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Endoplasmic reticulum (ER)–derived organelles, ER bodies, participate in the defense against herbivores in Brassicaceae plants. ER bodies accumulate β-glucosidases, which hydrolyze specialized thioglucosides known as glucosinolates to generate bioactive substances. In Arabidopsis thaliana , the leaf ER (LER) bodies are formed in large pavement cells, which are found in the petioles, margins and blades of rosette leaves. However, the regulatory mechanisms involved in establishing large pavement cells are unknown. Here, we show that the ARABIDOPSIS THALIANA MERISTEM L1 LAYER (ATML1) transcription factor regulates the formation of LER bodies in large pavement cells of rosette leaves. Overexpression of ATML1 enhanced the expression of LER body–related genes and the number of LER body–containing large pavement cells, whereas its knock-out resulted in opposite effects. ATML1 enhances endoreduplication and cell size through LOSS OF GIANT CELLS FROM ORGANS (LGO). Although the overexpression and knock-out of LGO affected the appearance of large pavement cells in Arabidopsis , the effect on LER body–related gene expression and LER body formation was weak. LER body–containing large pavement cells were also found in Eutrema salsugineum , another Brassicaceae species. Our results demonstrate that ATML1 establishes large pavement cells to induce LER body formation in Brassicaceae plants and thereby possibly contribute to the defense against herbivores. [ABSTRACT FROM AUTHOR]

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 verylong- 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 VLCFAcontaining 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. [ABSTRACT FROM AUTHOR]

The chance to watch floral organs develop live is not to be missed! Here, we outline reasons why quantitative, live-cell imaging is an important approach to study floral morphogenesis, and provide a basic workflow of how to get started. We highlight key advances in morphodynamics of lateral organ development, and discuss recent work that uses live confocal imaging to address the regulation of floral organ number, its robustness, and patterning mechanisms that exploit stochasticity. [ABSTRACT FROM AUTHOR]

The cloning of the ATML1 gene, encoding an HD-ZIP class IV transcription factor, was first reported in 1996. Because ATML1 mRNA was preferentially detected in the shoot epidermis, cis-regulatory sequences of ATML1 have been used to drive gene expression in the outermost cells of the shoot apical meristem and leaves, even before the function of ATML1 was understood. Later studies revealed that ATML1 is required for developmental processes related to shoot epidermal specification and differentiation. Consistent with its central role in epidermal development, ATML1 activity has been revealed to be restricted to the outermost cells via several regulatory mechanisms. In this review, we look back on the history of ATML1 research and provide a perspective for future studies.

Cell fate determination in plants relies on positional cues. To investigate the position-dependent gene regulation in plants, we focused on shoot epidermal cell specification, which occurs only in the outermost cells. ATML1, which encodes an HD-ZIP class IV transcription factor, is a positive regulator of shoot epidermal cell identity. Despite the presence of a weak ATML1 promoter activity in the inner cells, ATML1 protein was detected mostly in the outermost cells, which suggests that ATML1 accumulation is inhibited in the inner cells. ATML1 nuclear localization was reduced in the epidermis and therewas a positive, albeit weak, correlation between the amount of ATML1 in the nuclei and the expression of a direct target of ATML1. Nuclear accumulation of ATML1 was more strongly inhibited in the inner cells than in the outermost cells. Domain deletion analyses revealed that the ZLZ-coding sequence was necessary and partially sufficient for the post-transcriptional repression of ATML1. Our results suggest that post-transcriptional repressions contribute to the restriction of master transcriptional regulator activity in specific cells to enable position-dependent cell differentiation. [ABSTRACT FROM AUTHOR]

Multicellular development produces patterns of specialized cell types. Yet, it is often unclear how individual cells within a field of identical cells initiate the patterning process. Using live imaging, quantitative image analyses and modeling, we show that during Arabidopsis thaliana sepal development, fluctuations in the concentration of the transcription factor ATML1 pattern a field of identical epidermal cells to differentiate into giant cells interspersed between smaller cells. We find that ATML1 is expressed in all epidermal cells. However, its level fluctuates in each of these cells. If ATML1 levels surpass a threshold during the G2 phase of the cell cycle, the cell will likely enter a state of endoreduplication and become giant. Otherwise, the cell divides. Our results demonstrate a fluctuation-driven patterning mechanism for how cell fate decisions can be initiated through a random yet tightly regulated process.

Growth and developmental processes are occasionally accompanied by multiple rounds of DNA replication, known as endoreduplication. Coordination between endoreduplication and cell size regulation often plays a crucial role in proper organogenesis and cell differentiation. Here, we report that the level of correlation between ploidy and cell volume is different in the outer and inner cell layers of leaves of Arabidopsis thaliana using a novel imaging technique. Although there is a well-known, strong correlation between ploidy and cell volume in pavement cells of the epidermis, this correlation was extremely weak in palisade mesophyll cells. Induction of epidermis cell identity based on the expression of the homeobox gene ATML1 in mesophyll cells enhanced the level of correlation between ploidy and cell volume to near that of wild-type epidermal cells. We therefore propose that the correlation between ploidy and cell volume is regulated by cell identity. [ABSTRACT FROM AUTHOR]

The epidermis of shoot organs in plants develops from the outermost layer (L1) of the shoot apical meristem. In Arabidopsis, a pair of homeobox genes, ARABIDOPSIS THALIANA MERISTEM LAYER1 (ATML1) and PROTODERMAL FACTOR2 (PDF2), play a role in regulating the expression of L1-specific genes. atml1-1 pdf2-1 double mutants show striking defects in the differentiation of shoot epidermal cells. However, because atml1-1 and pdf2-1 have a T-DNA inserted downstream of the respective homeobox sequences, these alleles may not represent null mutations. Here we characterized additional mutant alleles that have a T-DNA insertion at different positions of each gene. Double mutants of a strong atml1-3 allele with each pdf2 allele were found to cause embryonic arrest at the globular stage. Although with low frequency, all double mutant combinations of a weak atml1-1 allele with each pdf2 allele germinated and showed phenotypes defective in shoot epidermal cell differentiation. We further confirmed that transgenic induction of PDF2 fused to the Drosophila Engrailed repressor domain temporarily interferes with epidermal cell differentiation in the wild-type background. These results indicate that ATML1 and PDF2 act redundantly as a positive regulator of shoot epidermal cell differentiation and at least one copy of these genes is essential for embryo development. [ABSTRACT FROM AUTHOR]

The cloning of the ATML1 gene, encoding an HD-ZIP class IV transcription factor, was first reported in 1996. Because ATML1 mRNA was preferentially detected in the shoot epidermis, cis-regulatory sequences of ATML1 have been used to drive gene expression in the outermost cells of the shoot apical meristem and leaves, even before the function of ATML1 was understood. Later studies revealed that ATML1 is required for developmental processes related to shoot epidermal specification and differentiation. Consistent with its central role in epidermal development, ATML1 activity has been revealed to be restricted to the outermost cells via several regulatory mechanisms. In this review, we look back on the history of ATML1 research and provide a perspective for future studies., Competing Interests: The authors declare no conflict of interest.

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.This article has an associated 'The people behind the papers' interview., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2021. Published by The Company of Biologists Ltd.)

Cell fate determination in plants relies on positional cues. To investigate the position-dependent gene regulation in plants, we focused on shoot epidermal cell specification, which occurs only in the outermost cells. ATML1 , which encodes an HD-ZIP class IV transcription factor, is a positive regulator of shoot epidermal cell identity. Despite the presence of a weak ATML1 promoter activity in the inner cells, ATML1 protein was detected mostly in the outermost cells, which suggests that ATML1 accumulation is inhibited in the inner cells. ATML1 nuclear localization was reduced in the epidermis and there was a positive, albeit weak, correlation between the amount of ATML1 in the nuclei and the expression of a direct target of ATML1. Nuclear accumulation of ATML1 was more strongly inhibited in the inner cells than in the outermost cells. Domain deletion analyses revealed that the ZLZ-coding sequence was necessary and partially sufficient for the post-transcriptional repression of ATML1 Our results suggest that post-transcriptional repressions contribute to the restriction of master transcriptional regulator activity in specific cells to enable position-dependent cell differentiation., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2019. Published by The Company of Biologists Ltd.)

Multicellular development produces patterns of specialized cell types. Yet, it is often unclear how individual cells within a field of identical cells initiate the patterning process. Using live imaging, quantitative image analyses and modeling, we show that during Arabidopsis thaliana sepal development, fluctuations in the concentration of the transcription factor ATML1 pattern a field of identical epidermal cells to differentiate into giant cells interspersed between smaller cells. We find that ATML1 is expressed in all epidermal cells. However, its level fluctuates in each of these cells. If ATML1 levels surpass a threshold during the G2 phase of the cell cycle, the cell will likely enter a state of endoreduplication and become giant. Otherwise, the cell divides. Our results demonstrate a fluctuation-driven patterning mechanism for how cell fate decisions can be initiated through a random yet tightly regulated process.

Growth and developmental processes are occasionally accompanied by multiple rounds of DNA replication, known as endoreduplication. Coordination between endoreduplication and cell size regulation often plays a crucial role in proper organogenesis and cell differentiation. Here, we report that the level of correlation between ploidy and cell volume is different in the outer and inner cell layers of leaves of Arabidopsis thaliana using a novel imaging technique. Although there is a well-known, strong correlation between ploidy and cell volume in pavement cells of the epidermis, this correlation was extremely weak in palisade mesophyll cells. Induction of epidermis cell identity based on the expression of the homeobox gene ATML1 in mesophyll cells enhanced the level of correlation between ploidy and cell volume to near that of wild-type epidermal cells. We therefore propose that the correlation between ploidy and cell volume is regulated by cell identity., (© 2016. Published by The Company of Biologists Ltd.)

The epidermis of shoot organs in plants develops from the outermost layer (L1) of the shoot apical meristem. In Arabidopsis, a pair of homeobox genes, ARABIDOPSIS THALIANA MERISTEM LAYER1 (ATML1) and PROTODERMAL FACTOR2 (PDF2), play a role in regulating the expression of L1-specific genes. atml1-1 pdf2-1 double mutants show striking defects in the differentiation of shoot epidermal cells. However, because atml1-1 and pdf2-1 have a T-DNA inserted downstream of the respective homeobox sequences, these alleles may not represent null mutations. Here we characterized additional mutant alleles that have a T-DNA insertion at different positions of each gene. Double mutants of a strong atml1-3 allele with each pdf2 allele were found to cause embryonic arrest at the globular stage. Although with low frequency, all double mutant combinations of a weak atml1-1 allele with each pdf2 allele germinated and showed phenotypes defective in shoot epidermal cell differentiation. We further confirmed that transgenic induction of PDF2 fused to the Drosophila Engrailed repressor domain temporarily interferes with epidermal cell differentiation in the wild-type background. These results indicate that ATML1 and PDF2 act redundantly as a positive regulator of shoot epidermal cell differentiation and at least one copy of these genes is essential for embryo development., (© The Author 2015. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oup.com.)

Land plants have evolved a cuticle-bearing epidermis to protect themselves from environmental stress and pathogen attack. Despite its important role, little is known about the molecular mechanisms regulating shoot epidermal cell identity. In a recent study, we found that the Arabidopsis thaliana ATML1 gene is possibly a master regulator of shoot epidermal cell fate. We revealed that ATML1 has the ability to confer shoot epidermis-related traits to non-epidermal cells of the seedlings. These data are consistent with the previous loss-of-function mutant analyses, which implied a positive role of ATML1 in epidermal cell differentiation. Importantly, ectopic epidermal cells induced in ATML1-overexpressing lines provide a novel tool to assess the intrinsic properties of epidermal cells and to study epistatic interactions among genes involved in epidermal/mesophyll differentiation. Using this system, we obtained data revealing that ATML1 negatively influenced mesophyll cell fate. In addition, we provided a working model of how division planes in epidermal cells are determined.