A novel regulatory circuit specifies cell fate in the <i>Arabidopsis</i> root epidermis

Schiefelbein, John,Lee, Myeong Min Blackwell Publishing Ltd 2006 Physiologia plantarum Vol.126 No.4

<P>The specification of distinct cell fates in multicellular organisms is a fundamental process in developmental biology. The <I>Arabidopsis</I> root epidermis, which consists of root-hair cells and non-hair cells, provides a useful model system for studying cell fate specification. In this tissue, the cell fates are determined by their relative position to the underlying cortical cells, and many genes have been identified that regulate this position-dependent cell fate specification. Recent studies using genetic, molecular, and biochemical approaches have shed new light on this process and revealed a complex network of interacting and interdependent components. In particular, a novel regulatory circuit has recently been identified, which includes a lateral inhibition pathway and a feedback loop that enables intercellular communication and ensures that two distinct cell types arise in an appropriate pattern. This regulatory circuit is also influenced by a positional signaling pathway which includes the SCRAMBLED leucine-rich repeat receptor kinase. The studies of cell fate specification in the <I>Arabidopsis</I> root epidermis provide new insights into the molecular strategies used to define distinct cell types in plants.</P>

Nuclear Trapping Controls the Position-Dependent Localization of CAPRICE in the Root Epidermis of Arabidopsis

Kang, Yeon Hee,Song, Sang-Kee,Schiefelbein, John,Lee, Myeong Min American Society of Plant Biologists 2013 PLANT PHYSIOLOGY - Vol.163 No.1

<P><I>Differential nuclear trapping of a transcription factor between root epidermal cells at distinct positions causes differential accumulation of the protein and affects cell fate decision</I>.</P>

Distinct Signaling Mechanisms in Multiple Developmental Pathways by the SCRAMBLED Receptor of Arabidopsis

Kwak, Su-Hwan,Woo, Sooah,Lee, Myeong Min,Schiefelbein, John American Society of Plant Biologists 2014 Plant Physiology Vol.166 No.2

<P><I>A single receptor-like kinase exhibits distinct signaling requirements to mediate different developmental events in Arabidopsis</I>.</P><P>SCRAMBLED (SCM), a leucine-rich repeat receptor-like kinase in Arabidopsis (<I>Arabidopsis thaliana</I>), is required for positional signaling in the root epidermis and for tissue/organ development in the shoot. To further understand SCM action, we generated a series of kinase domain variants and analyzed their ability to complement <I>scm</I> mutant defects. We found that the SCM kinase domain, but not kinase activity, is required for its role in root epidermal patterning, supporting the view that SCM is an atypical receptor kinase. We also describe a previously uncharacterized role for SCM in fruit dehiscence, because mature siliques from <I>scm</I> mutants fail to open properly. Interestingly, the kinase domain of SCM appears to be dispensable for this developmental process. Furthermore, we found that most of the SCM kinase domain mutations dramatically inhibit inflorescence development. Because this process is not affected in <I>scm</I> null mutants, it is likely that SCM acts redundantly to regulate inflorescence size. The importance of distinct kinase residues for these three developmental processes provides an explanation for the maintenance of the conserved kinase domain in the SCM protein, and it may generally explain its conservation in other atypical kinases. Furthermore, these results indicate that individual leucine-rich repeat receptor-like kinases may participate in multiple pathways using distinct signaling mechanisms to mediate diverse cellular communication events.</P>

The MYB23 gene provides a positive feedback loop for cell fate specification in the Arabidopsis root epidermis.

Kang, Yeon Hee,Kirik, Victor,Hulskamp, Martin,Nam, Kyoung Hee,Hagely, Katherine,Lee, Myeong Min,Schiefelbein, John American Society of Plant Physiologists 2009 The Plant cell Vol.21 No.4

<P>The specification of cell fates during development requires precise regulatory mechanisms to ensure robust cell type patterns. Theoretical models of pattern formation suggest that a combination of negative and positive feedback mechanisms are necessary for efficient specification of distinct fates in a field of differentiating cells. Here, we examine the role of the R2R3-MYB transcription factor gene, AtMYB23 (MYB23), in the establishment of the root epidermal cell type pattern in Arabidopsis thaliana. MYB23 is closely related to, and is positively regulated by, the WEREWOLF (WER) MYB gene during root epidermis development. Furthermore, MYB23 is able to substitute for the function of WER and to induce its own expression when controlled by WER regulatory sequences. We also show that the MYB23 protein binds to its own promoter, suggesting a MYB23 positive feedback loop. The localization of MYB23 transcripts and MYB23-green fluorescent protein (GFP) fusion protein, as well as the effect of a chimeric MYB23-SRDX repressor construct, links MYB23 function to the developing non-hair cell type. Using mutational analyses, we find that MYB23 is necessary for precise establishment of the root epidermal pattern, particularly under conditions that compromise the cell specification process. These results suggest that MYB23 participates in a positive feedback loop to reinforce cell fate decisions and ensure robust establishment of the cell type pattern in the Arabidopsis root epidermis.</P>

A Gene Regulatory Network for Root Epidermis Cell Differentiation in Arabidopsis

Bruex, Angela,Kainkaryam, Raghunandan M.,Wieckowski, Yana,Kang, Yeon Hee,Bernhardt, Christine,Xia, Yang,Zheng, Xiaohua,Wang, Jean Y.,Lee, Myeong Min,Benfey, Philip,Woolf, Peter J.,Schiefelbein, John Public Library of Science 2012 PLoS genetics Vol.8 No.1

<▼1><P>The root epidermis of Arabidopsis provides an exceptional model for studying the molecular basis of cell fate and differentiation. To obtain a systems-level view of root epidermal cell differentiation, we used a genome-wide transcriptome approach to define and organize a large set of genes into a transcriptional regulatory network. Using cell fate mutants that produce only one of the two epidermal cell types, together with fluorescence-activated cell-sorting to preferentially analyze the root epidermis transcriptome, we identified 1,582 genes differentially expressed in the root-hair or non-hair cell types, including a set of 208 “core” root epidermal genes. The organization of the core genes into a network was accomplished by using 17 distinct root epidermis mutants and 2 hormone treatments to perturb the system and assess the effects on each gene's transcript accumulation. In addition, temporal gene expression information from a developmental time series dataset and predicted gene associations derived from a Bayesian modeling approach were used to aid the positioning of genes within the network. Further, a detailed functional analysis of likely bHLH regulatory genes within the network, including <I>MYC1</I>, <I>bHLH54</I>, <I>bHLH66</I>, and <I>bHLH82</I>, showed that three distinct subfamilies of bHLH proteins participate in root epidermis development in a stage-specific manner. The integration of genetic, genomic, and computational analyses provides a new view of the composition, architecture, and logic of the root epidermal transcriptional network, and it demonstrates the utility of a comprehensive systems approach for dissecting a complex regulatory network.</P></▼1><▼2><P><B>Author Summary</B></P><P>A current challenge in the field of developmental biology is to define the composition and organization of gene networks that direct the pattern and differentiation of cells, tissues, and organs. In this study, we address this problem using Arabidopsis root epidermis development, a relatively simple model for studies of cell pattern formation and differentiation in plants. We used a tissue-specific cell sorting approach to define more than 1,500 genes whose transcripts differentially accumulate in the developing root epidermis. A series of transcriptome analyses were performed with 17 root epidermal mutants and 2 plant hormone treatments to dissect the regulatory relationships between 208 core genes. In addition, gene expression information from a developmental time series dataset was used to organize genes temporally. The results provide insight into the composition, organization, and logic of a developmental gene regulatory network. Furthermore, this work demonstrates the utility of an integrated analysis in gene regulatory network construction using genetic, genomic, and computational approaches.</P></▼2>