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GIP1 protein is a novel cofactor that regulates DNA-binding affinity of redox-regulated members of bZIP transcription factors involved in the early stages of Arabidopsis development

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Abstract

In response to environmental light signals, gene expression adjustments play an important role in regulation of photomorphogenesis. LHCB2.4 is among the genes responsive to light signals, and its expression is regulated by redox-regulated members of G-group bZIP transcription factors. The biochemical interrelations of GBF1-interacting protein 1 (GIP1) and the G-group bZIP transcription factors have been investigated. GIP1, previously shown to enhance DNA-binding activities of maize GBF1 and Arabidopsis GBF3, is a plant specific protein that reduces DNA-binding activity of AtbZIP16, AtbZIP68, and AtGBF1 under non-reducing conditions through direct physical interaction shown by the yeast two-hybrid and pull-down assays. Fluorescence microscopy studies using cyan fluorescent protein (CFP)-fusion protein indicate that GIP1 is exclusively localized in the nucleus. Under non- reducing conditions, GIP1 exhibits predominantly high molecular weight forms, whereas it predominates in low molecular weight monomers under reducing conditions. While reduced GIP1 induced formation of DNA-protein complexes of G-group bZIPs, oxidized GIP1 decreased the amount of those complexes and instead induced its chaperone function suggesting functional switching from redox to chaperone activity. Finally analysis of transgenic plants overexpressing GIP1 revealed that GIP1 is a negative co-regulator in red and blue light mediated hypocotyl elongation. By regulating the repression effect by bZIP16 and the activation effect by bZIP68 and GBF1 on LHCB2.4 expression, GIP1 functions to promote hypocotyl elongation during the early stages of Arabidopsis seedling development.

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Abbreviations

BL:

Blue light

BN:

Blue native

bZIP:

Basic region leucine zipper

CLSM:

Confocal laser scanning microscopy

DTT:

Dithiothreitol

EMSA:

Electrophoretic mobility shift assay

GIP1:

GBF1 interacting protein 1

IOD:

Iodoacetamide

LBD18:

Lateral organ boundaries domain 18

NEM:

N-ethylmaleimide

NLS:

Nuclear localization signal

NPE:

Nuclear protein extracts

ONPG:

O-nitrophenyl β-d-galactopyranoside

RL:

Red light

SDS-PAGE:

Sodium dodecyl sulfate polyacrylamide gel electrophoresis

TPE:

Total protein extraction

2D:

Two-dimensional

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Acknowledgments

I would like to thank Prof. Gunnar Wingsle and Dr. Juande Dios Barajas-Lopez for their critical reading of the manuscript. I thank Dr. Robert J. Ferl for the gift of anti-GIP1 antibody. Dr. Jungmook Kim is gratefully acknowledged for providing seeds of 35S:GIP1 transgenic lines. This work was supported by a grant from the KEMPE foundation.

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The author declares that he has no conflict of interest.

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  1. Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences SLU, 901 83, Umeå, Sweden

    Jehad Shaikhali

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Correspondence to Jehad Shaikhali.

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Figure S1

Homology of ZmGBF1, AtGBF3 and AtGBF1 proteins. A, Amino acid sequence alignment of ZmGBF1, AtGBF3 and AtGBF1 proteins. The asterisks (*) indicates perfectly conserved amino acid residues, (:) indicates general similarities, similarity among 2 to 4 is represented by (.) and dashes (−) indicate gaps introduced to maximize alignment. B, The phylogenetic tree was produced using Phylogeny.fr (http://www.phylogeny.fr/). (PDF 149 kb)

Figure S2

Gene expression of GIP1, bZIP16, bZIP68 and GBF1 genes during development and photomorphogenesis. A, Transcript abundance in the different stages of Arabidopsis development using the developmental tool of Genevestigator (www.genevestigator.com). B, Heat map representing the co-expression patterns of GIP1, bZIP16, bZIP68 and GBF1 genes (in row) during photomorphogenesis such as seed germination after 12 and 24 h and in response to red and blue light (in column). (PDF 84 kb)

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Shaikhali, J. GIP1 protein is a novel cofactor that regulates DNA-binding affinity of redox-regulated members of bZIP transcription factors involved in the early stages of Arabidopsis development. Protoplasma 252, 867–883 (2015). https://doi.org/10.1007/s00709-014-0726-9

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