This is a repository copy of Structural disorder in plant proteins : where plasticity meets sessility. White Rose Research Online URL for this paper: http://eprints.whiterose.ac.uk/152165/ Version: Accepted Version Article: Covarrubias, A.A., Cuevas-Velazquez, C.L., Romero-Pérez, P.S. et al. (2 more authors) (2017) Structural disorder in plant proteins : where plasticity meets sessility. Cellular and Molecular Life Sciences, 74 (17). pp. 3119-3147. ISSN 1420-682X https://doi.org/10.1007/s00018-017-2557-2 This is a post-peer-review, pre-copyedit version of an article published in Cellular and Molecular Life Sciences. The final authenticated version is available online at: http://dx.doi.org/10.1007/s00018-017-2557-2 Reuse Items deposited in White Rose Research Online are protected by copyright, with all rights reserved unless indicated otherwise. They may be downloaded and/or printed for private study, or other acts as permitted by national copyright laws. The publisher or other rights holders may allow further reproduction and re-use of the full text version. This is indicated by the licence information on the White Rose Research Online record for the item. Takedown If you consider content in White Rose Research Online to be in breach of UK law, please notify us by emailing [email protected] including the URL of the record and the reason for the withdrawal request. [email protected] https://eprints.whiterose.ac.uk/ 1 2 3 4 5 STRUCTURAL DISORDER IN PLANT PROTEINS: 6 WHERE PLASTICITY MEETS SESSILITY 7 8 Alejandra A. Covarrubias*, Cesar L. Cuevas-Velazquez, Paulette S. Romero-Pérez 9 David F. Rendón-Luna and Caspar C. Chater 10 11 Departamento de Biología Molecular de Plantas, Instituto de Biotecnología, Universidad 12 Nacional Autónoma de México, 62250 Cuernavaca, México 13 14 15 16 Running title: Protein structural disorder in plants 17 18 19 Key words: intrinsically disordered proteins, plant development, plant metabolism, plant 20 stress responses, plant signalling, LEA proteins, transcription factors. 21 22 23 24 * Corresponding author: E-mail: [email protected]; Tel.: 52-777-329-1643; Fax: 52- 25 777-313-9988; 26 1 1 ABSTRACT 2 Plants are sessile organisms. This intriguing nature provokes the question of how they 3 survive despite the continual perturbations caused by their constantly changing 4 environment. The large amount of knowledge accumulated to date demonstrates the 5 fascinating dynamic and plastic mechanisms, which underpin the diverse strategies 6 selected in plants in response to the fluctuating environment. This phenotypic plasticity 7 requires an efficient integration of external cues to their growth and developmental 8 programs that can only be achieved through the dynamic and interactive coordination of 9 various signalling networks. Given the versatility of intrinsic structural disorder within 10 proteins, this feature appears as one of the leading characters of such complex 11 functional circuits, critical for plant adaptation and survival in their wild habitats. In this 12 review, we present information of those intrinsically disordered proteins (IDPs) from 13 plants for which their high level of predicted structural disorder has been correlated with 14 a particular function, or where there is experimental evidence linking this structural 15 feature with its protein function. Using examples of plant IDPs involved in the control of 16 cell cycle, metabolism, hormonal signalling and regulation of gene expression, 17 development and responses to stress, we demonstrate the critical importance of IDPs 18 throughout the life of the plant. 19 2 1 2 INTRODUCTION 3 Throughout evolution plants have developed an extraordinary ability to overcome 4 fluctuating and drastic environmental changes. Their sessile nature has imposed the 5 selection of particular defense strategies allowing them efficient and effective adjustment 6 or acclimation responses to these conditions, as well as skilled mechanisms to tolerate 7 and survive them. The different endurance strategies selected in these organisms are 8 the result of complex structural and interconnected regulatory networks, which have 9 evolved in an intimate relationship with developmental programs. For instance, in many 10 plant species, the reproductive stage waits for favorable climatic conditions to instrument 11 a crucial set of processes for their perpetuation; root architecture modifies according to 12 the availability of water, phosphorus and other nutrients; and orthodox seeds once 13 desiccated can remain dormant for many years without significant loss in viability until 14 they find sufficient water to germinate [1, 2]. This outstanding resourcefulness suggests 15 mechanisms that make them capable of detecting diverse changes in the plant cell 16 milieu, imposed by the external environment or by developmental programs. 17 Many molecular response mechanisms are efficiently adapted for rapid detection of 18 subtle environmental fluctuations, as can be observed in mechano-sensitivity, ion 19 channels, proton pumps and post-translational protein modifications. The modification of 20 protein structure also seems to be an efficient and effective transducer of a great 21 diversity of signals. This phenomenon is commonly associated with changes in protein 22 conformation produced by phosphorylation or acetylation, or by interactions between 23 proteins or other partners such as nucleic acids or other small molecules acting as 24 substrates, cofactors, allosteric regulators, etc. [3, 4]. However, an adaptation that has 25 received less attention is that related to the intrinsic plasticity found in those proteins that 26 have the ability to present different transient structures depending on the nature of their 27 surroundings. 28 During the last decade we have witnessed significant advances in the identification and 29 characterization of many proteins showing intrinsic structural disorder. This has 30 increased our knowledge of their functional relevance, structural properties and 31 dynamics, as well as mechanisms of action (For review see [5-7]). Intrinsically 3 1 disordered proteins (IDPs) are widely distributed in all domains of life. Although only a 2 few complete proteomes from the different domains are currently available, various 3 bioinformatic studies agree that Eukaryota proteomes show a higher average of 4 disorder, compared to those of Bacteria, which in turn present higher disorder than 5 those of Archea. Interestingly, the predicted disorder in eukaryote proteomes spans a 6 broad range of score values, with both very low and very high disorder [8, 9]. Overall, 7 current information indicates that the level of disorder is higher in eukaryotic organisms 8 than in prokaryotes. Even more important is the observation that protein superfamilies, 9 which have undergone massive diversification during evolution, present more structural 10 disorder than other families. These data also correlate with the expansion of the number 11 of cell types in an organism, revealing a positive relationship between proteome disorder 12 and organism complexity [10, 11]. 13 The accumulated knowledge on IDPs has revealed their functional versatility resulting 14 from their peculiar properties. For example, IDPs can form ensembles with different 15 structural conformations, allowing variability in the exposed surfaces [7, 12-14]. This 16 structural plasticity confers to IDPs the ability to differentially exhibit different post- 17 translational modification sites and/or recognition motifs, depending on specific 18 conditions, to interact transiently, but specifically, with proteins or nucleic acids. With this 19 in mind, it is not surprising the central roles that IDPs play in cellular functions, achieving 20 regulatory and signalling roles as well as acting as scaffold or assembly proteins. 21 In this review, we present a general panorama of the available knowledge on protein 22 disorder in plants. We have put together this information in the context of fundamental 23 biological processes such as development, metabolism and stress responses, which in 24 spite of the limited number of studies unveil the functional relevance of these proteins in 25 the life of plants. The different IDPs referred to in this work are compiled in Tables 1 and 26 2. 27 28 IDPs DISTRIBUTION IN PLANTS 29 In recent years the discovery and characterization of proteins with different amounts of 30 structural disorder has revealed their high representation in plants [15-18]. Large-scale 31 analysis of IDPs and intrinsically disordered regions (IDRs) in Arabidopsis thaliana, a 4 1 widely used experimental model in plant biology, has shown that approximately 30% of 2 its proteome is mostly disordered [10, 16] whereas Zea mays and Glycine max 3 proteomes contain an even higher proportion of disorder (50%) [19]. Interestingly, the 4 chloroplast and mitochondrial proteomes show a significantly lower occurrence of 5 disorder (between 2–19%) when compared to nuclear proteomes of different plant 6 species. The abundance of disorder in these organellar proteomes is comparable to that 7 of Archaea and bacteria, in accordance with the bacterial origin of the genes encoding 8 their proteins [20]. The IDPs encoded in these organellar genomes are mostly involved 9 in translation, transcription or RNA biosynthesis, and some are structural constituents of 10 ribosomes, having in common the ability to form large complexes or to interact with 11 numerous partners, as expected from their intrinsic structural