123
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      A Central Regulatory System Largely Controls Transcriptional Activation and Repression Responses to Phosphate Starvation in Arabidopsis

      research-article

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Plants respond to different stresses by inducing or repressing transcription of partially overlapping sets of genes. In Arabidopsis, the PHR1 transcription factor (TF) has an important role in the control of phosphate (Pi) starvation stress responses. Using transcriptomic analysis of Pi starvation in phr1, and phr1 phr1-like (phl1) mutants and in wild type plants, we show that PHR1 in conjunction with PHL1 controls most transcriptional activation and repression responses to phosphate starvation, regardless of the Pi starvation specificity of these responses. Induced genes are enriched in PHR1 binding sequences (P1BS) in their promoters, whereas repressed genes do not show such enrichment, suggesting that PHR1(-like) control of transcriptional repression responses is indirect. In agreement with this, transcriptomic analysis of a transgenic plant expressing PHR1 fused to the hormone ligand domain of the glucocorticoid receptor showed that PHR1 direct targets (i.e., displaying altered expression after GR:PHR1 activation by dexamethasone in the presence of cycloheximide) corresponded largely to Pi starvation-induced genes that are highly enriched in P1BS. A minimal promoter containing a multimerised P1BS recapitulates Pi starvation-specific responsiveness. Likewise, mutation of P1BS in the promoter of two Pi starvation-responsive genes impaired their responsiveness to Pi starvation, but not to other stress types. Phylogenetic footprinting confirmed the importance of P1BS and PHR1 in Pi starvation responsiveness and indicated that P1BS acts in concert with other cis motifs. All together, our data show that PHR1 and PHL1 are partially redundant TF acting as central integrators of Pi starvation responses, both specific and generic. In addition, they indicate that transcriptional repression responses are an integral part of adaptive responses to stress.

          Author Summary

          As sessile organisms, plants are often exposed to stress conditions, and have evolved adaptive responses to protect themselves from different types of stress. Some responses are stress type-specific whereas others are common to different stress types. Understanding how these responses are controlled is crucial for rational improvement of stress tolerance, a limiting factor in crop productivity. Here we examined the physiological and molecular responses to phosphate starvation and found that a single transcription factor family, represented by PHOSPHATE STARVATION RESPONSE REGULATOR 1 (PHR1), has a central role in the control of specific and shared phosphate starvation stress responses. In consonance with the importance of PHR1, we found that the PHR1-binding sequence, present in most PHR1 direct targets, is a crucial cis motif for Pi starvation responsiveness. An artificial promoter controlled by PHR1 recapitulates responsiveness to Pi starvation and to modulators of this response, qualifying PHR1 family members as central integrators in Pi starvation signalling. This central integrator system also controls most transcriptional repression responses to Pi starvation, indicating that they are an integral part of the adaptive response, and not a consequence of plant malfunction due to stress.

          Related collections

          Most cited references53

          • Record: found
          • Abstract: found
          • Article: not found

          Leaf senescence.

          Leaf senescence constitutes the final stage of leaf development and is critical for plants' fitness as nutrient relocation from leaves to reproducing seeds is achieved through this process. Leaf senescence involves a coordinated action at the cellular, tissue, organ, and organism levels under the control of a highly regulated genetic program. Major breakthroughs in the molecular understanding of leaf senescence were achieved through characterization of various senescence mutants and senescence-associated genes, which revealed the nature of regulatory factors and a highly complex molecular regulatory network underlying leaf senescence. The genetically identified regulatory factors include transcription regulators, receptors and signaling components for hormones and stress responses, and regulators of metabolism. Key issues still need to be elucidated, including cellular-level analysis of senescence-associated cell death, the mechanism of coordination among cellular-, organ-, and organism-level senescence, the integration mechanism of various senescence-affecting signals, and the nature and control of leaf age.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox.

            High-throughput gene expression analysis has become a frequent and powerful research tool in biology. At present, however, few software applications have been developed for biologists to query large microarray gene expression databases using a Web-browser interface. We present GENEVESTIGATOR, a database and Web-browser data mining interface for Affymetrix GeneChip data. Users can query the database to retrieve the expression patterns of individual genes throughout chosen environmental conditions, growth stages, or organs. Reversely, mining tools allow users to identify genes specifically expressed during selected stresses, growth stages, or in particular organs. Using GENEVESTIGATOR, the gene expression profiles of more than 22,000 Arabidopsis genes can be obtained, including those of 10,600 currently uncharacterized genes. The objective of this software application is to direct gene functional discovery and design of new experiments by providing plant biologists with contextual information on the expression of genes. The database and analysis toolbox is available as a community resource at https://www.genevestigator.ethz.ch.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae.

              Plants have evolved a number of adaptive responses to cope with growth in conditions of limited phosphate (Pi) supply involving biochemical, metabolic, and developmental changes. We prepared an EMS-mutagenized M(2) population of an Arabidopsis thaliana transgenic line harboring a reporter gene specifically responsive to Pi starvation (AtIPS1::GUS), and screened for mutants altered in Pi starvation regulation. One of the mutants, phr1 (phosphate starvation response 1), displayed reduced response of AtIPS1::GUS to Pi starvation, and also had a broad range of Pi starvation responses impaired, including the responsiveness of various other Pi starvation-induced genes and metabolic responses, such as the increase in anthocyanin accumulation. PHR1 was positionally cloned and shown be related to the PHOSPHORUS STARVATION RESPONSE 1 (PSR1) gene from Chlamydomonas reinhardtii. A GFP::PHR1 protein fusion was localized in the nucleus independently of Pi status, as is the case for PSR1. PHR1 is expressed in Pi sufficient conditions and, in contrast to PSR1, is only weakly responsive to Pi starvation. PHR1, PSR1, and other members of the protein family share a MYB domain and a predicted coiled-coil (CC) domain, defining a subtype within the MYB superfamily, the MYB-CC family. Therefore, PHR1 was found to bind as a dimer to an imperfect palindromic sequence. PHR1-binding sequences are present in the promoter of Pi starvation-responsive structural genes, indicating that this protein acts downstream in the Pi starvation signaling pathway.
                Bookmark

                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, USA )
                1553-7390
                1553-7404
                September 2010
                September 2010
                9 September 2010
                : 6
                : 9
                : e1001102
                Affiliations
                [1]Department of Plant Molecular Genetics, Centro Nacional de Biotecnología-CSIC, Madrid, Spain
                The Salk Institute for Biological Studies, United States of America
                Author notes
                [¤a]

                Current address: CBGP, Pozuelo de Alarcón, Madrid, Spain

                [¤b]

                Current address: SECUGEN, Madrid, Spain

                Conceived and designed the experiments: RB GC JPA. Performed the experiments: RB GC FL MIP JPA. Analyzed the data: RB GC JPA. Contributed reagents/materials/analysis tools: VR JPP RS AL. Wrote the paper: RB GC JPA.

                Article
                09-PLGE-RA-1054R3
                10.1371/journal.pgen.1001102
                2936532
                20838596
                1bb5018b-267a-4353-adc9-9f505e4f1c06
                Bustos et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 22 June 2009
                : 29 July 2010
                Page count
                Pages: 15
                Categories
                Research Article
                Genetics and Genomics/Plant Genetics and Gene Expression
                Plant Biology/Plant Biochemistry and Physiology
                Plant Biology/Plant-Environment Interactions

                Genetics
                Genetics

                Comments

                Comment on this article