by stimulating the function of ARABIDOPSIS THALIANA MERISTEM LAYER1 (ATML1), a master regulator of protoderm/epidermis differentiation, during lateral root development. We show that VLCFA-Cers, which are synthesized predominantly in the outermost cells, bind to the lipid-binding domain of ATML1. Importantly, this cell type-specific protein-lipid association alters the activity of ATML1 protein and consequently restricts its expression to the protoderm/epidermis through a transcriptional feedback loop. Furthermore, establishment of a compartment, enriched with VLCFA-containing sphingolipids, at the outer lateral membrane facing the external environment may function as a determinant of protodermal cell fate. Taken together, our results indicate that VLCFA-Cers play a pivotal role in directing protoderm/epidermis differentiation by mediating positional signals to ATML1.
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Footnotes
Competing interests
The authors declare no competing or financial interests.
Author contributions
Conceptualization: K.N., M.A.; Methodology: M.A.; Investigation: K.N., T.I., M.K.-Y., M.A.; Resources: K.N., M.A.; Writing - original draft: K.N., M.A.; Writing - review & editing: K.N., T.I., M.K.-Y., T.T., M.A.; Supervision: M.K.-Y., T.T., M.A.; Funding acquisition: K.N., M.A.
Funding
This work is supported by the Ministry of Education, Culture, Sports, Science and Technology (MEXT) [Grants-in-Aid for Scientific Research (C) 26440133 and 19K06703 to M.A.], by the NOVARTIS Foundation (Japan) for the Promotion of Science (37246 to M.A.) and by Japan Society for the Promotion of Science (19J12442 to K.N.).
Supplementary information
Supplementary information available online at https://dev.biologists.org/lookup/doi/10.1242/dev.194969.supplemental
- Received July 14, 2020.
- Accepted December 4, 2020.
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