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Arabidopsis immunophilins ROF1 (AtFKBP62) and ROF2 (AtFKBP65) exhibit tissue specificity, are heat-stress induced, and bind HSP90

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Abstract

The plant co-chaperones FK506-binding proteins (FKBPs) are peptidyl prolyl cis-trans isomerases that function in protein folding, signal transduction and chaperone activity. We report the characterization of the Arabidopsis large FKBPs ROF1 (AtFKBP62) and ROF2 (AtFKBP65) expression and protein accumulation patterns. Transgenic plants expressing ROF1 promoter fused to GUS reporter gene reveal that ROF1 expression is organ specific. High expression was observed in the vascular elements of roots, in hydathodes and trichomes of leaves and in stigma, sepals, and anthers. The tissue specificity and temporal expression of ROF1 and ROF2 show that they are developmentally regulated. Although ROF1 and ROF2 share 85% identity, their expression in response to heat stress is differentially regulated. Both genes are induced in plants exposed to 37 °C, but only ROF2 is a bonafide heat-stress protein, undetected when plants are grown at 22 °C. ROF1/ROF2 proteins accumulate at 37 °C, remain stable for at least 4 h upon recovery at 22 °C, whereas, their mRNA level is reduced after 1 h at 22 °C. By protein interaction assays, it was demonstrated, that ROF1 is a novel partner of HSP90. The five amino acids identified as essential for recognition and interaction between the mammalian chaperones and HSP90 are conserved in the plant ROF1-HSP90. We suggest that ROF/HSP90 complexes assemble in vivo. We propose that specific complexes formation between an HSP90 and ROF isoforms depends on their spatial and temporal expression. Such complexes might be regulated by environmental conditions such as heat stress or internal cues such as different hormones.

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Abbreviations

FKBP:

FK506-binding protein

PPIase:

Peptidyl prolyl cis-trans isomerase

Cyp40:

Cyclophilin 40

CsA:

Cyclosporin A

TPR:

Tripartite tetratricopeptide repeats

HOP:

HSP70 and HSP90 organizing protein

FKBD:

FKBP12-like domain

CaMBD:

Calmodulin binding domain

GUS:

β-Glucoronidase

HSP:

Heat shock protein

PP5:

Protein phosphatase 5

HSF:

Heat shock factor

HSE:

Heat shock element

STRE:

Stress response element

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Acknowledgment

This work was supported by a grant from the Israeli National Academy of Science to A. Breiman; by CONICET–PIP6167 and ANPCyT PICT2003/01–14123 to M. Galigniana; by FEBS short-term fellowship to K. Aviezer-Hagai. We thank Dedi Meiri for his generous contribution and fruitful discussions. We also thank Neomi Dafni for her technical help.

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Authors and Affiliations

  1. Department of Plant Sciences, Tel Aviv University, Tel Aviv, Israel

    Keren Aviezer-Hagai, Julia Skovorodnikova, Odelia Farchi-Pisanty, Erez Maayan, Shmuel Bocovza, Yael Efrat, Nir Ohad & Adina Breiman

  2. Instituto de Investigaciones Bioquimicas, Fundacion Instituto Leloir Buenos Aires, Buenos Aires, Argentina

    Mario Galigniana

  3. Institute of Molecular Bio Sciences, Goethe University, Frankfurt, Germany

    Pascal von Koskull-Döring

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  1. Keren Aviezer-Hagai
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  10. Adina Breiman
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Correspondence to Adina Breiman.

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Aviezer-Hagai, K., Skovorodnikova, J., Galigniana, M. et al. Arabidopsis immunophilins ROF1 (AtFKBP62) and ROF2 (AtFKBP65) exhibit tissue specificity, are heat-stress induced, and bind HSP90. Plant Mol Biol 63, 237–255 (2007). https://doi.org/10.1007/s11103-006-9085-z

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