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1.
J Exp Bot ; 71(12): 3664-3677, 2020 06 22.
Article in English | MEDLINE | ID: mdl-32133499

ABSTRACT

The F-bZIP transcription factors bZIP19 and bZIP23 are the central regulators of the zinc deficiency response in Arabidopsis, and phylogenetic analysis of F-bZIP homologs across land plants indicates that the regulatory mechanism of the zinc deficiency response may be conserved. Here, we identified the rice F-bZIP homologs and investigated their function. OsbZIP48 and OsbZIP50, but not OsbZIP49, complement the zinc deficiency-hypersensitive Arabidopsis bzip19bzip23 double mutant. Ectopic expression of OsbZIP50 in Arabidopsis significantly increases plant zinc accumulation under control zinc supply, suggesting an altered Zn sensing in OsbZIP50. In addition, we performed a phylogenetic analysis of F-bZIP homologs from representative monocot species that supports the branching of plant F-bZIPs into Group 1 and Group 2. Our results suggest that regulation of the zinc deficiency response in rice is conserved, with OsbZIP48 being a functional homolog of AtbZIP19 and AtbZIP23. A better understanding of the mechanisms behind the Zn deficiency response in rice and other important crops will contribute to develop plant-based strategies to address the problems of Zn deficiency in soils, crops, and cereal-based human diets.


Subject(s)
Basic-Leucine Zipper Transcription Factors , Oryza , Basic-Leucine Zipper Transcription Factors/metabolism , Gene Expression Regulation, Plant , Oryza/genetics , Oryza/metabolism , Phylogeny , Plant Proteins/genetics , Plant Proteins/metabolism , Zinc/metabolism
2.
Curr Opin Plant Biol ; 53: 10-14, 2020 02.
Article in English | MEDLINE | ID: mdl-31593816

ABSTRACT

The periderm acts as the first line of defence for a plant, protecting wood and phloem from abiotic and biotic stresses. During secondary growth, through the increase in girth of plant organs, the periderm replaces the epidermis as the outermost tissue. The phellogen, a bifacial post-embryonic meristem, forms the phelloderm inwards (toward the vasculature) and the suberized phellem outwards (toward the environment). These three tissues are collectively referred to as the periderm. Here, we summarize recent findings on the molecular mechanisms of periderm development by describing periderm formation in connection to the fate of the surrounding tissues, by discussing common regulatory hubs between the vascular cambium and the phellogen, and by highlighting transcription factors (TFs) controlling phellem differentiation.


Subject(s)
Gene Expression Regulation, Plant , Solanum tuberosum , Cambium , Meristem , Transcription Factors
3.
Development ; 146(6)2019 03 15.
Article in English | MEDLINE | ID: mdl-30858228

ABSTRACT

Pattern formation is typically controlled through the interaction between molecular signals within a given tissue. During early embryonic development, roots of the model plant Arabidopsis thaliana have a radially symmetric pattern, but a heterogeneous input of the hormone auxin from the two cotyledons forces the vascular cylinder to develop a diarch pattern with two xylem poles. Molecular analyses and mathematical approaches have uncovered the regulatory circuit that propagates this initial auxin signal into a stable cellular pattern. The diarch pattern seen in Arabidopsis is relatively uncommon among flowering plants, with most species having between three and eight xylem poles. Here, we have used multiscale mathematical modelling to demonstrate that this regulatory module does not require a heterogeneous auxin input to specify the vascular pattern. Instead, the pattern can emerge dynamically, with its final form dependent upon spatial constraints and growth. The predictions of our simulations compare to experimental observations of xylem pole number across a range of species, as well as in transgenic systems in Arabidopsis in which we manipulate the size of the vascular cylinder. By considering the spatial constraints, our model is able to explain much of the diversity seen in different flowering plant species.


Subject(s)
Arabidopsis/growth & development , Gene Expression Regulation, Plant , Plant Roots/anatomy & histology , Arabidopsis/genetics , Arabidopsis Proteins/physiology , Flowers/genetics , Indoleacetic Acids , Models, Biological , Plant Growth Regulators/physiology , Signal Transduction , Species Specificity , Stochastic Processes , Xylem/physiology
4.
New Phytol ; 222(4): 1816-1831, 2019 06.
Article in English | MEDLINE | ID: mdl-30724367

ABSTRACT

Tree bark is a highly specialized array of tissues that plays important roles in plant protection and development. Bark tissues develop from two lateral meristems; the phellogen (cork cambium) produces the outermost stem-environment barrier called the periderm, while the vascular cambium contributes with phloem tissues. Although bark is diverse in terms of tissues, functions and species, it remains understudied at higher resolution. We dissected the stem of silver birch (Betula pendula) into eight major tissue types, and characterized these by a combined transcriptomics and metabolomics approach. We further analyzed the varying bark types within the Betulaceae family. The two meristems had a distinct contribution to the stem transcriptomic landscape. Furthermore, inter- and intraspecies analyses illustrated the unique molecular profile of the phellem. We identified multiple tissue-specific metabolic pathways, such as the mevalonate/betulin biosynthesis pathway, that displayed differential evolution within the Betulaceae. A detailed analysis of suberin and betulin biosynthesis pathways identified a set of underlying regulators and highlighted the important role of local, small-scale gene duplication events in the evolution of metabolic pathways. This work reveals the transcriptome and metabolic diversity among bark tissues and provides insights to its development and evolution, as well as its biotechnological applications.


Subject(s)
Betula/genetics , Plant Bark/chemistry , Plant Bark/genetics , Plant Stems/genetics , Transcriptome/genetics , Betula/growth & development , Biosynthetic Pathways/genetics , Cambium/genetics , Evolution, Molecular , Gene Expression Regulation, Plant , Genome, Plant , Lipids/chemistry , Meristem/genetics , Organ Specificity , Species Specificity , Stem Cell Niche , Triterpenes/metabolism , Wood/genetics
5.
Front Plant Sci ; 9: 1955, 2018.
Article in English | MEDLINE | ID: mdl-30723487

ABSTRACT

All living organisms require zinc as an essential micronutrient. Maintaining appropriate intracellular zinc supply, and avoiding deficiency or toxic excess, requires a tight regulation of zinc homeostasis. In Arabidopsis, bZIP19 and bZIP23 (basic-leucine zipper) transcription factors are the central regulators of the zinc deficiency response. Their targets include members of the ZIP (Zrt/Irt-like Protein) transporter family, involved in cellular zinc uptake, which are up-regulated at zinc deficiency. However, the mechanisms by which these transcription factors are regulated by cellular zinc status are not yet known. Here, to further our insight, we took advantage of the zinc deficiency hypersensitive phenotype of the bzip19 bzip23 double mutant, and used it as background to produce complementation lines of each Arabidopsis F-bZIP transcription factor, including bZIP24. On these lines, we performed complementation and localization studies, analyzed the transcript level of a subset of putative target genes, and performed elemental tissue profiling. We find evidence supporting that the zinc-dependent activity of bZIP19 and bZIP23 is modulated by zinc at protein level, in the nucleus, where cellular zinc sufficiency represses their activity and zinc deficiency is required. In addition, we show that these two transcription factors are functionally redundant to a large extent, and that differential tissue-specific expression patterns might, at least partly, explain distinct regulatory activities. Finally, we show that bZIP24 does not play a central role in the Zn deficiency response. Overall, we provide novel information that advances our understanding of the regulatory activity of bZIP19 and bZIP23.

6.
New Phytol ; 215(1): 157-172, 2017 07.
Article in English | MEDLINE | ID: mdl-28503769

ABSTRACT

N6-adenosine methylation (m6 A) of mRNA is an essential process in most eukaryotes, but its role and the status of factors accompanying this modification are still poorly understood. Using combined methods of genetics, proteomics and RNA biochemistry, we identified a core set of mRNA m6 A writer proteins in Arabidopsis thaliana. The components required for m6 A in Arabidopsis included MTA, MTB, FIP37, VIRILIZER and the E3 ubiquitin ligase HAKAI. Downregulation of these proteins led to reduced relative m6 A levels and shared pleiotropic phenotypes, which included aberrant vascular formation in the root, indicating that correct m6 A methylation plays a role in developmental decisions during pattern formation. The conservation of these proteins amongst eukaryotes and the demonstration of a role in writing m6 A for the E3 ubiquitin ligase HAKAI is likely to be of considerable relevance beyond the plant sciences.


Subject(s)
Arabidopsis Proteins/physiology , Arabidopsis/metabolism , Methyltransferases/physiology , RNA, Messenger/metabolism , Ubiquitin-Protein Ligases/physiology , Adenosine/metabolism , Arabidopsis Proteins/genetics , Arabidopsis Proteins/metabolism , Conserved Sequence , Methylation , Methyltransferases/genetics , Methyltransferases/metabolism , Plants, Genetically Modified/metabolism , Sequence Alignment , Ubiquitin-Protein Ligases/genetics , Ubiquitin-Protein Ligases/metabolism
7.
Nat Commun ; 5: 4276, 2014 Jul 10.
Article in English | MEDLINE | ID: mdl-25008948

ABSTRACT

Phloem, a plant tissue responsible for long-distance molecular transport, harbours specific junctions, sieve areas, between the conducting cells. To date, little is known about the molecular framework related to the biogenesis of these sieve areas. Here we identify mutations at the CHER1/AtCTL1 locus of Arabidopsis thaliana. The mutations cause several phenotypic abnormalities, including reduced pore density and altered pore structure in the sieve areas associated with impaired phloem function. CHER1 encodes a member of a poorly characterized choline transporter-like protein family in plants and animals. We show that CHER1 facilitates choline transport, localizes to the trans-Golgi network, and during cytokinesis is associated with the phragmoplast. Consistent with its function in the elaboration of the sieve areas, CHER1 has a sustained, polar localization in the forming sieve plates. Our results indicate that the regulation of choline levels is crucial for phloem development and conductivity in plants.


Subject(s)
Arabidopsis Proteins/physiology , Arabidopsis/growth & development , Cell Communication/physiology , Glycoside Hydrolases/physiology , Phloem/growth & development , Plant Development/physiology , Arabidopsis/genetics , Arabidopsis/physiology , Arabidopsis Proteins/genetics , Cell Communication/genetics , Cell Polarity/genetics , Cell Polarity/physiology , Cytokinesis/genetics , Cytokinesis/physiology , Glycoside Hydrolases/genetics , Membrane Transport Proteins/genetics , Membrane Transport Proteins/physiology , Mutation/genetics , Phloem/genetics , Phloem/physiology , Plant Development/genetics
8.
Plant Signal Behav ; 8(8)2013 Aug.
Article in English | MEDLINE | ID: mdl-23759550

ABSTRACT

Expression patterns of orthologous genes can be similar between distantly related species, suggesting that developmental programs can be conserved between organisms. Here, we show that the promoter of AHP6, a gene which is involved in Arabidopsis lateral root development, also drives the expression of the reporter GUS gene in lateral roots of Medicago truncatula suggesting that similar regulatory elements are involved in lateral root organogenesis in these species. Interestingly, the AHP6 promoter was able to drive GUS expression in root nodules and nodule primordia, structures that are absent in Arabidopsis. We found two AHP6 orthologous genes in the M. truncatula genome and we speculate that these putative cytokinin inhibitors may play a role during lateral root and nodule development in this species.


Subject(s)
Arabidopsis Proteins/genetics , Arabidopsis/genetics , Gene Expression Regulation, Plant , Genes, Plant/genetics , Medicago truncatula/genetics , Root Nodules, Plant/genetics , Amino Acid Sequence , Arabidopsis Proteins/chemistry , Arabidopsis Proteins/metabolism , Glucuronidase/metabolism , Medicago truncatula/growth & development , Molecular Sequence Data , Plants, Genetically Modified , Root Nodules, Plant/growth & development
9.
PLoS One ; 8(2): e56370, 2013.
Article in English | MEDLINE | ID: mdl-23457561

ABSTRACT

In Arabidopsis thaliana, lateral roots (LRs) initiate from anticlinal cell divisions of pericycle founder cells. The formation of LR primordia is regulated antagonistically by the phytohormones cytokinin and auxin. It has previously been shown that cytokinin has an inhibitory effect on the patterning events occurring during LR formation. However, the molecular players involved in cytokinin repression are still unknown. In a similar manner to protoxylem formation in Arabidopsis roots, in which AHP6 (ARABIDOPSIS HISTIDINE PHOSPHOTRANSFER PROTEIN 6) acts as a cytokinin inhibitor, we reveal that AHP6 also functions as a cytokinin repressor during early stages of LR development. We show that AHP6 is expressed at different developmental stages during LR formation and is required for the correct orientation of cell divisions at the onset of LR development. Moreover, we demonstrate that AHP6 influences the localization of the auxin efflux carrier PIN1, which is necessary for patterning the LR primordia. In summary, we show that the inhibition of cytokinin signaling through AHP6 is required to establish the correct pattern during LR initiation.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/cytology , Arabidopsis/growth & development , Cell Division , Cytokinins/metabolism , Plant Roots/growth & development , Signal Transduction , Arabidopsis/metabolism , Gene Expression Regulation, Plant , Indoleacetic Acids/metabolism , Membrane Transport Proteins/metabolism , Protein Transport
10.
Dev Cell ; 21(6): 1144-55, 2011 Dec 13.
Article in English | MEDLINE | ID: mdl-22172675

ABSTRACT

Plant cells are connected through plasmodesmata (PD), membrane-lined channels that allow symplastic movement of molecules between cells. However, little is known about the role of PD-mediated signaling during plant morphogenesis. Here, we describe an Arabidopsis gene, CALS3/GSL12. Gain-of-function mutations in CALS3 result in increased accumulation of callose (ß-1,3-glucan) at the PD, a decrease in PD aperture, defects in root development, and reduced intercellular trafficking. Enhancement of CALS3 expression during phloem development suppressed loss-of-function mutations in the phloem abundant callose synthase, CALS7 indicating that CALS3 is a bona fide callose synthase. CALS3 alleles allowed us to spatially and temporally control the PD aperture between plant tissues. Using this tool, we are able to show that movement of the transcription factor SHORT-ROOT and microRNA165 between the stele and the endodermis is PD dependent. Taken together, we conclude that regulated callose biosynthesis at PD is essential for cell signaling.


Subject(s)
Arabidopsis/growth & development , Arabidopsis/metabolism , Glucans/biosynthesis , Arabidopsis/genetics , Arabidopsis Proteins/genetics , Arabidopsis Proteins/metabolism , Gene Expression Regulation, Developmental , Gene Expression Regulation, Enzymologic , Gene Expression Regulation, Plant , Genes, Plant , Glucosyltransferases/genetics , Glucosyltransferases/metabolism , MicroRNAs/genetics , MicroRNAs/metabolism , Molecular Sequence Data , Multigene Family , Mutation , Plant Roots/growth & development , Plant Roots/metabolism , Plants, Genetically Modified , RNA, Plant/genetics , RNA, Plant/metabolism , Signal Transduction , Transcription Factors/metabolism
11.
Nature ; 465(7296): 316-21, 2010 May 20.
Article in English | MEDLINE | ID: mdl-20410882

ABSTRACT

A key question in developmental biology is how cells exchange positional information for proper patterning during organ development. In plant roots the radial tissue organization is highly conserved with a central vascular cylinder in which two water conducting cell types, protoxylem and metaxylem, are patterned centripetally. We show that this patterning occurs through crosstalk between the vascular cylinder and the surrounding endodermis mediated by cell-to-cell movement of a transcription factor in one direction and microRNAs in the other. SHORT ROOT, produced in the vascular cylinder, moves into the endodermis to activate SCARECROW. Together these transcription factors activate MIR165a and MIR166b. Endodermally produced microRNA165/6 then acts to degrade its target mRNAs encoding class III homeodomain-leucine zipper transcription factors in the endodermis and stele periphery. The resulting differential distribution of target mRNA in the vascular cylinder determines xylem cell types in a dosage-dependent manner.


Subject(s)
Arabidopsis/metabolism , Cell Lineage , Gene Dosage , MicroRNAs/metabolism , Plant Roots/cytology , RNA, Plant/metabolism , Signal Transduction , Arabidopsis/cytology , Arabidopsis/genetics , Arabidopsis/growth & development , Arabidopsis Proteins/metabolism , Body Patterning , Cell Movement , Endoderm/cytology , Endoderm/metabolism , Gene Expression Regulation, Plant , MicroRNAs/genetics , Organogenesis , Plant Roots/genetics , Plant Roots/growth & development , Plant Roots/metabolism , RNA Transport , RNA, Plant/genetics , Transcription Factors/metabolism , Xylem/cytology , Xylem/growth & development , Xylem/metabolism
12.
Plant Cell ; 22(3): 640-54, 2010 Mar.
Article in English | MEDLINE | ID: mdl-20197506

ABSTRACT

The root cap has a central role in root growth, determining the growth trajectory and facilitating penetration into the soil. Root cap cells have specialized functions and morphologies, and border cells are released into the rhizosphere by specific cell wall modifications. Here, we demonstrate that the cellular maturation of root cap is redundantly regulated by three genes, SOMBRERO (SMB), BEARSKIN1 (BRN1), and BRN2, which are members of the Class IIB NAC transcription factor family, together with the VASCULAR NAC DOMAIN (VND) and NAC SECONDARY WALL THICKENING PROMOTING FACTOR (NST) genes that regulate secondary cell wall synthesis in specialized cell types. Lateral cap cells in smb-3 mutants continue to divide and fail to detach from the root, phenotypes that are independent of FEZ upregulation in smb-3. In brn1-1 brn2-1 double mutants, columella cells fail to detach, while in triple mutants, cells fail to mature in all parts of the cap. This complex genetic redundancy involves differences in expression, protein activity, and target specificity. All three genes have very similar overexpression phenotypes to the VND/NST genes, indicating that members of this family are largely functionally equivalent. Our results suggest that Class IIB NAC proteins regulate cell maturation in cells that undergo terminal differentiation with strong cell wall modifications.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/genetics , Plant Root Cap/growth & development , Transcription Factors/metabolism , Amino Acid Sequence , Arabidopsis/growth & development , Arabidopsis/metabolism , Arabidopsis Proteins/genetics , Gene Expression Regulation, Developmental , Gene Expression Regulation, Plant , Molecular Sequence Data , Phylogeny , Plant Root Cap/genetics , Plant Root Cap/metabolism , Plants, Genetically Modified/genetics , Plants, Genetically Modified/growth & development , Plants, Genetically Modified/metabolism , Sequence Alignment , Transcription Factors/genetics
13.
Comput Biol Med ; 39(9): 785-93, 2009 Sep.
Article in English | MEDLINE | ID: mdl-19604506

ABSTRACT

To obtain development information of individual plant cells, it is necessary to perform in vivo imaging of the specimen under study, through time-lapse confocal microscopy. Automation of cell detection/marking process is important to provide research tools in order to ease the search for special events, such as cell division. In this paper we discuss an automatic cell detection approach for Arabidopsis thaliana based on segmentation, which selects the best cell candidates from a starting watershed-based image segmentation and improves the result by merging adjacent regions. The selection of individual cells is obtained using a support vector machine (SVM) classifier, based on a cell descriptor constructed from the shape and edge strength of the cells' contour. In addition we proposed a novel cell merging criterion based on edge strength along the line that connects adjacent cells' centroids, which is a valuable tool in the reduction of cell over-segmentation. The result is largely pruned of badly segmented and over-segmented cells, thus facilitating the study of cells. When comparing the results after merging with the basic watershed segmentation, we obtain 1.5% better coverage (increase in F-measure) and up to 27% better precision in correct cell segmentation.


Subject(s)
Arabidopsis/cytology , Plant Roots/cytology , Arabidopsis/growth & development , Artificial Intelligence , Cell Shape , Cell Wall/ultrastructure , Computer Simulation , Image Processing, Computer-Assisted/statistics & numerical data , Models, Biological
14.
Dev Cell ; 15(6): 913-22, 2008 Dec.
Article in English | MEDLINE | ID: mdl-19081078

ABSTRACT

Because plant cells do not migrate, cell division planes are crucial determinants of plant cellular architecture. In Arabidopsis roots, stringent control of cell divisions leads to a virtually invariant division pattern, including those that create new tissue layers. However, the mechanisms that control oriented cell divisions are hitherto poorly understood. Here, we reveal one such mechanism in which FEZ and SOMBRERO (SMB), two plant-specific NAC-domain transcription factors, control the delicately tuned reorientation and timing of cell division in a subset of stem cells. FEZ is expressed in root cap stem cells, where it promotes periclinal, root cap-forming cell divisions. In contrast, SMB negatively regulates FEZ activity, repressing stem cell-like divisions in the root cap daughter cells. FEZ becomes expressed in predivision stem cells, induces oriented cell division, and activates expression of its negative regulator, SMB, thus generating a feedback loop for controlled switches in cell division plane.


Subject(s)
Arabidopsis Proteins/chemistry , Arabidopsis/genetics , Cell Division , Gene Expression Regulation, Plant , Plant Roots/metabolism , Transcription Factors/physiology , Amino Acid Sequence , Arabidopsis Proteins/metabolism , Arabidopsis Proteins/physiology , Cloning, Molecular , Enhancer Elements, Genetic , Gene Expression Profiling , Models, Biological , Molecular Sequence Data , Mutagenesis , Protein Structure, Tertiary , Sequence Homology, Amino Acid , Transcription Factors/metabolism
15.
Plant J ; 48(4): 619-27, 2006 Nov.
Article in English | MEDLINE | ID: mdl-17087761

ABSTRACT

In the Arabidopsis root, asymmetric stem-cell divisions produce daughters that form the different root cell types. Here we report the establishment of a confocal tracking system that allows the analysis of numbers and orientations of cell divisions in root stem cells. The system provides direct evidence that stem cells have lower division rates than cells in the proximal meristem. It also allows tracking of cell division timing, which we have used to analyse the synchronization of root cap divisions. Finally, it gives new insights into lateral root cap formation: epidermal stem-cell daughters can rotate the orientation of the division plane like the stem cell.


Subject(s)
Arabidopsis/cytology , Meristem/cytology , Plant Roots/cytology , Stem Cells/cytology , Cell Division , Photoperiod , Time Factors
16.
Cell ; 123(7): 1337-49, 2005 Dec 29.
Article in English | MEDLINE | ID: mdl-16377572

ABSTRACT

The maintenance of stem cells in defined locations is crucial for all multicellular organisms. Although intrinsic factors and signals for stem cell fate have been identified in several species, it has remained unclear how these connect to the ability to reenter the cell cycle that is one of the defining properties of stem cells. We show that local reduction of expression of the RETINOBLASTOMA-RELATED (RBR) gene in Arabidopsis roots increases the amount of stem cells without affecting cell cycle duration in mitotically active cells. Conversely, induced RBR overexpression dissipates stem cells prior to arresting other mitotic cells. Overexpression of D cyclins, KIP-related proteins, and E2F factors also affects root stem cell pool size, and genetic interactions suggest that these factors function in a canonical RBR pathway to regulate somatic stem cells. Expression analysis and genetic interactions position RBR-mediated regulation of the stem cell state downstream of the patterning gene SCARECROW.


Subject(s)
Arabidopsis Proteins/physiology , Arabidopsis/cytology , Plant Roots/cytology , Plant Roots/growth & development , Stem Cells/metabolism , Arabidopsis/growth & development , Arabidopsis Proteins/genetics , Cell Differentiation/genetics , Cell Differentiation/physiology , Down-Regulation , Plant Roots/metabolism , Retinoblastoma Protein/genetics , Signal Transduction/physiology , Stem Cells/cytology
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