Irreversible fate commitment in the Arabidopsis stomatal lineage requires a FAMA and RETINOBLASTOMA-RELATED module

Matos, Juliana L.; Lau, On Sun; Hachez, Charles; Cruz‐Ramírez, Alfredo; Scheres, Ben; Bergmann, Dominique C.

doi:10.7554/elife.03271

Cited by 97 publications

(131 citation statements)

References 46 publications

(89 reference statements)

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“…Cells representing specific developmental stages isolated by FACS after a short protoplasting step included: stomatal entry (stage 1, SPCHp::SPCH-YFP , SSY ), commitment (stage 2, MUTEp::nucGFP , MG ), and differentiation (stage 3, FAMAp::GFP-FAMA , FGF ) stages, as well as mature stomata (stage 4, enhancer trap E1728::GFP , E1728G ) and a marker of the entire aerial epidermis ( ML1p::YFP-RCI2A , ML1Y ). The cell-type specific expression patterns of the five marker lines used have been extensively characterized previously (Davies and Bergmann, 2014; Gardner et al, 2008; MacAlister et al, 2007; Matos et al, 2014; Ohashi-Ito and Bergmann, 2006; Pillitteri et al, 2007; Robinson et al, 2011; Roeder et al, 2010). SPCHp::SPCH-YFP is expressed most brightly just prior to and after asymmetric divisions of MMCs, thus marking a potentially mixed population of precursors; a timecourse of this expression is provided in Figure S1D and E.…”

Section: Resultsmentioning

confidence: 99%

Transcriptome Dynamics of the Stomatal Lineage: Birth, Amplification, and Termination of a Self-Renewing Population

et al. 2015

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Summary Developmental transitions can be described in terms of morphology and the roles of individual genes, but also in terms of global transcriptional and epigenetic changes. Temporal dissections of transcriptome changes, however, are rare for intact, developing tissues. We used RNA sequencing and microarray platforms to quantify gene expression from labeled cells isolated by Fluorescence Activated Cell Sorting to generate cell-type specific transcriptomes during development of an adult stem-cell lineage in the Arabidopsis leaf. We show regulatory modules in this early lineage link cell types that had previously been considered to be under separate control and provide evidence for recruitment of individual members of gene families for different developmental decisions. Because stomata are physiologically important and because stomatal lineage cells exhibit exemplary division, cell fate and cell signaling behaviors, this dataset serves as a valuable resource for further investigations of fundamental developmental processes.

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Section: Resultsmentioning

confidence: 99%

Transcriptome Dynamics of the Stomatal Lineage: Birth, Amplification, and Termination of a Self-Renewing Population

et al. 2015

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“…FAMA was recently shown to recruit RBR through its LxCxE interaction motif (23). Because a version of SPCH missing its potential RBR-binding sites behaved indistinguishably from WT SPCH, FAMA is likely unique in its physical interaction with RBR.…”

Section: Discussionmentioning

confidence: 99%

Functional specialization of stomatal bHLHs through modification of DNA-binding and phosphoregulation potential

Davies¹,

Bergmann

2014

Proc. Natl. Acad. Sci. U.S.A.

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Transcription factor duplication events and subsequent specialization can drive evolution by facilitating biological innovation and developmental complexity. Identification of sequences that confer distinct biochemical function in vivo is an important step in understanding how related factors could refine specific developmental processes over time. Functional analysis of the basic helix-loop-helix (bHLH) protein SPEECHLESS, one of three closely related transcription factors required for stomatal lineage progression in Arabidopsis thaliana, allowed a dissection of motifs associated with specific developmental outputs. Phosphorylated residues, shown previously to quantitatively affect activity, also allow a qualitative shift in function between division and cell fate-promoting activities. Our data also provide surprising evidence that, despite deep sequence conservation in DNAbinding domains, the functional requirement for these domains has diverged, with the three stomatal bHLHs exhibiting absolute, partial, or no requirements for DNA-binding residues for their in vivo activities. Using these data, we build a plausible model describing how the current unique and overlapping roles of these proteins might have evolved from a single ancestral protein.stomata | bHLH transcription factors | Arabidopsis | evolution | SPEECHLESS T ranscription factors regulate various processes integral to multicellular development, from framing the overall body plan to specifying the fates of individual cells. Paralogs within transcription factor families can exhibit distinct but related functions, and these unique functions can arise through alterations in expression patterns (via mutations in cis-regulatory elements) or through alterations of biochemical function via mutations in the gene's coding sequence. The Drosophila homeobox gene paired, for example, is able to rescue the gooseberry larval cuticle phenotype when expressed under the gooseberry promoter, indicating divergent embryonic roles owing to cis-regulatory elements (1), but a later role of paired in male fertility cannot be rescued by ectopic expression of gooseberry, indicating that biochemical differences also exist between these two transcription factors (2). Investigating specific sequence alterations that functionally distinguish genes from one another is critical to understanding the evolution and diversification of biological processes.Stomatal development is a useful system for addressing how closely related transcription factors fulfill distinct functions. Stomata, pores in the plant epidermis that regulate gas exchange, develop via a series of divisions and cell fate transitions. Although stomatal development shows variation throughout the plant kingdom in terms of structure, precursors, and patterning (3), related basic-helix-loop-helix (bHLH) transcription factors are likely central to specifying cell fates in all stomata-producing plants (4, 5), and the evolutionary diversification of these bHLH proteins may be responsible for stomatal development variation (...

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“…CYCLIND/CDKA;1 complexes phosphorylate RETINOBLASTOMA RELATED1 (RBR1), releasing E2F transcription factors to activate cell cycle gene transcription (Desvoyes et al, 2006, 2014). RBR1 can bind to and regulate the activity of other transcription factors including the key developmental regulators FAMA and SCARECROW (Cruz-Ramírez et al, 2012; Matos et al, 2014). In addition, CDKs can phosphorylate transcription factors to regulate their activity (Reindl et al, 1997; Yang et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Transcriptomic Effects of the Cell Cycle Regulator LGO in Arabidopsis Sepals

Schwarz

Roeder

2016

Front. Plant Sci.

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Endoreduplication is a specialized cell cycle in which DNA replication occurs, but mitosis is skipped creating enlarged polyploid cells. Endoreduplication is associated with the differentiation of many specialized cell types. In the Arabidopsis thaliana sepal epidermis endoreduplicated giant cells form interspersed between smaller cells. Both the transcription factor Arabidopsis thaliana MERISTEM LAYER1 (ATML1) and the plant-specific cyclin dependent kinase inhibitor LOSS OF GIANT CELLS FROM ORGANS (LGO)/SIAMESE RELATED1 (SMR1) are required for the formation of giant cells. Overexpression of LGO is sufficient to produce sepals covered in highly endoreduplicated giant cells. Here we ask whether overexpression of LGO changes the transcriptome of these mature sepals. We show that overexpression of LGO in the epidermis (LGOoe) drives giant cell formation even in atml1 mutant sepals. Using RNA-seq we show that LGOoe has significant effects on the mature sepal transcriptome that are primarily ATML1-independent changes of gene activity. Genes activated by LGOoe, directly or indirectly, predominantly encode proteins involved in defense responses, including responses to wounding, insects (a predator of Arabidopsis), and fungus. They also encode components of the glucosinolate biosynthesis pathway, a key biochemical pathway in defense against herbivores. LGOoe-activated genes include previously known marker genes of systemic acquired resistance such as PR1 through PR5. The defensive functions promoted by LGOoe in sepals overlap with functions recently shown to be transcriptionally activated by hyperimmune cpr5 mutants in a LGO-dependent manner. Our findings show that the cell cycle regulator LGO can directly or indirectly drive specific states of gene expression; in particular, they are consistent with recent findings showing LGO to be necessary for transcriptional activation of many defense genes in Arabidopsis.

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Irreversible fate commitment in the Arabidopsis stomatal lineage requires a FAMA and RETINOBLASTOMA-RELATED module

Cited by 97 publications

References 46 publications

Transcriptome Dynamics of the Stomatal Lineage: Birth, Amplification, and Termination of a Self-Renewing Population

Transcriptome Dynamics of the Stomatal Lineage: Birth, Amplification, and Termination of a Self-Renewing Population

Functional specialization of stomatal bHLHs through modification of DNA-binding and phosphoregulation potential

Transcriptomic Effects of the Cell Cycle Regulator LGO in Arabidopsis Sepals

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