An Ancient Mechanism Controls the Development of Cells with a Rooting Function in Land Plants

Menand, Benoît; Yi, Keke; Jouannic, Stéfan; Hoffmann, Laurent; Ryan, Eoin G.; Linstead, Paul; Schaefer, Didier G.; Dolan, Liam

doi:10.1126/science.1142618

Cited by 394 publications

(435 citation statements)

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“…Mechanisms that control multicellular development in land plants, therefore, either evolved from genes directing unicellular development in the sporophyte or were recruited from existing genetic toolkits that controlled multicellular morphology in the gametophyte. Evidence exists for the recruitment of gametophyte genes into the sporophyte (Menand et al, 2007); however, genetic analyses in green algae and basal land plants suggest that ancestral KNOX genes controlled diploid development and diversified in land plants to control multicellular body plans.…”

Section: Evolving Knox Functions: Knox Genes and The Rise Of The Spormentioning

confidence: 99%

KNOX genes: versatile regulators of plant development and diversity

2010

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SummaryKnotted1-like homeobox (KNOX) proteins are homeodomain transcription factors that maintain an important pluripotent cell population called the shoot apical meristem, which generates the entire above-ground body of vascular plants. KNOX proteins regulate target genes that control hormone homeostasis in the meristem and interact with another subclass of homeodomain proteins called the BELL family. Studies in novel genetic systems, both at the base of the land plant phylogeny and in flowering plants, have uncovered novel roles for KNOX proteins in sculpting plant form and its diversity. Here, we discuss how KNOX proteins influence plant growth and development in a versatile context-dependent manner.

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Section: Evolving Knox Functions: Knox Genes and The Rise Of The Spormentioning

confidence: 99%

KNOX genes: versatile regulators of plant development and diversity

2010

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“…Stem cells are initiated at an early stage of development and maintained during the growth period, providing cells that give rise to most parts of the plant body. In addition, stem cells are repeatedly formed from differentiated cells during development and growth, such as the formation of rhizoids (Sakakibara et al, 2003;Menand et al, 2007b) and side branches (Harrison et al, 2009) in bryophytes. Furthermore, under the appropriate inductive conditions, differentiated cells can be reprogrammed to form stem cells.…”

Section: Introductionmentioning

confidence: 99%

PhyscomitrellaCyclin-Dependent Kinase A Links Cell Cycle Reactivation to Other Cellular Changes during Reprogramming of Leaf Cells

et al. 2011

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During regeneration, differentiated plant cells can be reprogrammed to produce stem cells, a process that requires coordination of cell cycle reactivation with acquisition of other cellular characteristics. However, the factors that coordinate the two functions during reprogramming have not been determined. Here, we report a link between cell cycle reactivation and the acquisition of new cell-type characteristics through the activity of cyclin-dependent kinase A (CDKA) during reprogramming in the moss Physcomitrella patens. Excised gametophore leaf cells of P. patens are readily reprogrammed, initiate tip growth, and form chloronema apical cells with stem cell characteristics at their first cell division. We found that leaf cells facing the cut undergo CDK activation along with induction of a D-type cyclin, tip growth, and transcriptional activation of protonema-specific genes. A DNA synthesis inhibitor, aphidicolin, inhibited cell cycle progression but prevented neither tip growth nor protonemal gene expression, indicating that cell cycle progression is not required for acquisition of protonema cell-type characteristics. By contrast, treatment with a CDK inhibitor or induction of dominant-negative CDKA;1 protein inhibited not only cell cycle progression but also tip growth and protonemal gene expression. These findings indicate that cell cycle progression is coordinated with other cellular changes by the concomitant regulation through CDKA;1.

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“…Auxin signaling (17,18), ethylene perception (19), abscisic acid signaling (20), and several small RNAs are conserved between mosses and flowering plants (21,22), suggesting that many switches and plug-ins of land plant GRNs have been conserved since before the evolution of vascular plants over 440 million y ago. However, the architecture and evolutionary history of these hypothetical ancient GRN kernels are mostly unknown.In the angiosperm Arabidopsis thaliana, root hair development is controlled by the basic helix-loop-helix (bHLH) transcription factors AtRHD6 (A. thaliana ROOT HAIR DEFECTIVE 6) and AtRSL1 (A. thaliana RHD SIX-LIKE 1); their homologs in the moss Physcomitrella patens (Pp), PpRSL1 and PpRSL2, control the development of filamentous rooting structures: caulonema and rhizoids (23)(24)(25). This finding suggests that RSL genes belong to an ancient land plant GRN that controls the differentiation of cells with a rooting function.…”

mentioning

confidence: 99%

“…In the angiosperm Arabidopsis thaliana, root hair development is controlled by the basic helix-loop-helix (bHLH) transcription factors AtRHD6 (A. thaliana ROOT HAIR DEFECTIVE 6) and AtRSL1 (A. thaliana RHD SIX-LIKE 1); their homologs in the moss Physcomitrella patens (Pp), PpRSL1 and PpRSL2, control the development of filamentous rooting structures: caulonema and rhizoids (23)(24)(25). This finding suggests that RSL genes belong to an ancient land plant GRN that controls the differentiation of cells with a rooting function.…”

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confidence: 99%

Recruitment and remodeling of an ancient gene regulatory network during land plant evolution

Pires

Breuninger

et al. 2013

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

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The evolution of multicellular organisms was made possible by the evolution of underlying gene regulatory networks. In animals, the core of gene regulatory networks consists of kernels, stable subnetworks of transcription factors that are highly conserved in distantly related species. However, in plants it is not clear when and how kernels evolved. We show here that RSL (ROOT HAIR DEFECTIVE SIX-LIKE) transcription factors form an ancient land plant kernel controlling caulonema differentiation in the moss Physcomitrella patens and root hair development in the flowering plant Arabidopsis thaliana. Phylogenetic analyses suggest that RSL proteins evolved in aquatic charophyte algae or in early land plants, and have been conserved throughout land plant radiation. Genetic and transcriptional analyses in loss of function A. thaliana and P. patens mutants suggest that the transcriptional interactions in the RSL kernel were remodeled and became more hierarchical during the evolution of vascular plants. We predict that other gene regulatory networks that control development in derived groups of plants may have originated in the earliest land plants or in their ancestors, the Charophycean algae.T he development of multicellular organisms is controlled by gene regulatory networks (GRNs) and the reorganization of GRN architecture is thought to be a major factor underlying morphological evolution (1-5). GRNs are hierarchic and modular structures where four major component classes can be identified (3): at the periphery of GRNs are differentiation gene batteries encoding proteins that execute cell type-specific functions (such as building a pigmented cell); upstream of these batteries are switches that allow or prevent subcircuits to function in specific developmental contexts, and "plug-ins," small subcircuits that are flexibly and repeatedly used during development (such as signal transduction pathways); at the core of GRNs are kernels, small conserved subcircuits that execute specific developmental functions (such as defining spatial patterns in an embryo). Kernels are comprised of transcription factors that are highly conserved in distantly related species and are unusually stable components of GRNs.Ancient kernels that regulate body plan and organ development are highly conserved among diverse groups of metazoans (animals) (6-10). In contrast, the core components of plant GRNs are difficult to identify because of the dynamic nature of plant genome evolution and the plastic character of plant development. Floral homeotic genes form a relatively recent kernel controlling flower development (11). Homologs of KNOX and LEAFY transcription factors control shoot development in vascular plants and sporophyte development in mosses (12-15). KNOX/BEL genes also control the development of the diploid phase in unicellular chlorophytes (16) and the haploid-to-diploid transition in mosses (15), suggesting that KNOX and LEAFY genes may be core members of ancient GRNs that control diploid development in plants. Auxin signaling (17,18), et...

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An Ancient Mechanism Controls the Development of Cells with a Rooting Function in Land Plants

Cited by 394 publications

References 18 publications

KNOX genes: versatile regulators of plant development and diversity

KNOX genes: versatile regulators of plant development and diversity

PhyscomitrellaCyclin-Dependent Kinase A Links Cell Cycle Reactivation to Other Cellular Changes during Reprogramming of Leaf Cells

Recruitment and remodeling of an ancient gene regulatory network during land plant evolution

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