RESUMO
In plants, developmental plasticity allows for the modulation of organ growth in response to environmental cues. Being in contact with soil, roots are the first organ that responds to various types of soil abiotic stress such as high salt concentration. In the root, developmental plasticity relies on changes in the activity of the apical meristem, the region at the tip of the root where a set of self-renewing undifferentiated stem cells sustain growth. Here, we show that salt stress promotes differentiation of root meristem cells via reducing the dosage of the microRNAs miR165 and 166. By means of genetic, molecular and computational analysis, we show that the levels of miR165 and 166 respond to high salt concentration, and that miR165 and 166-dependent PHABULOSA (PHB) modulation is central to the response of root growth to this stress. Specifically, we show that salt-dependent reduction of miR165 and 166 causes a rapid increase in PHB expression and, hence, production of the root meristem pro-differentiation hormone cytokinin. Our data provide direct evidence for how the miRNA-dependent modulation of transcription factor dosage mediates plastic development in plants.
Assuntos
Proteínas de Arabidopsis , Arabidopsis , Arabidopsis/metabolismo , Meristema/metabolismo , Proteínas de Arabidopsis/genética , Proteínas de Arabidopsis/metabolismo , Fatores de Transcrição/metabolismo , Estresse Salino/genéticaRESUMO
During organogenesis, a key step toward the development of a functional organ is the separation of cells into specific domains with different activities. Mutual inhibition of gene expression has been shown to be sufficient to establish and maintain these domains during organogenesis in several multicellular organisms. Here, we show that the mutual inhibition between the PLETHORA transcription factors (PLTs) and the ARABIDOPSIS RESPONSE REGULATORs (ARRs) transcription factors is sufficient to separate cell division and cell differentiation during root organogenesis. In particular, we show that ARR1 suppresses PLT activities and that PLTs suppress ARR1 and ARR12 by targeting their proteins for degradation via the KISS ME DEADLY 2 F-box protein. These findings reveal new important aspects of the complex process of root zonation and development.
Assuntos
Proteínas de Arabidopsis , Arabidopsis , Raízes de Plantas , Fatores de Transcrição , Arabidopsis/metabolismo , Proteínas de Arabidopsis/genética , Proteínas de Arabidopsis/metabolismo , Regulação da Expressão Gênica de Plantas , Meristema/metabolismo , Raízes de Plantas/genética , Raízes de Plantas/metabolismo , Fatores de Transcrição/genética , Fatores de Transcrição/metabolismoRESUMO
In both animals and plants, development involves anatomical modifications. In the root of Arabidopsis thaliana, maturation of the ground tissue (GT)-a tissue comprising all cells between epidermal and vascular ones-is a paradigmatic example of these modifications, as it generates an additional tissue layer, the middle cortex (MC).1-4 In early post-embryonic phases, the Arabidopsis root GT is composed of one layer of endodermis and one of cortex. A second cortex layer, the MC, is generated by asymmetric cell divisions in about 80% of Arabidopsis primary roots, in a time window spanning from 7 to 14 days post-germination (dpg). The cell cycle regulator CYCLIN D6;1 (CYCD6;1) plays a central role in this process, as its accumulation in the endodermis triggers the formation of MC.5 The phytohormone gibberellin (GA) is a key regulator of the timing of MC formation, as alterations in its signaling and homeostasis result in precocious endodermal asymmetric cell divisions.3,6,7 However, little is known on how GAs are regulated during GT maturation. Here, we show that the HOMEODOMAIN LEUCINE ZIPPER III (HD-ZIPIII) transcription factor PHABULOSA (PHB) is a master regulator of MC formation, controlling the accumulation of CYCD6;1 in the endodermis in a cell non-autonomous manner. We show that PHB activates the GA catabolic gene GIBBERELLIN 2 OXIDASE 2 (GA2ox2) in the vascular tissue, thus regulating the stability of the DELLA protein GIBBERELLIN INSENSITIVE (GAI)-a GA signaling repressor-in the root and, hence, CYCD6;1 expression in the endodermis.
Assuntos
Proteínas de Arabidopsis/genética , Proteínas de Arabidopsis/metabolismo , Arabidopsis/crescimento & desenvolvimento , Ciclinas/genética , Regulação da Expressão Gênica no Desenvolvimento , Regulação da Expressão Gênica de Plantas , Proteínas de Homeodomínio/metabolismo , Arabidopsis/genética , Divisão Celular Assimétrica/genética , Giberelinas/metabolismo , Proteínas de Homeodomínio/genética , MicroRNAs/metabolismo , Oxigenases de Função Mista/genética , Raízes de Plantas/crescimento & desenvolvimento , Plantas Geneticamente ModificadasRESUMO
During organogenesis, coherent organ growth arises from spatiotemporally coordinated decisions of individual cells. In the root of Arabidopsis thaliana, this coordination results in the establishment of a division and a differentiation zone. Cells continuously move through these zones; thus, a major question is how the boundary between these domains, the transition zone, is formed and maintained. By combining molecular genetics with computational modeling, we reveal how an auxin/PLETHORA/ARR-B network controls these dynamic patterning processes. We show that after germination, cell division causes a drop in distal PLT2 levels that enables transition zone formation and ARR12 activation. The resulting PLT2-ARR12 antagonism controls expansion of the division zone (the meristem). The successive ARR1 activation antagonizes PLT2 through inducing the cell-cycle repressor KRP2, thus setting final meristem size. Our work indicates a key role for the interplay between cell division dynamics and regulatory networks in root zonation and transition zone patterning.
Assuntos
Proteínas de Arabidopsis/metabolismo , Arabidopsis/crescimento & desenvolvimento , Ácidos Indolacéticos/farmacologia , Raízes de Plantas/crescimento & desenvolvimento , Fatores de Transcrição/metabolismo , Arabidopsis/efeitos dos fármacos , Arabidopsis/genética , Arabidopsis/metabolismo , Proteínas de Arabidopsis/genética , Proteínas de Ciclo Celular/genética , Proteínas de Ciclo Celular/metabolismo , Regulação da Expressão Gênica no Desenvolvimento , Reguladores de Crescimento de Plantas/farmacologia , Raízes de Plantas/efeitos dos fármacos , Raízes de Plantas/genética , Raízes de Plantas/metabolismo , Fatores de Transcrição/genéticaRESUMO
Hypoxic conditions often arise from waterlogging and flooding, affecting several aspects of plant metabolism, including the uptake of nutrients. We identified a member of the CALCINEURIN ß-LIKE INTERACTING PROTEIN KINASE (CIPK) family in Arabidopsis, CIPK25, which is induced in the root endodermis under low-oxygen conditions. A cipk25 mutant exhibited higher sensitivity to anoxia in conditions of potassium limitation, suggesting that this kinase is involved in the regulation of potassium uptake. Interestingly, we found that CIPK25 interacts with AKT1, the major inward rectifying potassium channel in Arabidopsis. Under anoxic conditions, cipk25 mutant seedlings were unable to maintain potassium concentrations at wild-type levels, suggesting that CIPK25 likely plays a role in modulating potassium homeostasis under low-oxygen conditions. In addition, cipk25 and akt1 mutants share similar developmental defects under waterlogging, further supporting an interplay between CIPK25 and AKT1.
Assuntos
Proteínas de Arabidopsis , Arabidopsis , Oxigênio , Potássio/metabolismo , Proteínas Serina-Treonina Quinases , Arabidopsis/genética , Arabidopsis/metabolismo , Proteínas de Arabidopsis/genética , Proteínas de Arabidopsis/metabolismo , Calcineurina , Homeostase , Raízes de Plantas/metabolismo , Canais de Potássio/genética , Proteínas Serina-Treonina Quinases/genética , Proteínas Serina-Treonina Quinases/metabolismoRESUMO
The root of the plant Arabidopsis thaliana is a dynamic structure in which cells continuously divide and differentiate to sustain its postembryonic undetermined growth. Cells at different developmental stages are organized in distinguished zones whose position and activities are maintained constant during root growth. In this review, we will discuss the latest discoveries on the regulatory networks involved in root zonation and, in particular, in the mechanisms involved in maintaining the position of the transition zone, a root developmental boundary. Developmental boundaries physically divide cells with different functions and identities. The transition zone separates dividing cells from differentiating cells in two functional domains, preserving their identity during root growth and thus controlling root development.
Assuntos
Proteínas de Arabidopsis , Arabidopsis , Ácidos Indolacéticos , Meristema , Raízes de PlantasRESUMO
Abstract: The Arabidopsis root is a dynamic system where the interaction between different plant hormones controls root meristem activity and, thus, organ growth. In the root, a characteristic graded distribution of the hormone auxin provides positional information, coordinating the proliferating and differentiating cell status. The hormone cytokinin shapes this gradient by positioning an auxin minimum in the last meristematic cells. This auxin minimum triggers a cell developmental switch necessary to start the differentiation program, thus, regulating the root meristem size. To position the auxin minimum, cytokinin promotes the expression of the IAA-amido synthase group II gene GH3.17, which conjugates auxin with amino acids, in the most external layer of the root, the lateral root cap tissue. Since additional GH3 genes are expressed in the root, we questioned whether cytokinin to position the auxin minimum also operates via different GH3 genes. Here, we show that cytokinin regulates meristem size by activating the expression of GH3.5 and GH3.6 genes, in addition to GH3.17. Thus, cytokinin activity provides a robust control of auxin activity in the entire organ necessary to regulate root growth.
RESUMO
Plant developmental plasticity relies on the activities of meristems, regions where stem cells continuously produce new cells [1]. The lateral root cap (LRC) is the outermost tissue of the root meristem [1], and it is known to play an important role during root development [2-6]. In particular, it has been shown that mechanical or genetic ablation of LRC cells affect meristem size [7, 8]; however, the molecular mechanisms involved are unknown. Root meristem size and, consequently, root growth depend on the position of the transition zone (TZ), a boundary that separates dividing from differentiating cells [9, 10]. The interaction of two phytohormones, cytokinin and auxin, is fundamental in controlling the position of the TZ [9, 10]. Cytokinin via the ARABIDOPSIS RESPONSE REGULATOR 1 (ARR1) control auxin distribution within the meristem, generating an instructive auxin minimum that positions the TZ [10]. We identify a cytokinin-dependent molecular mechanism that acts in the LRC to control the position of the TZ and meristem size. We show that auxin levels within the LRC cells depends on PIN-FORMED 5 (PIN5), a cytokinin-activated intracellular transporter that pumps auxin from the cytoplasm into the endoplasmic reticulum, and on irreversible auxin conjugation mediated by the IAA-amino synthase GRETCHEN HAGEN 3.17 (GH3.17). By titrating auxin in the LRC, the PIN5 and the GH3.17 genes control auxin levels in the entire root meristem. Overall, our results indicate that the LRC serves as an auxin sink that, under the control of cytokinin, regulates meristem size and root growth.
Assuntos
Proteínas de Arabidopsis/genética , Arabidopsis/metabolismo , Ácidos Indolacéticos/metabolismo , Raízes de Plantas/crescimento & desenvolvimento , Arabidopsis/crescimento & desenvolvimento , Proteínas de Arabidopsis/metabolismo , Citocininas/genética , Citocininas/metabolismo , Meristema/crescimento & desenvolvimento , Meristema/metabolismo , Raízes de Plantas/metabolismoRESUMO
A key question in biology is to understand how interspecies morphological diversities originate. Plant roots present a huge interspecific phenotypical variability, mostly because roots largely contribute to adaptation to different kinds of soils. One example is the interspecific cortex layer number variability, spanning from one to several. Here, we review the latest advances in the understanding of the mechanisms expanding and/or restricting cortical layer number in Arabidopsis thaliana and their involvement in cortex pattern variability among multi-cortical layered species such as Cardamine hirsuta or Oryza sativa.
Assuntos
Arabidopsis/crescimento & desenvolvimento , Cardamine/crescimento & desenvolvimento , Oryza/crescimento & desenvolvimento , Raízes de Plantas/crescimento & desenvolvimento , Arabidopsis/anatomia & histologia , Cardamine/anatomia & histologia , Oryza/anatomia & histologia , Raízes de Plantas/anatomia & histologiaRESUMO
The root apical meristem is established during embryogenesis, when its organizer, the quiescent center, is specified and the stem cell niche is positioned. The SCARECROW-SHORTROOT heterodimer is essential for quiescent center specification and maintenance. As continuous post-embryonic root growth relies upon the SCARECROW-mediated control of the cytokinin/auxin balance, we investigated the role of SCARECROW and SHORTROOT in controlling cytokinin signaling during embryonic quiescent center specification. We found that from embryogenesis onward both SCARECROW and SHORTROOT antagonize cytokinin signaling, thus repressing the expression of the auxin biosynthetic enzyme ANTRANILATHE SYNTHASE BETA 1. This mechanism prevents detrimental and premature high auxin levels in the QC allowing the establishment of a functional embryonic root pole.
Assuntos
Proteínas de Arabidopsis/metabolismo , Arabidopsis/metabolismo , Citocininas/metabolismo , Ácidos Indolacéticos/metabolismo , Nicho de Células-Tronco/fisiologia , Fatores de Transcrição/metabolismo , Arabidopsis/genética , Proteínas de Arabidopsis/genética , Regulação da Expressão Gênica de Plantas , Fatores de Transcrição/genéticaRESUMO
In multicellular systems, the control of cell size is fundamental in regulating the development and growth of the different organs and of the whole organism. In most systems, major changes in cell size can be observed during differentiation processes where cells change their volume to adapt their shape to their final function. How relevant changes in cell volume are in driving the differentiation program is a long-standing fundamental question in developmental biology. In the Arabidopsis root meristem, characteristic changes in the size of the distal meristematic cells identify cells that initiated the differentiation program. Here, we show that changes in cell size are essential for the initial steps of cell differentiation and that these changes depend on the concomitant activation by the plant hormone cytokinin of the EXPAs proteins and the AHA1 and AHA2 proton pumps. These findings identify a growth module that builds on a synergy between cytokinin-dependent pH modification and wall remodeling to drive differentiation through the mechanical control of cell walls.
Assuntos
Arabidopsis/metabolismo , Diferenciação Celular/fisiologia , Células Vegetais/metabolismo , Raízes de Plantas/metabolismo , Arabidopsis/citologia , Proteínas de Arabidopsis/metabolismo , Citocininas/metabolismo , Raízes de Plantas/citologia , ATPases Translocadoras de Prótons/metabolismoRESUMO
Plant postembryonic development takes place in region called meristems that represent a reserve of undifferentiated cells. In the root meristem of Arabidopsis thaliana, all tissues originate from a stem-cell niche. Stem-cell daughters undergo a finite number of cell divisions until they reach the transition zone where divisions cease and cells start to differentiate. For meristem maintenance, and therefore continuous root growth, the rate of cell differentiation must equal the rate of generation of new cells. How this balance is achieved is a central question in plant biology. In this chapter we described protocols to help the operator in approaching developmental studies on the Arabidopsis root meristem.
Assuntos
Arabidopsis/fisiologia , Meristema/fisiologia , Fenótipo , Desenvolvimento Vegetal , Arabidopsis/anatomia & histologia , Arabidopsis/citologia , Meristema/anatomia & histologia , Meristema/citologia , Microscopia , Raízes de Plantas/anatomia & histologia , Raízes de Plantas/citologia , Raízes de Plantas/fisiologiaRESUMO
How the body plan is established and maintained in multicellular organisms is a central question in developmental biology. Thanks to its simple and symmetric structure, the root represents a powerful tool to study the molecular mechanisms underlying the establishment and maintenance of developmental axes. Plant roots show two main axes along which cells pass through different developmental stages and acquire different fates: the root proximodistal axis spans longitudinally from the hypocotyl junction (proximal) to the root tip (distal), whereas the radial axis spans transversely from the vasculature tissue (centre) to the epidermis (outer). Both axes are generated by stereotypical divisions occurring during embryogenesis and are maintained post-embryonically. Here, we review the latest scientific advances on how the correct formation of root proximodistal and radial axes is achieved.
RESUMO
In multicellular organisms, a stringent control of the transition between cell division and differentiation is crucial for correct tissue and organ development. In the Arabidopsis root, the boundary between dividing and differentiating cells is positioned by the antagonistic interaction of the hormones auxin and cytokinin. Cytokinin affects polar auxin transport, but how this impacts the positional information required to establish this tissue boundary, is still unknown. By combining computational modeling with molecular genetics, we show that boundary formation is dependent on cytokinin's control on auxin polar transport and degradation. The regulation of both processes shapes the auxin profile in a well-defined auxin minimum. This auxin minimum positions the boundary between dividing and differentiating cells, acting as a trigger for this developmental transition, thus controlling meristem size.
Assuntos
Arabidopsis/metabolismo , Arabidopsis/fisiologia , Diferenciação Celular/fisiologia , Divisão Celular/fisiologia , Ácidos Indolacéticos/metabolismo , Raízes de Plantas/metabolismo , Raízes de Plantas/fisiologia , Proteínas de Arabidopsis/metabolismo , Transporte Biológico/fisiologia , Citocininas/metabolismo , Regulação da Expressão Gênica de Plantas/fisiologia , Meristema/metabolismo , Meristema/fisiologia , Reguladores de Crescimento de Plantas/metabolismo , Transdução de Sinais/fisiologiaRESUMO
Maintenance of mitotic cell clusters such as meristematic cells depends on their capacity to maintain the balance between cell division and cell differentiation necessary to control organ growth. In the Arabidopsis thaliana root meristem, the antagonistic interaction of two hormones, auxin and cytokinin, regulates this balance by positioning the transition zone, where mitotically active cells lose their capacity to divide and initiate their differentiation programs. In animals, a major regulator of both cell division and cell differentiation is the tumor suppressor protein RETINOBLASTOMA. Here, we show that similarly to its homolog in animal systems, the plant RETINOBLASTOMA-RELATED (RBR) protein regulates the differentiation of meristematic cells at the transition zone by allowing mRNA accumulation of AUXIN RESPONSE FACTOR19 (ARF19), a transcription factor involved in cell differentiation. We show that both RBR and the cytokinin-dependent transcription factor ARABIDOPSIS RESPONSE REGULATOR12 are required to activate the transcription of ARF19, which is involved in promoting cell differentiation and thus root growth.
Assuntos
Proteínas de Arabidopsis/metabolismo , Arabidopsis/metabolismo , Citocininas/metabolismo , Meristema/citologia , Raízes de Plantas/metabolismo , Arabidopsis/citologia , Arabidopsis/genética , Proteínas de Arabidopsis/genética , Diferenciação Celular , Regulação da Expressão Gênica de Plantas , Histidina Quinase , Meristema/genética , Meristema/metabolismo , Raízes de Plantas/citologia , Plantas Geneticamente Modificadas , Proteínas Quinases/genética , Proteínas Quinases/metabolismo , Transdução de Sinais , Fatores de Transcrição/genética , Fatores de Transcrição/metabolismoRESUMO
A critical issue in development is the coordination of the activity of stem cell niches with differentiation of their progeny to ensure coherent organ growth. In the plant root, these processes take place at opposite ends of the meristem and must be coordinated with each other at a distance. Here, we show that in Arabidopsis, the gene SCR presides over this spatial coordination. In the organizing center of the root stem cell niche, SCR directly represses the expression of the cytokinin-response transcription factor ARR1, which promotes cell differentiation, controlling auxin production via the ASB1 gene and sustaining stem cell activity. This allows SCR to regulate, via auxin, the level of ARR1 expression in the transition zone where the stem cell progeny leaves the meristem, thus controlling the rate of differentiation. In this way, SCR simultaneously controls stem cell division and differentiation, ensuring coherent root growth.
Assuntos
Arabidopsis/citologia , Diferenciação Celular , Meristema/citologia , Células-Tronco/citologia , Arabidopsis/genética , Arabidopsis/metabolismo , Proteínas de Arabidopsis/genética , Proteínas de Arabidopsis/metabolismo , Diferenciação Celular/efeitos dos fármacos , Citocininas/farmacologia , Regulação da Expressão Gênica de Plantas/efeitos dos fármacos , Proteínas de Fluorescência Verde/metabolismo , Ácidos Indolacéticos/metabolismo , Meristema/efeitos dos fármacos , Meristema/metabolismo , Modelos Biológicos , Nicho de Células-Tronco/efeitos dos fármacos , Nicho de Células-Tronco/genética , Células-Tronco/efeitos dos fármacos , Células-Tronco/metabolismoRESUMO
A key question in plant developmental biology is how cell division and cell differentiation are balanced to modulate organ growth and shape organ size. In recent years, several advances have been made in understanding how this balance is achieved during root development. In the Arabidopsis root meristem, stem cells in the apical region of the meristem self-renew and produce daughter cells that differentiate in the distal meristem transition zone. Several factors have been implicated in controlling the different functional zones of the root meristem to modulate root growth; among these, plant hormones have been shown to play a main role. In this review, we summarize recent findings regarding the role of hormone signaling and transcriptional networks in regulating root development.
Assuntos
Meristema/crescimento & desenvolvimento , Arabidopsis/citologia , Arabidopsis/embriologia , Meristema/embriologia , Modelos Biológicos , Nicho de Células-TroncoRESUMO
The chromatin modifying Polycomb group (PcG) and trithorax group (trxG) proteins are central regulators of cell identity that maintain a tightly controlled balance between cell proliferation and cell differentiation. The opposing activities of PcG and trxG proteins ensure the correct expression of specific transcriptional programs at defined developmental stages. Here, we report that the chromatin remodeling factor PICKLE (PKL) and the PcG protein CURLY LEAF (CLF) antagonistically determine root meristem activity. Whereas loss of PKL function caused a decrease in meristematic activity, loss of CLF function increased meristematic activity. Alterations of meristematic activity in pkl and clf mutants were not connected with changes in auxin concentration but correlated with decreased or increased expression of root stem cell and meristem marker genes, respectively. Root stem cell and meristem marker genes are modified by the PcG-mediated trimethylation of histone H3 on lysine 27 (H3K27me3). Decreased expression levels of root stem cell and meristem marker genes in pkl correlated with increased levels of H3K27me3, indicating that root meristem activity is largely controlled by the antagonistic activity of PcG proteins and PKL.
Assuntos
Proteínas de Arabidopsis/metabolismo , Arabidopsis/genética , Proteínas de Homeodomínio/metabolismo , Meristema/crescimento & desenvolvimento , Raízes de Plantas/crescimento & desenvolvimento , Proteínas Repressoras/metabolismo , Arabidopsis/citologia , Arabidopsis/crescimento & desenvolvimento , Arabidopsis/metabolismo , Diferenciação Celular , Divisão Celular , Montagem e Desmontagem da Cromatina , DNA Helicases , Regulação da Expressão Gênica no Desenvolvimento , Regulação da Expressão Gênica de Plantas , Histonas/metabolismo , Meristema/citologia , Meristema/metabolismo , Metilação , Mutação , Raízes de Plantas/citologia , Raízes de Plantas/genética , Raízes de Plantas/metabolismo , Proteínas do Grupo PolycombRESUMO
Upon seed germination, apical meristems grow as cell division prevails over differentiation and reach their final size when division and differentiation reach a balance. In the Arabidopsis root meristem, this balance results from the interaction between cytokinin (promoting differentiation) and auxin (promoting division) through a regulatory circuit whereby the ARR1 cytokinin-responsive transcription factor activates the gene SHY2, which negatively regulates the PIN genes encoding auxin transport facilitators. However, it remains unknown how the final meristem size is set, i.e., how a change in the relative rates of cell division and differentiation is brought about to cause meristem growth to stop. Here, we show that during meristem growth, expression of SHY2 is driven by another cytokinin-response factor, ARR12, and that completion of growth is brought about by the upregulation of SHY2 caused by both ARR12 and ARR1: this leads to an increase in cell differentiation rate that balances it with division, thus setting root meristem size. We also show that gibberellins selectively repress expression of ARR1 at early stages of meristem development, and that the DELLA protein REPRESSOR OF GA 1-3 (RGA) mediates this negative control.