Correlations between predicted protein disorder and post-translational modifications in plants

Atsushi Kurotani,Kazuo Shinozaki,Yutaka Kuroda,Alexander A Tokmakov,Tetsuya Sakurai,Yasuo Fukami

doi:10.1093/bioinformatics/btt762

Abstract

Motivation: Protein structural research in plants lags behind that in animal and bacterial species. This lag concerns both the structural analysis of individual proteins and the proteome-wide characterization of structure-related properties. Until now, no systematic study concerning the relationships between protein disorder and multiple post-translational modifications (PTMs) in plants has been presented.Results: In this work, we calculated the global degree of intrinsic disorder in the complete proteomes of eight typical monocotyledonous and dicotyledonous plant species. We further predicted multiple sites for phosphorylation, glycosylation, acetylation and methylation and examined the correlations of protein disorder with the presence of the predicted PTM sites. It was found that phosphorylation, acetylation and O-glycosylation displayed a clear preference for occurrence in disordered regions of plant proteins. In contrast, methylation tended to avoid disordered sequence, whereas N-glycosylation did not show a universal structural preference in monocotyledonous and dicotyledonous plants. In addition, the analysis performed revealed significant differences between the integral characteristics of monocot and dicot proteomes. They included elevated disorder degree, increased rate of O-glycosylation and R-methylation, decreased rate of N-glycosylation, K-acetylation and K-methylation in monocotyledonous plant species, as compared with dicotyledonous species. Altogether, our study provides the most compelling evidence so far for the connection between protein disorder and multiple PTMs in plants.Contact: tokmak@phoenix.kobe-u.ac.jp or tetsuya.sakurai@riken.jpSupplementary information: Supplementary data are available at Bioinformatics online.

Highlights

Proteins with long disordered regions, often referred to as intrinsically disordered regions (IDRs), have been extensively investigated over the past several years
The proteins with IDRs are widespread in plant proteomes with the overall proteome disorder content in different plant species being typical for other eukaryotes (Dunker et al, 2001; Fukuchi et al, 2011; Xue et al, 2012)
We have found that this modification displayed a negative correlation with protein disorder in the analyzed plant species, suggesting that it has a preference for occurrence in ordered regions (Fig. 4D and Supplementary Figures S6B and S7B)

Summary

Introduction

Proteins with long disordered regions, often referred to as intrinsically disordered regions (IDRs), have been extensively investigated over the past several years They represent a broad class of proteins found more abundantly in eukaryotes than in bacteria or archaea (Dunker et al, 2001). The proteins with IDRs are widespread in plant proteomes with the overall proteome disorder content in different plant species being typical for other eukaryotes (Dunker et al, 2001; Fukuchi et al, 2011; Xue et al, 2012). These proteins fulfill important cellular functions in plants, often serving as the integrators of multiple regulatory and environmental signals (Sun et al, 2013). It has been estimated that 82–94% of all transcription factors, including those from Arabidopsis thaliana, contain extended IDRs (Liu et al, 2006) and 470% of signaling proteins have long disordered regions (Iakoucheva et al, 2002)

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Results

Conclusion