Abstract
Intrinsic protein disorder is an interesting structural feature where fully functional proteins lack a three-dimensional structure in solution. In this work, we estimated the relative content of intrinsic protein disorder in 96 plant proteomes including monocots and eudicots. In this analysis, we found variation in the relative abundance of intrinsic protein disorder among these major clades; the relative level of disorder is higher in monocots than eudicots. In turn, there is an inverse relationship between the degree of intrinsic protein disorder and protein length, with smaller proteins being more disordered. The relative abundance of amino acids depends on intrinsic disorder and also varies among clades. Within the nucleus, intrinsically disordered proteins are more abundant than ordered proteins. Intrinsically disordered proteins are specialized in regulatory functions, nucleic acid binding, RNA processing, and in response to environmental stimuli. The implications of this on plants’ responses to their environment are discussed.
Similar content being viewed by others
References
Afanasyeva A, Bockwoldt M, Cooney CR, Heiland I, Gossmann TI (2018) Human long intrinsically disordered protein regions are frequent targets of positive selection. Genome Res 28(7):975–998. https://doi.org/10.1101/gr.232645.117
Alvarez-Ponce D, Ruiz-González MX, Vera-Sirera F, Feyertag F, Perez-Amador M, Fares M (2018) Arabidopsis heat stress-induced proteins are enriched in electrostatically charged amino acids and intrinsically disordered regions. Int J Mol Sci 19(8):2276. https://doi.org/10.3390/ijms19082276
Bhowmick A, Brookes DH, Yost SR, Dyson HJ, Forman-Kay JD, Gunter D, Head-Gordon M, Hura GL, Pande VS, Wemmer DE, Wright PE, Head-Gordon T (2016) Finding our way in the dark proteome. J Am Chem Soc 138:9730–9742. https://doi.org/10.1021/jacs.6b06543
Brown CJ, Takayama S, Campen AM, Vise P, Marshall TW, Oldfield CJ, Williams CJ, Keith Dunker A (2002) Evolutionary rate heterogeneity in proteins with long disordered regions. J Mol Evol 55(1):104–110. https://doi.org/10.1007/s00239-001-2309-6
Carugo O (2008) Amino acid composition and protein dimension. Protein Sci 17:2187–2191. https://doi.org/10.1110/ps.037762.108
Choura M, Ebel C, Hanin M (2019) Genomic analysis of intrinsically disordered proteins in cereals: from mining to meaning. Gene:143984. https://doi.org/10.1016/j.gene.2019.143984
Covarrubias AA, Cuevas-Velazquez CL, Romero-Pérez PS, Rendón-Luna DF, Chater CCC (2017) Structural disorder in plant proteins: where plasticity meets sessility. Cell Mol Life Sci 74:3119–3147. https://doi.org/10.1007/s00018-017-2557-2
Dai J, Liu H, Zhou J, Huang K (2016) Selenoprotein R protects human lens epithelial cells against D-galactose-induced apoptosis by regulating oxidative stress and endoplasmic reticulum stress. Int J Mol Sci 17(2):231–250. https://doi.org/10.3390/ijms17020231
Deiana A, Forcelloni S, Porrello A, Giansanti A (2019) Intrinsically disordered proteins and structured proteins with intrinsically disordered regions have different functional roles in the cell. PLoS One 14(8):e0217889. https://doi.org/10.1371/journal.pone.0217889
Dosztányi Z (2018) Prediction of protein disorder based on IUPred. Protein Sci 27:331–340. https://doi.org/10.1002/pro.3334
Dunker AK, Silman I, Uversky VN, Sussman JL (2008) Function and structure of inherently disordered proteins. Curr Opin Struct Biol 18(6):756–764. https://doi.org/10.1016/j.sbi.2008.10.002
Forcelloni S, Giansanti A (2020) Evolutionary forces and codon bias in different flavors of intrinsic disorder in the human proteome. J Mol Evol 88(2):164–178. https://doi.org/10.1007/s00239-019-09921-4
Frege T, Uversky VN (2015) Intrinsically disordered proteins in the nucleus of human cells. Biochem Biophys Reports 1:33–51. https://doi.org/10.1016/j.bbrep.2015.03.003
Ge S, Jung D, Yao R (2020) ShinyGO: a graphical enrichment tool for animals and plants. Bioinformatics 36(8):2628–2629. https://doi.org/10.1093/bioinformatics/btz931
Ginestet C (2011) ggplot2: elegant graphics for data analysis. J R Stat Soc Ser A (Statistics Soc) 174(1):245–246. https://doi.org/10.1111/j.1467-985x.2010.00676_9.x
Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40(1):D1178–DD118. https://doi.org/10.1093/nar/gkr944
Howe KL, Contreras-Moreira B, De Silva N, Maslen G, Akanni W, Allen J, Alvarez-Jarreta J, Barba M, Bolser DM, Cambell L, Carbajo M, Chakiachvili M, Christensen M, Cummins C, Cuzick A, Davis P, Fexova S, Gall A, George N, Gil L, Gupta P, Hammond-Kosack KE, Haskell E, Hunt SE, Jaiswal P, Janacek SH, Kersey PJ, Langridge N, Maheswari U, Maurel T, McDowall MD, Moore B, Muffato M, Naamati G, Naithani S, Olson A, Papatheodorou I, Patricio M, Paulini M, Pedro H, Perry E, Preece J, Rosello M, Russell M, Sitnik V, Staines DM, Stein J, Tello-Ruiz MK, Trevanion SJ, Urban M, Wei S, Ware D, Williams G, Yates AD, Flicek P (2020) Ensembl Genomes 2020-enabling non-vertebrate genomic research. Nucleic Acids Res 48(D1):D689–D695. https://doi.org/10.1093/nar/gkz890
Howell MH, Green R, Killeen A, Wedderburn L, Picascio V, Rabionet A, Peng Z, Larina MV, Xue B, Kurgan LA, Uversky VN (2012) Not that rigid midgets and not so flexible giants: on the abundance and roles of intrinsic disorder in short and long proteins. J Biol Syst 20(4):471–511. https://doi.org/10.1142/S0218339012400086
Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong SY, Lopez R, Hunter S (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30(9):1236–1240. https://doi.org/10.1093/bioinformatics/btu031
Kovacs D, Agoston B, Tompa P (2008) Disordered plant LEA proteins as molecular chaperones. Plant Signal Behav 3:710–713. https://doi.org/10.4161/psb.3.9.6434
Kurotani A, Tokmakov AA, Kuroda Y, Fukami Y, Shinozaki K, Sakurai T (2014) Correlations between predicted protein disorder and post-translational modifications. Bioinformatics 30:1095–1103. https://doi.org/10.1093/bioinformatics/btt762
Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. Journal of statistical software 25(1):1–18. https://doi.org/10.18637/jss.v025.i01
Letunic I, Bork P (2019) Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 47(W1):W256–W259. https://doi.org/10.1093/nar/gkz239
Lin YS, Hsu WL, Hwang JK, Li WH (2007) Proportion of solvent-exposed amino acids in a protein and rate of protein evolution. Mol Biol Evol 24(4):1005–1011. https://doi.org/10.1093/molbev/msm019
Ling Z, Brockmöller T, Baldwin IT, Xu S (2019) Evolution of alternative splicing in eudicots. Front Plant Sci 10. https://doi.org/10.3389/fpls.2019.00707
Lipman DJ, Souvorov A, Koonin EV, Panchenko AR, Tatusova TA (2002) The relationship of protein conservation and sequence length. BMC Evol Biol 2:20. https://doi.org/10.1186/1471-2148-2-20
Liu J, Perumal NB, Oldfield CJ, Su EW, Uversky VN, Dunker AK (2006) Intrinsic disorder in transcription factors. Biochemistry 45(22):6873–6888. https://doi.org/10.1021/bi0602718
Liu Y, Wu J, Sun N, Tu C, Shi X, Cheng H, Liu S, Li S, Wang Y, Zheng Y, Uversky VN (2017) Intrinsically disordered proteins as important players during desiccation stress of soybean radicles. J Proteome Res 16:2393–2409. https://doi.org/10.1021/acs.jproteome.6b01045
Mastrangelo AM, Marone D, Laidò G, De Leonardis AM, De Vita P (2012) Alternative splicing: enhancing ability to cope with stress via transcriptome plasticity. Plant Sci 185-186:40–49. https://doi.org/10.1016/j.plantsci.2011.09.006
Mészáros B, Simon I, Dosztányi Z (2009) Prediction of protein binding regions in disordered proteins. PLoS Comput Biol 5(5):e1000376. https://doi.org/10.1371/journal.pcbi.1000376
Moore JP, Vicré-Gibouin M, Farrant JM, Driouich A (2008) Adaptations of higher plant cell walls to water loss: drought vs desiccation. Physiol Plant 124:336–342. https://doi.org/10.1111/j.1399-3054.2008.01134.x
Mukherjee S, Panda A, Ghosh TC (2015) Elucidating evolutionary features and functional implications of orphan genes in Leishmania major. Infect Genet Evol 32:330–337. https://doi.org/10.1016/j.meegid.2015.03.031
Pancsa R, Tompa P (2012) Structural disorder in eukaryotes. PLoS One 7(4):e3468–e34687. https://doi.org/10.1371/journal.pone.0034687
Pazos F, Pietrosemoli N, García-Martín JA, Solano R (2013) Protein intrinsic disorder in plants. Front Plant Sci 4. https://doi.org/10.3389/fpls.2013.00363
Peng K, Radivojac P, Vucetic S, Dunker AK, Obradovic Z (2006) Length-dependent prediction of protein in intrinsic disorder. BMC Bioinformatics 7:208. https://doi.org/10.1186/1471-2105-7-208
Peng Z, Yan J, Fan X, Mizianty MJ, Xue B, Wang K, Hu G, Uversky VN, Kurgan L (2014) Exceptionally abundant exceptions: comprehensive characterization of intrinsic disorder in all domains of life. Cell Mol Life Sci 72:137–151. https://doi.org/10.1007/s00018-014-1661-9
Pietrosemoli N, García-Martín JA, Solano R, Pazos F (2013) Genome-wide analysis of protein disorder in Arabidopsis thaliana: implications for plant environmental adaptation. PLoS One 8(2):e55524. https://doi.org/10.1371/journal.pone.0055524
R Development Core Team (2016) R: a language and environment for statistical computing. R Found Stat Comput. https://doi.org/10.1007/978-3-540-74686-7
Radivojac P (2003) Protein flexibility and intrinsic disorder. Protein Sci 13(1):71–80. https://doi.org/10.1110/ps.03128904
Rancurel C, Khosravi M, Dunker AK, Romero PR, Karlin D (2009) Overlapping genes produce proteins with unusual sequence properties and offer insight into de novo protein creation. J Virol 83:10719–10736. https://doi.org/10.1128/JVI.00595-09
Romero P, Obradovic Z, Li X, Garner EC, Brown CJ, Dunker AK (2001) Sequence complexity of disordered protein. Proteins Struct Funct Genet 42(1):38–48. https://doi.org/10.1002/1097-0134(20010101)42:1<38::AID-PROT50>3.0.CO;2-3
Schad E, Tompa P, Hegyi H (2011) The relationship between proteome size, structural disorder and organism complexity. Genome Biol 12(12):R120. https://doi.org/10.1186/gb-2011-12-12-r120
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12(6):1–18. https://doi.org/10.1186/gb-2011-12-6-r60
Skupien-Rabian B, Jankowska U, Swiderska B, Lukasiewicz S, Ryszawy D, Dziedzicka-Wasylewska M, Kedracka-Krok S (2015) Proteomic and bioinformatic analysis of a nuclear intrinsically disordered proteome. J Proteome 130:76–84. https://doi.org/10.1016/j.jprot.2015.09.004
Sun X, Rikkerink EHA, Jones WT, Uversky VN (2013) Multifarious roles of intrinsic disorder in proteins illustrate its broad impact on plant biology. Plant Cell 25(1):38–55. https://doi.org/10.1105/tpc.112.106062
Tompa P, Csermely P (2004) The role of structural disorder in the function of RNA and protein chaperones. ASEB J 18(11):1169–1175. https://doi.org/10.1096/fj.04-1584rev
Uversky VN (2011) Intrinsically disordered proteins from A to Z. Int J Biochem Cell Biol 43(8):1090–1103. https://doi.org/10.1016/j.biocel.2011.04.001
Uversky VN, Gillespie JR, Fink AL (2000) Why are “natively unfolded” proteins unstructured under physiologic conditions? Proteins Struct Funct Genet 41(3):415–427. https://doi.org/10.1002/1097-0134(20001115)41:3<415::AID-PROT130>3.0.CO;2-7
Vincent M, Schnell S (2016) A collection of intrinsic disorder characterizations from eukaryotic proteomes. Sci Data 3:160045. https://doi.org/10.1038/sdata.2016.45
Walsh I, Martin AJM, Di Domenico T, Tosatto SCE (2012) Espritz: accurate and fast prediction of protein disorder. Bioinformatics 28(4):503–509. https://doi.org/10.1093/bioinformatics/btr682
Ward JJ, Sodhi JS, McGuffin LJ, Buxton BF, Jones DT (2004) Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J Mol Biol 337(3):635–645. https://doi.org/10.1016/j.jmb.2004.02.002
Wilson B, Foy S, Neme R, Masel J (2017) Young genes are highly disordered as predicted by the preadaptation hypothesis of de novo gene birth. Nat Ecol Evol 1:0146. https://doi.org/10.1038/s41559-017-0146
Wright PE, Dyson HJ (2015) Intrinsically disordered proteins in cellular signalling and regulation. Nat Rev Mol Cell Biol 16(1):18–29. https://doi.org/10.1038/nrm3920
Xue B, Williams RW, Oldfield CJ, Dunker K, Uversky VN (2010) Archaic chaos : intrinsically disordered proteins in Archaea. BMC Syst Biol 4:S1. https://doi.org/10.1186/1752-0509-4-S1-S1
Xue B, Dunker AK, Uversky VN (2012) Orderly order in protein intrinsic disorder distribution: disorder in 3500 proteomes from viruses and the three domains of life. J Biomol Struct Dyn 30:137–149. https://doi.org/10.1080/07391102.2012.675145
Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang Jing Li S, Li R, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 3:W293–W297. https://doi.org/10.1093/nar/gkl031
Yruela I, Contreras-Moreira B (2012) Protein disorder in plants: a view from the chloroplast. BMC Plant Biol 12(1):165. https://doi.org/10.1186/1471-2229-12-165
Yruela I, Contreras-Moreira B (2013) Genetic recombination is associated with intrinsic disorder in plant proteomes. BMC Genom:14. https://doi.org/10.1186/1471-2164-14-772
Yruela I, Oldfield CJ, Niklas KJ, Dunker AK (2017) Evidence for a strong correlation between transcription factor protein disorder and organismic complexity. Genome Biol Evol 9:1248–1265. https://doi.org/10.1093/gbe/evx073
Zamora-Briseño JA, Reyes-Hernández SJ, Zapata LCR (2018) Does water stress promote the proteome-wide adjustment of intrinsically disordered proteins in plants? Cell Stress Chaperones 23(5):807–812. https://doi.org/10.1007/s12192-018-0918-x
Zamora-Briseño JA, Pereira-Santana A, Reyes-Hernández SJ, Castaño E, Rodríguez-Zapata LC (2019) Global dynamics in protein disorder during maize seed development. Genes (Basel) 10(7):pii: E502. https://doi.org/10.3390/genes10070502
Zhang Y, Launay H, Schramm A, Lebrun R, Gontero B (2018) Exploring intrisincally disordered proteins in Chlamydomonas reinhardtii. Sci Rep 8(1):6805. https://doi.org/10.1038/s41598-018-24772-7
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Zamora-Briseño, J.A., Pereira-Santana, A., Reyes-Hernández, S.J. et al. Towards an understanding of the role of intrinsic protein disorder on plant adaptation to environmental challenges. Cell Stress and Chaperones 26, 141–150 (2021). https://doi.org/10.1007/s12192-020-01162-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12192-020-01162-5