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Conserved redox-dependent DNA binding of ROXY glutaredoxins with TGA transcription factors.

ABSTRACT: The Arabidopsis thaliana CC-type glutaredoxin (GRX) ROXY1 and the bZIP TGA transcription factor (TF) PERIANTHIA (PAN) interact in the nucleus and together regulate petal development. The CC-type GRXs exist exclusively in land plants, and in contrast to the ubiquitously occurring CPYC and CGFS GRX classes, only the CC-type GRXs expanded strongly during land plant evolution. Phylogenetic analyses show that TGA TFs evolved before the CC-type GRXs in charophycean algae. MpROXY1/2 and MpTGA were isolated from the liverwort Marchantia polymorpha to analyze regulatory ROXY/TGA interactions in a basal land plant. Homologous and heterologous protein interaction studies demonstrate that nuclear ROXY/TGA interactions are conserved since the occurrence of CC-type GRXs in bryophytes and mediated by a conserved ROXY C-terminus. Redox EMSA analyses show a redox-sensitive binding of MpTGA to the cis-regulatory as-1-like element. Furthermore, we demonstrate that MpTGA binds together with MpROXY1/2 to this motif under reducing conditions, whereas this interaction is not observed under oxidizing conditions. Remarkably, heterologous complementation studies reveal a strongly conserved land plant ROXY activity, suggesting an ancestral role for CC-type GRXs in modulating the activities of TGA TFs. Super-resolution microscopy experiments detected a strong colocalization of ROXY1 with the active form of the RNA polymerase II in the nucleus. Together, these data shed new light on the function of ROXYs and TGA TFs and the evolution of redox-sensitive transcription regulation processes, which likely contributed to adapt land plants to novel terrestrial habitats.

SUBMITTER: Gutsche N

PROVIDER: S-EPMC6508501 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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Conserved redox-dependent DNA binding of ROXY glutaredoxins with TGA transcription factors.

Gutsche Nora N Holtmannspötter Michael M Maß Lucia L O'Donoghue Martin M Busch Andrea A Lauri Andrea A Schubert Veit V Zachgo Sabine S

Plant direct 20171214 6

The <i>Arabidopsis thaliana</i> CC-type glutaredoxin (GRX) ROXY1 and the bZIP TGA transcription factor (TF) PERIANTHIA (PAN) interact in the nucleus and together regulate petal development. The CC-type GRXs exist exclusively in land plants, and in contrast to the ubiquitously occurring CPYC and CGFS GRX classes, only the CC-type GRXs expanded strongly during land plant evolution. Phylogenetic analyses show that TGA TFs evolved before the CC-type GRXs in charophycean algae. Mp<i>ROXY1/2</i> and M ...[more]

PMID: 31245678

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Project description:The Arabidopsis TGA transcription factor (TF) PERIANTHIA (PAN) regulates the formation of the floral organ primordia as revealed by the pan mutant forming an abnormal pentamerous arrangement of the outer three floral whorls. The Arabidopsis TGA bZIP TF family comprises 10 members, of which PAN and TGA9/10 control flower developmental processes and TGA1/2/5/6 participate in stress-responses. For the TGA1 protein it was shown that several cysteines can be redox-dependently modified. TGA proteins interact in the nucleus with land plant-specific glutaredoxins, which may alter their activities posttranslationally. Here, we investigated the DNA-binding of PAN to the AAGAAT motif under different redox-conditions. The AAGAAT motif is localized in the second intron of the floral homeotic regulator AGAMOUS (AG), which controls stamen and carpel development as well as floral determinacy. Whereas PAN protein binds to this regulatory cis-element under reducing conditions, the interaction is strongly reduced under oxidizing conditions in EMSA studies. The redox-sensitive DNA-binding is mediated via a special PAN N-terminus, which is not present in other Arabidopsis TGA TFs and comprises five cysteines. Two N-terminal PAN cysteines, Cys68 and Cys87, were shown to form a disulfide bridge and Cys340, localized in a C-terminal putative transactivation domain, can be S-glutathionylated. Comparative land plant analyses revealed that the AAGAAT motif exists in asterid and rosid plant species. TGA TFs with N-terminal extensions of variable length were identified in all analyzed seed plants. However, a PAN-like N-terminus exists only in the rosids and exclusively Brassicaceae homologs comprise four to five of the PAN N-terminal cysteines. Redox-dependent modifications of TGA cysteines are known to regulate the activity of stress-related TGA TFs. Here, we show that the N-terminal PAN cysteines participate in a redox-dependent control of the PAN interaction with a highly conserved regulatory AG cis-element, emphasizing the importance of redox-modifications in the regulation of flower developmental processes.

Dataset Information

Conserved redox-dependent DNA binding of ROXY glutaredoxins with TGA transcription factors.

Publications

Conserved redox-dependent DNA binding of ROXY glutaredoxins with TGA transcription factors.

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