GeBP/GPL Transcription Factors Regulate a Subset ofCPR5-Dependent Processes    

Abstract

The CONSTITUTIVE EXPRESSOR OF PATHOGENESIS-RELATED GENES5 (CPR5) gene of Arabidopsis (Arabidopsis thaliana) encodes a putative membrane protein of unknown biochemical function and displays highly pleiotropic functions, particularly in pathogen responses, cell proliferation, cell expansion, and cell death. Here, we demonstrate a link between CPR5 and the GLABRA1 ENHANCER BINDING PROTEIN (GeBP) family of transcription factors. We investigated the primary role of the GeBP/GeBP-like (GPL) genes using transcriptomic analysis of the quadruple gebp gpl1,2,3 mutant and one overexpressing line that displays several cpr5-like phenotypes including dwarfism, spontaneous necrotic lesions, and increased pathogen resistance. We found that GeBP/GPLs regulate a set of genes that represents a subset of the CPR5 pathway. This subset includes genes involved in response to stress as well as cell wall metabolism. Analysis of the quintuple gebp gpl1,2,3 cpr5 mutant indicates that GeBP/GPLs are involved in the control of cell expansion in a CPR5-dependent manner but not in the control of cell proliferation. In addition, to our knowledge, we provide the first evidence that the CPR5 protein is localized in the nucleus of plant cells and that a truncated version of the protein with no transmembrane domain can trigger cpr5-like processes when fused to the VP16 constitutive transcriptional activation domain. Our results provide clues on how CPR5 and GeBP/GPLs play opposite roles in the control of cell expansion and suggest that the CPR5 protein is involved in transcription.Pleiotropic genes participate in many seemingly unrelated traits and play a key role in fundamental aspects of life such as evolution, development, and aging. In Arabidopsis (Arabidopsis thaliana), the CONSTITUTIVE EXPRESSOR OF PATHOGENESIS-RELATED GENES5 (CPR5; CPR5/HYS1/OLD1) gene is involved in highly pleiotropic developmental processes. Although initially identified based on their constitutive pathogen response phenotype, mutants of CPR5 possess striking phenotypes including (1) enhanced constitutive expression of pathogen-related (PR) genes associated with increased pathogen resistance (Bowling et al., 1994;Boch et al., 1998); (2) defects in cell division, expansion, endoreduplication, and cell wall biogenesis associated with a reduced stature (Kirik et al., 2001;Brininstool et al., 2008); (3) spontaneous lesions mimicking cell death and accelerated leaf senescence (Jing et al., 2002(Jing et al., , 2007Yoshida et al., 2002); and (4) modified hormonal and metabolic responses in the salicylic acid, jasmonic acid, abscisic acid, ethylene, and sugar-sensing pathways (Clarke 1 This work was supported by the Centre National de la Recherche Scientifique and Université Joseph Fourier (Grenoble) and a National Science Foundation grant (no. IOS 0744566 to J.C.L.). F.C. was a recipient of a Ph.D. thesis fellowship from the Ministère de la Recherche et de l'Enseignement Supérieur.2 Present address: Plant Molecular Genetics Department, Centro Nacional de Biotecnología, Campus de ...

STOREKEEPER RELATED1/G-Element Binding Protein (STKR1) Interacts with Protein Kinase SnRK1

“…In this study, we show by independent methods that both Arabidopsis SnRK1 a-subunit isoforms interact with STKR1 also in planta. BiFC assays show that the interaction occurs predominantly inside the plant cell nucleus, which is consistent with a proposed role of STKR1 in transcriptional regulation (Curaba et al, 2003;Chevalier et al, 2008;Perazza et al, 2011) and suggests a functional link between STKR1-mediated transcriptional regulation and SnRK1 signaling inside the nucleus. Previous data suggest that SnRK1 can be localized to the cytosol as well as to the nucleus in Arabidopsis and N. benthamiana (Gazzarrini et al, 2004;Bitrián et al, 2011) and that the binding of SnRK1 to nucleus-localized proteins can change the partitioning in favor of a nuclear localization of the kinase (Nietzsche et al, 2014).…”

“…The similarities between cpr5 and STKR1-overexpressing plants raise the possibility that STKR1 and its related GPL proteins are involved in a subset of CPR5 responses. It was shown previously that overexpression of GPL2 with constitutive transcriptional activation activity or a quadruple knockout of stkr1/gpl1,2,3 also leads to transcriptional changes similar to cpr5 (Perazza et al, 2011), lending further support to the notion that STKR1/GPL proteins and CPR5 share a subset of regulated genes. Interestingly, both cpr5 and stkr1/gpl1,2,3 plants display misregulation of the SnRK1 marker gene ASN1 (Perazza et al, 2011).…”

“…It was shown previously that overexpression of GPL2 with constitutive transcriptional activation activity or a quadruple knockout of stkr1/gpl1,2,3 also leads to transcriptional changes similar to cpr5 (Perazza et al, 2011), lending further support to the notion that STKR1/GPL proteins and CPR5 share a subset of regulated genes. Interestingly, both cpr5 and stkr1/gpl1,2,3 plants display misregulation of the SnRK1 marker gene ASN1 (Perazza et al, 2011). Thus, other than being a kinase substrate in a direct SnRK1 signaling pathway, STKR1 could be involved in the facilitation of nuclear signaling events, including SnRK1, but likely also of other nuclearcytoplasmic proteins.…”

“…One protein found to interact with both SnRK1 a-subunits in yeast was STOREKEEPER RE-LATED1 (STKR1), also known as GL1 enhancer binding protein (GeBP; At4g00270.1; Curaba et al, 2003). STKR1/GeBP together with three GeBP-like (GPL) genes belong to a small gene family encoding noncanonical Leu zipper transcription factors with redundant roles in the indirect regulation of some cytokinin response genes in Arabidopsis (Chevalier et al, 2008) and that also might be involved in the transcriptional regulation of certain stress responses (Perazza et al, 2011). A STOREKEEPER protein has been described to regulate Suc-inducible expression of patatin in potato (Solanum tuberosum) tubers, suggesting that this family of transcriptional regulators also could be involved in relaying metabolic signals to adjust gene expression (Zourelidou et al, 2002).…”

The Agrobacterium F-Box Protein Effector VirF Destabilizes the Arabidopsis GLABROUS1 Enhancer/Binding Protein-Like Transcription Factor VFP4, a Transcriptional Activator of Defense Response Genes

“…GeBP/GPL proteins are a class of leucine-zipper transcription factors that have been implicated in regulation of cell expansion, cytokinin response, and stress and defense responses (Chevalier et al 2008; Perazza et al 2011). For example, overexpressing Arabidopsis GPL2 enhances plant resistance to bacterial pathogens (Perazza et al 2011). As a potential transcription factor and consistent with its ability to enter the nucleus (Fig.…”