The survival of plants, as sessile organisms, depends on a series of postembryonic developmental events that determine the final architecture of plants and allow them to contend with a continuously changing environment. Modulation of cell differentiation and organ formation by environmental signals has not been studied in detail. Here, we report that alterations in the pattern of lateral root (LR) formation and emergence in response to phosphate (Pi) availability is mediated by changes in auxin sensitivity in Arabidopsis thaliana roots. These changes alter the expression of auxin-responsive genes and stimulate pericycle cells to proliferate. Modulation of auxin sensitivity by Pi was found to depend on the auxin receptor TRANSPORT INHIBITOR RESPONSE1 (TIR1) and the transcription factor AUXIN RESPONSE FACTOR19 (ARF19). We determined that Pi deprivation increases the expression of TIR1 in Arabidopsis seedlings and causes AUXIN/INDOLE-3-ACETIC ACID (AUX/IAA) auxin response repressors to be degraded. Based on our results, we propose a model in which auxin sensitivity is enhanced in Pi-deprived plants by an increased expression of TIR1, which accelerates the degradation of AUX/IAA proteins, thereby unshackling ARF transcription factors that activate/repress genes involved in LR formation and emergence.
SUMMARY In plants, where cells cannot migrate, asymmetric cell divisions (ACDs) must be confined to the appropriate spatial context. We investigate tissue-generating asymmetric divisions in a stem cell daughter within the Arabidopsis root. Spatial restriction of these divisions requires physical binding of the stem cell regulator SCARECROW (SCR) by the RETINOBLASTOMA-RELATED (RBR) protein. In the stem cell niche, SCR activity is counteracted by phosphorylation of RBR through a cyclinD6;1-CDK complex. This cyclin is itself under transcriptional control of SCR and its partner SHORT ROOT (SHR), creating a robust bistable circuit with either high or low SHR-SCR complex activity. Auxin biases this circuit by promoting CYCD6;1 transcription. Mathematical modeling shows that ACDs are only switched on after integration of radial and longitudinal information, determined by SHR and auxin distribution, respectively. Coupling of cell-cycle progression to protein degradation resets the circuit, resulting in a “flip flop” that constrains asymmetric cell division to the stem cell region.
When growing under limiting phosphate (P) conditions, Arabidopsis thaliana plants show dramatic changes in root architecture, including a reduction in primary root length, increased formation of lateral roots and greater formation of root hairs. Here we report that primary root growth inhibition by low P is caused by a shift from an indeterminate to a determinate developmental program. In the primary root, the low P-induced determinate growth program initiates with a reduction of cell elongation followed by the progressive loss of meristematic cells. At later stages, cell proliferation ceases and cell differentiation takes place at the former cell elongation and meristematic regions of the primary root. In low P, not only the primary but also almost all mature lateral roots enter the determinate developmental program. Kinetic studies of expression of the cell cycle marker CycB1;1:uidA and the quiescent center (QC) identity marker QC46:GUS showed that in low P conditions, reduction in proliferation in the primary root was preceded by alterations in the QC. These results suggest that in Arabidopsis, P limitation can induce a determinate root developmental program that plays an important role in altering root system architecture and that the QC could act as a sensor of environmental signals.
Low phosphate (Pi) availability is one of the major constraints for plant productivity in natural and agricultural ecosystems. Plants have evolved a myriad of developmental and biochemical mechanisms to increase internal Pi uptake and utilization efficiency. One important biochemical pathway leading to an increase in internal Pi availability is the hydrolysis of phospholipids. Hydrolyzed phospholipids are replaced by nonphosphorus lipids such as galactolipids and sulfolipids, which help to maintain the functionality and structure of membrane systems. Here we report that a member of the Arabidopsis phospholipase D gene family (PLDZ2) is gradually induced upon Pi starvation in both shoots and roots. From lipid content analysis we show that an Arabidopsis pldz2 mutant is defective in the hydrolysis of phospholipids and has a reduced capacity to accumulate galactolipids under limiting Pi conditions. Morphological analysis of the pldz2 root system shows a premature change in root architecture in response to Pi starvation. These results show that PLDZ2 is involved in the eukaryotic galactolipid biosynthesis pathway, specifically in hydrolyzing phosphatidylcholine and phosphatidylethanolamine to produce diacylglycerol for digalactosyldiacylglycerol synthesis and free Pi to sustain other Pi-requiring processes.phosphate starvation ͉ phospholipids ͉ root architecture ͉ sulfolipids P hosphate (Pi) influences virtually all developmental and biochemical processes in plants. Pi is not only a constituent of key cell molecules such as ATP, nucleic acids, and phospholipids, but it is also a pivotal metabolic regulator of many processes including energy transfer, protein activation, and carbon and nitrogen metabolism. However, Pi availability can be one of the major constraints for plant growth in both natural and agricultural ecosystems because of its low mobility and high absorption capacity in the soil. As a response to this limitation, plants have evolved a range of developmental, biochemical, and symbiotic adaptive strategies to cope with low Pi availability (1, 2). In Arabidopsis, a general, 3-fold strategy to cope with low Pi availability has been described. (i) The release and uptake of Pi from external sources that are not readily available for plant uptake. This mechanism includes the transcriptional activation of high-affinity Pi transporters and the excretion of RNases, acid phosphatases, and organic acids (3-5). (ii) Changes in the architecture of the root system that reflect alterations in cell length, root meristem activity, root hair elongation, and an increased number of lateral roots (6, 7). These changes presumably increase the exploratory capacity of the root and the absorptive surface area. (iii) Optimization of Pi utilization due to a wide range of metabolic alterations, and the mobilization of Pi from internal reserves by the hydrolysis of nucleic acids, proteins, and the recycling of Pi from membrane phospholipids.During Pi deprivation, the total content of diverse phospholipids such as phosphatidylcholin...
Ben Scheres and colleagues report that in the growing tip of plant roots, a gene regulatory network that includes the plant homologue of Retinoblastoma regulates the divisions of long-term stem cells to replenish tissue and to protect the root stem cell niche.
Plant cells cannot rearrange their positions; therefore, sharp tissue boundaries must be accurately programmed. Movement of the cell fate regulator SHORT-ROOT from the stele to the ground tissue has been associated with transferring positional information across tissue boundaries. The zinc finger BIRD protein JACKDAW has been shown to constrain SHORT-ROOT movement to a single layer, and other BIRD family proteins were postulated to counteract JACKDAW's role in restricting SHORT-ROOT action range. Here, we report that regulation of SHORT-ROOT movement requires additional BIRD proteins whose action is critical for the establishment and maintenance of the boundary between stele and ground tissue. We show that BIRD proteins act in concert and not in opposition. The exploitation of asymmetric redundancies allows the separation of two BIRD functions: constraining SHORT-ROOT spread through nuclear retention and transcriptional regulation of key downstream SHORT-ROOT targets, including SCARECROW and CYCLIND6. Our data indicate that BIRD proteins promote formative divisions and tissue specification in the Arabidopsis thaliana root meristem ground tissue by tethering and regulating transcriptional competence of SHORT-ROOT complexes. As a result, a tissue boundary is not "locked in" after initial patterning like in many animal systems, but possesses considerable developmental plasticity due to continuous reliance on mobile transcription factors.
Phosphate (Pi) availability is a significant limiting factor for plant growth and productivity in both natural and agricultural systems. To cope with such limiting conditions, plants have evolved a myriad of developmental and biochemical strategies to enhance the efficiency of Pi acquisition and assimilation to avoid nutrient starvation. In the past decade, these responses have been studied in detail at the level of gene expression; however, the possible epigenetic components modulating plant Pi starvation responses have not been thoroughly investigated. Here, we report that an extensive remodeling of global DNA methylation occurs in Arabidopsis plants exposed to low Pi availability, and in many instances, this effect is related to changes in gene expression. Modifications in methylation patterns within genic regions were often associated with transcriptional activation or repression, revealing the important role of dynamic methylation changes in modulating the expression of genes in response to Pi starvation. Moreover, Arabidopsis mutants affected in DNA methylation showed that changes in DNA methylation patterns are required for the accurate regulation of a number of Pi-starvation-responsive genes and that DNA methylation is necessary to establish proper morphological and physiological phosphate starvation responses.phosphate | epigenetics | abiotic stress | DNA methylation | methylome D uring evolution, plants have acquired a series of adaptive strategies that allow them to survive and complete their life cycles under adverse environmental conditions. Consequently, plants have evolved a myriad of physiological, cellular, and molecular mechanisms to cope with challenging environments. Plant responses to environmental stress include modifications in postembryonic development and metabolic reprogramming, which are highly dependent on the regulation of gene expression. It is well documented that gene regulation at the transcriptional and posttranscriptional levels plays an important role in plant stress responses; however, more recent evidence suggests that epigenetic mechanisms also play an important role in reprogramming gene expression in response to environmental cues and that epigenetic marks can serve as a priming mechanism to prepare future generations to better withstand biotic and abiotic stresses (1-3). These epigenetic marks include, but are not restricted to, posttranslational histone modifications and DNA methylation, a mechanism by which cytosine DNA methylation regulates the silencing and control of transposable elements (TEs) and repetitive sequences, genomic imprinting, and gene silencing. In plants, this DNA methylation modification is applied in three different sequence contexts (CG, CHG, and CHH, where H = A, C, or T), and the involvement of different pathways is necessary for the establishment, maintenance, and modification of DNA methylation patterns in these contexts (4, 5). These epigenetic processes can interact to orchestrate new heterochromatin states that modify gene expression [for re...
Nuclear Factor Y (NF-Y) is a heterotrimeric complex formed by NF-YA/NF-YB/NF-YC subunits that binds to the CCAAT-box in eukaryotic promoters. In contrast to other organisms, in which a single gene encodes each subunit, in plants gene families of over 10 members encode each of the subunits. Here we report that five members of the Arabidopsis thaliana NF-YA family are strongly induced by several stress conditions via transcriptional and miR169-related post-transcriptional mechanisms. Overexpression of NF-YA2, 7 and 10 resulted in dwarf late-senescent plants with enhanced tolerance to several types of abiotic stress. These phenotypes are related to alterations in sucrose/starch balance and cell elongation observed in NF-YA overexpressing plants. The use of transcriptomic analysis of transgenic plants that express miR169-resistant versions of NF-YA2, 3, 7, and 10 under an estradiol inducible system, as well as a dominant-repressor version of NF-YA2 revealed a set of genes, whose promoters are enriched in NF-Y binding sites (CCAAT-box) and that may be directly regulated by the NF-Y complex. This analysis also suggests that NF-YAs could participate in modulating gene regulation through positive and negative mechanisms. We propose a model in which the increase in NF-YA transcript levels in response to abiotic stress is part of an adaptive response to adverse environmental conditions in which a reduction in plant growth rate plays a key role.
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