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ABI5-binding proteins (AFPs) alter transcription of ABA-induced genes via a variety of interactions with chromatin modifiers

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Abstract

Key message

Overexpression of ABI5/ABF binding proteins (AFPs) results in extreme ABA resistance of seeds via multiple mechanisms repressing ABA response, including interactions with histone deacetylases and the co-repressor TOPLESS.

Abstract

Several ABI5/ABF binding proteins (AFPs) inhibit ABA response, resulting in extreme ABA resistance in transgenic Arabidopsis overexpression lines, but their mechanism of action has remained obscure. By analogy to the related Novel Interactor of JAZ (NINJA) protein, it was suggested that the AFPs interact with the co-repressor TOPLESS to inhibit ABA-regulated gene expression. This study shows that the AFPs that inhibit ABA response have intrinsic repressor activity in a heterologous system, which does not depend on the domain involved in the interaction with TOPLESS. This domain is also not essential for repressing ABA response in transgenic plants, but does contribute to stronger ABA resistance. Additional interactions between some AFPs and histone deacetylase subunits were observed in yeast two-hybrid and bimolecular fluorescence assays, consistent with a more direct mechanism of AFP-mediated repression of gene expression. Chemical inhibition of histone deacetylase activity by trichostatin A suppressed AFP effects on a small fraction of the ABI5-regulated genes tested. Collectively, these results suggest that the AFPs participate in multiple mechanisms modulating ABA response, including both TOPLESS-dependent and -independent chromatin modification.

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Abbreviations

ABA:

Abscisic acid

ABI:

ABA-insensitive

AFP:

ABI five binding protein

ABF/AREB:

ABRE binding factor

ABRE:

ABA-responsive element

AD:

GAL4 activation domain

Em6:

Arabidopsis early methionine-labelled 6

BiFC:

Bimolecular fluorescence complementation

BD:

GAL4 binding domain

bZIP:

Basic leucine zipper

EAR domain:

Ethylene-responsive element binding factor-associated amphiphilic repression domain

GM:

Germination media

HDA or HDAC:

Histone deacetylase

Lea:

Late embryogenesis abundant

Min:

Minimal media

MODD:

Mediator of OsbZIP46 deactivation and degradation

NINJA:

Novel Interactor of JAZ

RAB18:

Responsive to ABA 18

SAP18:

Sin3-associated protein 18

TPL/TPR:

Topless and topless-related

TSA:

Trichostatin A

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Acknowledgements

We thank the ABRC team at Ohio State University for efficient distribution of vectors and cDNA clones, Dr. Xinnian Dong for the yeast cell line Y122, Dr. Barry Causier for the TPL and TPR cDNAs, and Adam Protter for assistance in constructing the YFP-AFP3 fusion. This work was supported by UCSB Academic Senate Grant to RRF, Faculty Research Assistance Program funds, and National Science Foundation Grant# IOS1558011 to RRF.

Author contributions

RRF conceived and performed experiments, wrote the manuscript, and repeatedly applied for funding. TJL conceived and performed experiments and provided feedback. BJE and DRM performed experiments and provided feedback.

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  1. Dusty R. Miller

    Present address: Chemistry Department, Vanderbilt University, Nashville, TN, 37235, USA

Authors and Affiliations

  1. Molecular, Cellular, and Developmental Biology Department, University of California at Santa Barbara, Santa Barbara, CA, 93106, USA

    Tim J. Lynch & Ruth R. Finkelstein

  2. Biomolecular Science and Engineering Program, University of California at Santa Barbara, Santa Barbara, CA, 93106, USA

    B. Joy Erickson & Dusty R. Miller

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  1. Tim J. Lynch
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Correspondence to Ruth R. Finkelstein.

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Lynch, T.J., Erickson, B.J., Miller, D.R. et al. ABI5-binding proteins (AFPs) alter transcription of ABA-induced genes via a variety of interactions with chromatin modifiers. Plant Mol Biol 93, 403–418 (2017). https://doi.org/10.1007/s11103-016-0569-1

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