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Genome-wide identification and phylogenetic analysis of plant RNA binding proteins comprising both RNA recognition motifs and contiguous glycine residues

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Abstract

This study focused on the identification and phylogenetic analysis of glycine-rich RNA binding proteins that contain an RNA recognition motif (RRM)-type RNA binding domain in addition to a region with contiguous glycine residues in representative plant species. In higher plants, glycine-rich proteins with an RRM have met considerable interest as they are responsive to environmental cues and play a role in cold tolerance, pathogen defense, flowering time control, and circadian timekeeping. To identify such RRM containing proteins in plant genomes we developed an RRM profile based on the known glycine-rich RRM containing proteins in the reference plant Arabidopsis thaliana. The application of this remodeled RRM profile that omitted sequences from non-plant species reduced the noise when searching plant genomes for RRM proteins compared to a search performed with the known RRM_1 profile. Furthermore, we developed an island scoring function to identify regions with contiguous glycine residues, using a sliding window approach. This approach tags regions in a protein sequence with a high content of the same amino acid, and repetitive structures score higher. This definition of repetitive structures in a fixed sequence length provided a new glance for characterizing patterns which cannot be easily described as regular expressions. By combining the profile-based domain search for well-conserved regions (the RRM) with a scoring technique for regions with repetitive residues we identified groups of proteins related to the A. thaliana glycine-rich RNA binding proteins in eight plant species.

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Abbreviations

AtRZ:

Arabidopsis thaliana zinc finger-containing glycine-rich RNA binding protein

GRP:

Glycine-rich protein

RBP:

RNA binding protein

RRM:

RNA recognition motif

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Acknowledgments

We thank Dr. Florian Peschke for his contribution to writing of the manuscript and preparing the figures.

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Authors and Affiliations

  1. Molecular Cell Physiology, Faculty of Biology, Bielefeld University, Universitätsstr. 25, 33615, Bielefeld, Germany

    Martin Lewinski & Dorothee Staiger

  2. Bioinformatics/Medical Informatics Department, Universitätsstr. 25, 33615, Bielefeld, Germany

    Martin Lewinski

  3. Department of Cellular and Developmental Biology of Plants, Faculty of Biology, Bielefeld University, Universitätsstr. 25, 33615, Bielefeld, Germany

    Armin Hallmann

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  1. Martin Lewinski
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Correspondence to Dorothee Staiger.

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Funding

This work was supported by the DFG (STA653).

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Martin Lewinski declares that he has no conflict of interest. Armin Hallmann declares that he has no conflict of interest. Dorothee Staiger declares that she has no conflict of interest.

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This article does not contain any studies with animals performed by any of the authors.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

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438_2015_1144_MOESM1_ESM.pdf

Supplementary Fig. 1: Sequence alignment of 38 Arabidopsis thaliana rRRMs. 38 rRRMs of 24 Arabidopsis thaliana RRM proteins that additionally have a glycine rich stretch were aligned and manually trimmed to remove sequence blocks containing gaps prior to generation of the phylogenetic tree. The alignment is depicted using Jalview (Waterhouse et al. 2009). Conserved amino acid residues are highlighted. Information about conservation, quality and consensus is given below the alignment

438_2015_1144_MOESM2_ESM.tif

Supplementary Fig. 2: Phylogenetic tree of the rRRMs. The phylogenetic tree was calculated using the minimal evolution method. rRRMs identified with the calculated HMMER motif were used and 1000 replicates were performed for statistical significance. The obtained tree was further divided into six major branches corresponding to different groups of proteins

438_2015_1144_MOESM3_ESM.tif

Supplementary Fig. 3: Major branch I identified in the phylogenetic analysis. Detailed view of branch I identified in the phylogenetic analysis. This branch contains duplicated rRRMs of AtRNP1 and additional undescribed proteins based on TAIR10

438_2015_1144_MOESM4_ESM.tif

Supplementary Fig. 4: Major branch II identified in the phylogenetic analysis. Detailed view of branch II identified in the phylogenetic analysis. This branch includes duplications of rRRMs of the UBP1-associated proteins (UBAs) i.e.UBA2a, UBA2b and UBA2c

438_2015_1144_MOESM5_ESM.tif

Supplementary Fig. 5: Major branch IIIa identified in the phylogenetic analysis. Detailed view of branch IIIa identified in the phylogenetic analysis. This branch contains rRRMs of AtGRP7, AtGRP8 and AtRZ1a and AtRZ1c

438_2015_1144_MOESM6_ESM.tif

Supplementary Fig. 6: Major branch IIIb identified in the phylogenetic analysis. Detailed view of branch IIIb identified in the phylogenetic analysis. This branch contains the RNA-binding proteins AtGR-RBP2-6

438_2015_1144_MOESM7_ESM.tif

Supplementary Fig. 7: Major branch IIIc identified in the phylogenetic analysis. Detailed view of branch IIIc identified in the phylogenetic analysis. This branch comprises two rRRMs found in chloroplast ribonucleoprotein 29 (CP29)

438_2015_1144_MOESM8_ESM.tif

Supplementary Fig. 8: Major branch IV identified in the phylogenetic analysis. Detailed view of branch IV identified in the phylogenetic analysis. This branch includes only rRRMs of undescribed proteins based on TAIR10

438_2015_1144_MOESM9_ESM.tif

Supplementary Fig. 9: Major branch V identified in the phylogenetic analysis. Detailed view of branch V identified in the phylogenetic analysis. This branch comprises two rRRMs found in RBP45b and c

438_2015_1144_MOESM10_ESM.tif

Supplementary Fig. 10: Major branch VI identified in the phylogenetic analysis. Detailed view of branch VI identified in the phylogenetic analysis. This branch includes only rRRMs of undescribed proteins based on TAIR10

Supplementary Table 1: List of IDs as used in the phylogenetic analysis

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Lewinski, M., Hallmann, A. & Staiger, D. Genome-wide identification and phylogenetic analysis of plant RNA binding proteins comprising both RNA recognition motifs and contiguous glycine residues. Mol Genet Genomics 291, 763–773 (2016). https://doi.org/10.1007/s00438-015-1144-1

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