Differential Evolution of α-Glucan Water Dikinase (GWD) in Plants
Abstract
:1. Introduction
2. Materials and Methods
2.1. Sequence Curation and Multiple Sequence Alignment
2.2. Comparative Analysis of GWD Protein Primary Structure
2.3. Prediction of Signal Sequence, Motif Scanning and Analysis of Domains
2.4. Amino acid Substitution Prediction
3. Results
3.1. Sequence Comparison and Developmental Pattern
3.2. Assessment of Physio–Chemical Properties of GWD Protein Sequences
3.3. Prediction of Transit Peptide, Motif and Analysis of Functional Domain
3.4. Carbohydrate Binding Module (CBM45) Tandem Domains
3.5. Analysis of Amino Acid Mutation
4. Discussion
5. Conclusions
6. Declaration of Competing Interest
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Hejazi, M.; Steup, M.; Fettke, J. The plastidial glucan, water dikinase (GWD) catalyses multiple phosphotransfer reactions. FEBS J. 2012, 279, 1953–1966. [Google Scholar] [CrossRef]
- Mdodana, N.T.; Jewell, J.F.; Phiri, E.E.; Smith, M.L.; Oberlander, K.; Mahmoodi, S.; Kossmann, J.; Lloyd, J.R. Mutations in glucan, water dikinase affect starch degradation and gametophore development in the moss Physcomitrella patens. Sci. Rep. 2019, 9, 1–13. [Google Scholar] [CrossRef] [Green Version]
- Mikkelsen, R.; Suszkiewicz, K.; Blennow, A.A. A novel type carbohydrate-binding module identified in r-glucan water dikinases is specific for regulated plastidial starch metabolism. Biochem. J. 2006, 45, 4674–4682. [Google Scholar] [CrossRef]
- Ritte, G.; Lloyd, J.R.; Eckermann, N.; Rottmann, A.; Kossmann, J.; Steup, M. The starch-related R1 protein is an α-glucan, water dikinase. Proc. Natl. Acad. Sci. USA 2002, 99, 7166–7171. [Google Scholar] [CrossRef] [Green Version]
- Baunsgaard, L.; Lutken, H.; Mikkelsen, R.; Glaring, M.A.; Pham, T.T.; Blennow, A. A novel isoform of glucan, water dikinase phosphorylates pre-phosphorylated α-glucans and is involved in starch degradation in Arabidopsis. Plant J. 2005, 41, 595–605. [Google Scholar] [CrossRef]
- Kötting, O.; Pusch, K.; Tiessen, A.; Geigenberger, P.; Steup, M.; Ritte, G. Identification of a novel enzyme required for starch metabolism in Arabidopsis leaves. The phosphoglucan, water dikinase. Plant Physiol. 2005, 137, 242–252. [Google Scholar] [CrossRef] [Green Version]
- Ritte, G.; Heydenreich, M.; Mahlow, S.; Haebel, S.; Kotting, O.; Steup, M. Phosphorylation of C6- and C3-positions of glucosyl residues in starch is catalysed by distinct dikinases. FEBS Lett. 2006, 580, 4872–4876. [Google Scholar] [CrossRef] [Green Version]
- Pirone, C.; Gurrieri, L.; Gaiba, I.; Adamiano, A.; Valle, F.; Trost, P.; Sparla, F. The analysis of the different functions of starch-phosphorylating enzymes during the development of Arabidopsis thaliana plants discloses an unexpected role for the cytosolic isoform GWD2. Physiol. Plant 2017, 160, 447–457. [Google Scholar] [CrossRef]
- Mikkelsen, R.; Blennow, A. Functional domain organization of the potato R- glucan, water dikinase (GWD): Evidence for separate site catalysis as revealed by limited proteolysis and deletion mutants. Biochem. J. 2005, 385, 355–361. [Google Scholar] [CrossRef] [Green Version]
- Blennow, A.; Engelsen, S.B.; Munck, L.; Møller, B.L. Starch molecular structure and phosphorylation investigated by a combined chromatographic and chemometric approach. Carbohydr. Polym. 1999, 41, 163–174. [Google Scholar] [CrossRef]
- Xu, X.; Huang, X.F.; Visser, R.G.F.; Trindade, L.M. Engineering potato starch with a higher phosphate content. PLoS ONE 2017, 12, e0169610. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, W.; Hostettler, C.; Damberger, F.F.; Kossmann, J.; Lloyd, J.R.; Zeeman, S.C. Modification of Cassava root starch phosphorylation enhances starch functional properties. Front. Plant Sci. 2018, 9, 1562. [Google Scholar] [CrossRef] [PubMed]
- Schwall, G.P.; Safford, R.; Westcott, R.J.; Jeffcoat, R.; Tayal, A.; Shi, Y.C.; Jobling, S.A. Production of very-high-amylose potato starch by inhibition of SBE A and B. Nat. Biotechnol. 2000, 18, 551–554. [Google Scholar] [CrossRef] [PubMed]
- Tyzack, J.D.; Furnham, N.; Sillitoe, I.; Orengo, C.M.; Thornton, J.M. Understanding enzyme function evolution from a computational perspective. Curr. Opin. Struct. Biol. 2017, 47, 131–139. [Google Scholar] [CrossRef]
- Thalman, M.; Santelia, D. Starch as a determinant of plant fitness under abiotic stress. New Phytol. 2017, 214, 943–951. [Google Scholar] [CrossRef] [Green Version]
- Furnham, N.; Dawson, N.L.; Rahman, S.A.; Thornton, J.M.; Orengo, C.A. Large-scale analysis exploring evolution of catalytic machineries and mechanisms in enzyme superfamilies. J. Mol. Biol. 2016, 428, 253–267. [Google Scholar] [CrossRef] [Green Version]
- Nobeli, I.; Favia, A.D.; Thornton, J.M. Protein promiscuity and its implications for biotechnology. Nat. Biotechnol. 2009, 27, 157–167. [Google Scholar] [CrossRef]
- László, P. Chapter 5: Evolution of orthologous proteins. In Evolution of Protein, 2nd ed.; Wiley-Blackwell: Malden, MA, USA, 2007; pp. 91–104. [Google Scholar]
- Bekaert, M.; Edger, P.P.; Pires, J.C.; Conant, G.C. Two-phase resolution of polyploidy in the Arabidopsis metabolic network gives rise to relative and absolute dosage constraints. Plant Cell 2011, 23, 1719–1728. [Google Scholar] [CrossRef] [Green Version]
- Kong, Y.; Zhou, G.; Avci, U.; Gu, X.; Jones, C.; Yin, Y.; Xu, Y.; Hahn, M.G. Two poplar glycosyltransferase genes, PdGATL1.1 and PdGATL1.2 are functional orthologs to PARVUS / AtGATL1 in Arabidopsis. Mol. Plant 2009, 2, 1040–1050. [Google Scholar] [CrossRef] [Green Version]
- Aklilu, B.B.; Culligan, K.M. Molecular evolution and functional diversification of replication protein A1 in plants. Front. Plant Sci. 2016, 7, 33. [Google Scholar] [CrossRef] [Green Version]
- Zou, C.; Lehti-Shiu, M.D.; Thibaud-Nissen, F.; Prakash, T.; Buell, C.R.; Shiu, S.H. Evolutionary and expression signatures of pseudogenes in Arabidopsis and rice. Plant Physiol. 2009, 151, 3–15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brockington, S.F.; Yang, Y.; Gandia-Herrero, F.; Covshoff, S.; Hibberd, J.M.; Sage, R.F.; Wong, G.K.; Moore, M.J.; Smith, S.A. Lineage-specific gene radiations underlie the evolution of novel betalain pigmentation in Caryophyllales. New Phytol. 2015, 207, 1170–1180. [Google Scholar] [CrossRef]
- Hu, Y.; Liang, W.; Yin, C.; Yang, X.; Ping, B.; Li, A.; Jia, R.; Chen, M.; Luo, Z.; Cai, Q.; et al. Interactions of OsMADS1 with floral homeotic genes in rice flower development. Mol. Plant 2015, 8, 1366–1384. [Google Scholar] [CrossRef] [PubMed]
- Zhang, S.; Zhang, J.S.; Zhao, J.; He, C. Distinct subfunctionalization and neofunctionalization of the B-class MADS-box genes in Physalis floridana. Planta 2015, 241, 387–402. [Google Scholar] [CrossRef]
- Hansen, B.O.; Vaid, N.; Musialak-Lange, M.; Janowski, M.; Mutwil, M. Elucidating gene function and function evolution through comparison of co-expression networks of plants. Front. Plant Sci. 2014, 5, 394. [Google Scholar] [CrossRef] [Green Version]
- Waterhouse, A.M.; Procter, J.B.; Martin, D.M.A.; Clamp, M.; Barton, G.J. Jalview version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009, 25, 1189–1191. [Google Scholar] [CrossRef] [Green Version]
- Lemoine, F.; Correia, D.; Lefort, V.; Doppelt-Azeroual, O.; Mareuil, F.; Cohen-Boulakia, S.; Gascuel, O. NGPhylogeny.fr: New generation phylogenetic services for non-specialists. Nucleic Acids Res. 2019, 47, W260–W265. [Google Scholar] [CrossRef] [Green Version]
- Katoh, K.; Standley, D.M. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in performance and usability. Mol. Biol. Evol. 2013, 30, 772–780. [Google Scholar] [CrossRef] [Green Version]
- Criscuolo, A.; Gribaldo, S. BMGE (Block Mapping and Gathering with Entropy): A new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol. Biol. 2010, 10, 210. [Google Scholar] [CrossRef] [Green Version]
- Guindon, S.; Dufayard, J.F.; Lefort, V.; Anisimova, M.; Hordijk, W.; Gascuel, O. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst. Biol. 2010, 59, 307–321. [Google Scholar] [CrossRef] [Green Version]
- Lefort, V.; Longueville, J.-E.; Gascuel, O. SMS: Smart Model Selection in PhyML. Mol. Biol. Evol. 2017, 34, 2422–2424. [Google Scholar] [CrossRef] [Green Version]
- Anisimova, M.; Liberles, D.A.; Philippe, H.; Provan, J.; Pupko, T.; von Haeseler, A. State-of the art methodologies dictate new standards for phylogenetic analysis. BMC Evol. Biol. 2013, 13, 161. [Google Scholar] [CrossRef] [Green Version]
- Letunic, I.; Bork, P. Interactive Tree Of Life (iTOL) v4: Recent updates and new developments. Nucleic Acids Res. 2019, 47, W256–W259. Available online: https://www.itol.embl.de/ (accessed on 16 May 2020). [CrossRef] [Green Version]
- Gasteiger, E.; Hoogland, C.; Gattiker, A.; Duvaud, S.; Wilkins, M.R.; Appel, R.D.; Bairoch, A. Protein identification and analysis tools on the ExPASy server. In The Proteomics Protocol Handbook; Walker, J.M., Ed.; Humana press: Totowa, NJ, USA, 2005; pp. 571–607. Available online: https://www.expasy.org/protparam/ (accessed on 10 May 2020).
- Morenikeji, O.B.; Thomas, B.N. In silico analyses of CD14 molecule reveal significant evolutionary diversity, potentially associated with speciation and variable immune response in mammals. PeerJ 2019, 7, e7325. [Google Scholar] [CrossRef]
- Ferre, F.; Clote, P. DiANNA: A web server for disulfide connectivity prediction. Nucleic Acids Res. 2005, 33, W230–W232. [Google Scholar] [CrossRef] [Green Version]
- Ferre, F.; Clote, P. DiANNA 1.1: An extension of the DiANNA web server for ternary cysteine classification. Nucleic Acids Res. 2006, 34, W182–W185. [Google Scholar] [CrossRef] [Green Version]
- Mikkelsen, R.; Mutenda, K.E.; Mant, A.; Schurmann, P.; Blennow, A. Alpha-glucan water dikinase (GWD): A plastidic enzyme with redox-regulated and coordinated catalytic activity and binding affinity. Proc. Natl. Acad. Sci. USA 2005, 102, 1785–1790. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Armenteros, J.J.A.; Salvatore, M.; Emanuelsson, O.; Winther, O.; von Heijne, G.; Elofsson, A.; Nielsen, H. Detecting sequence signals in targeting peptides using deep learning. Life Sci. Alliance 2019, 2, e201900429. [Google Scholar] [CrossRef] [Green Version]
- Blum, T.; Briesemeister, S.; Kohlbacher, O. MultiLoc2: Integrating phlogeny and Gene ontology terms improves subcellular localization prediction. BMC Bioinform. 2009, 10, 274. [Google Scholar] [CrossRef] [Green Version]
- Choi, Y.; Chan, A.P. PROVEAN web server: A tool to predict the functional effect of amino acid substitutions and indels. Bioinformatics 2015, 31, 2745–2747. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lombard, V.; Golaconda, R.H.; Drula, E.; Coutinho, P.M.; Henrissat, B. The carbohydrate-active enzymes database (CAZy). Nucleic Acids Res. 2013, 42, D490–D495. Available online: http://www.cazy.org/ (accessed on 10 May 2020). [CrossRef] [PubMed] [Green Version]
- Glaring, M.A.; Baumann, M.J.; Hachem, M.A.; Nakai, H.; Nakai, N.; Santelia, D.; Svensson, B. Starch-binding domains in the CBM45 family—low-affinity domains from glucan, water dikinase and a-amylase involved in plastidial starch metabolism. FEBS J. 2011, 278, 1175–1185. [Google Scholar] [CrossRef] [PubMed]
- Zhou, W.; He, S.; Naconsie, M.; Ma, Q.; Zeeman, S.C.; Gruissem, W.; Zhnag, P. Alpha-Glucan, Water Dikinase 1 affects starch metabolism and storage root growth in cassava (Manihot esculenta Crantz). Sci. Rep. 2017, 7, 1–17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tatusov, R.L.; Koonin, E.V.; Lipman, D.J. A genome perspective on protein families. Science 1997, 278, 631–637. [Google Scholar] [CrossRef] [Green Version]
- Dumez, S.; Wattebled, F.; Dauvillee, D.; Delvalle, D.; Planchot, V.; Ball, S.G.; D’Hulst, C. Mutants of Arabidopsis lacking starch branching enzyme II substitute plastidial starch synthesis by cytoplasmic maltose accumulation. Plant Cell 2006, 18, 2694–2709. [Google Scholar] [CrossRef] [Green Version]
- Wu, P.Z.; Zhou, C.P.; Cheng, S.F.; Wu, Z.Y.; Lu, W.J.; Han, J.; Chen, Y.; Chen, Y.; Ni, P.; Wang, Y.; et al. Integrated genome sequence and linkage map of physic nut (Jatropha curcas L.), a biodiesel plant. Plant J. 2015, 81, 810–821. [Google Scholar] [CrossRef]
- Qin, S.; Tang, Y.; Chen, Y.; Wu, P.; Li, M.; Wu, G.; Jiang, H. Overexpression of the starch phosphorylase-Like gene (PHO3) in Lotus japonicus has a profound effect on the growth of plants and reduction of transitory starch accumulation. Front. Plant Sci. 2016, 7, 1315. [Google Scholar] [CrossRef]
- Ritte, G.; Lorberth, R.; Steup, M. Reversible binding of the starch-related R1 protein to the surface of transitory starch. Plant J. 2000, 21, 387–391. [Google Scholar] [CrossRef] [Green Version]
- Idicula-Thomas, S.; Petety, V.B. Understanding the relationship between the primary structure of proteins and its propensity to be soluble on overexpression in Escherichia coli. Protein Eng. Des. Sel. 2005, 18, 175–180. [Google Scholar] [CrossRef] [Green Version]
- Klesmith, J.R.; Bacik, J.; Wrenbeck, E.E.; Michalczyk, R.; Whitehead, T.A. Trade-offs between enzyme fitness and solubility illuminated by deep mutational scanning. Proc. Natl. Acad. Sci. USA 2017, 114, 2265–2270. [Google Scholar] [CrossRef] [Green Version]
- Bruce, B.D. Chloroplast transit peptides: Structure, function and evolution. Trends Cell Biol. 2000, 10, 440–447. [Google Scholar] [CrossRef]
- Bruce, B.D. The paradox of plastid transit peptides: Conservation of function despite divergence in primary structure. Biochem. Biophys. Acta 2001, 1541, 2–21. [Google Scholar] [CrossRef] [Green Version]
- Zhang, X.P.; Glaser, E. Interaction of plant mitochondrial and chloroplast signal peptides with the Hsp70 molecular chaperone. Trends Plant Sci. 2002, 7, 14–21. [Google Scholar] [CrossRef]
- Lee, D.W.; Lee, S.; Oh, Y.J.; Hwang, I. Multiple sequence motifs in the rubisco small subunit transit peptide independently contribute to Toc159-dependent import of proteins into chloroplasts. Plant Physiol. 2009, 151, 129–141. [Google Scholar] [CrossRef] [Green Version]
- Chotewutmontri, P.; Reddick, L.E.; McWilliams, D.R.; Campbell, I.M.; Bruce, B.D. Differential transit peptide recognition during preprotein binding and translocation into flowering plant plastids. Plant Cell 2012, 24, 3040–3059. [Google Scholar] [CrossRef] [Green Version]
- Lee, D.W.; Yun-joo, Y.; Abdur, R.; Inhwan, H. Prolines in transit peptides are crucial for efficient preprotein translocation into chloroplasts. Plants Physiol. 2018, 176, 663–677. [Google Scholar] [CrossRef] [Green Version]
- Hansen, K.G.; Johannes, M.H. Transport of proteins into mitochondria. Protein J. 2019, 38, 330–342. [Google Scholar] [CrossRef]
- Schnell, D.J. The TOC GTPase receptors: Regulators of the fidelity, specificity and substrate profiles of the general protein import machinery of chloroplasts. Protein J. 2019, 38, 343–350. [Google Scholar] [CrossRef] [Green Version]
- Nielsen, M.M.; Bozonnet, S.; Seo, E.S.; Motyan, J.A.; Andersen, J.M.; Dilokpimol, A.; Hachem, M.A.; Gyemant, G.; Naested, H.; Kandra, L.; et al. Two secondary carbohydrate binding sites on the surface of barley a-amylase 1 have distinct functions and display synergy in hydrolysis of starch granules. Biochem. J. 2009, 48, 7686–7697. [Google Scholar] [CrossRef]
- Machovic, M.; Janecek, S. Starch-binding domains in the post-genome era. Cell Mol. Life Sci. 2006, 63, 2710–2724. [Google Scholar] [CrossRef]
- Guillen, D.; Santiago, M.; Linares, L.; Perez, R.; Morlon, J.; Ruiz, B.; Sanchez, S.; Rodriguez-Sanoja, R. Alpha-amylase starch binding domains: Cooperative effects of binding to starch granules of multiple tandemly arranged domains. Appl. Environ. Microbiol. 2007, 73, 3833–3837. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kötting, O.; Santelia, D.; Edner, C.; Eicke, S.; Marthaler, T.; Gentry, M.S.; Comparot-Moss, S.; Chen, J.; Smith, A.M.; Steup, M.; et al. STARCH-EXCESS4 is a laforin-like phosphoglucan phosphatase required for starch degradation in Arabidopsis thaliana. Plant Cell 2009, 21, 334–346. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Species | Protein | Size | MW | II | AI | GRAVY | Cysteines | DC Prediction |
---|---|---|---|---|---|---|---|---|
P. umbilicalis | GWD1 | 1343 | 144,770.79 | 38.61 | 88.75 | −0.172 | 18 | 9 |
C. crispus | GWD1 | 1353 | 150,301.30 | 39.12 | 88.14 | −0.343 | 15 | 7 |
C. zofingiensis | GWD1 | 1086 | 118,300.07 | 45.26 | 87.13 | −0.120 | 18 | 9 |
A. protothecoides | GWD1 | 1252 | 135,517.80 | 34.80 | 94.46 | −0.122 | 10 | 5 |
C. reinhardtii | GWD1 | 1411 | 154,283.18 | 39.07 | 86.88 | −0.282 | 24 | 12 |
S. moellendorffi | GWD1 | 1309 | 146,481.65 | 39.89 | 92.80 | −0.330 | 10 | 5 |
M. polymorpha | GWD1 | 1424 | 156,626.81 | 44.27 | 89.37 | −0.336 | 14 | 7 |
S. magellanicum | GWD1 | 1546 | 170,633.58 | 43.31 | 91.60 | −0.294 | 18 | 9 |
P. patens GWDa | GWD1 | 1415 | 157,825.51 | 43.24 | 93.82 | −0.284 | 13 | 6 |
P. patens GWDb | GWD1 | 1420 | 157,172.42 | 37.61 | 88.67 | −0.336 | 14 | 7 |
A.trichopoda | GWD2 | 1302 | 146,933.48 | 43.48 | 95.38 | −0.303 | 21 | 10 |
L. usitatissimum | GWD2 | 1325 | 149,512.75 | 44.00 | 96.78 | −0.250 | 19 | 9 |
M. esculenta | GWD2 | 1228 | 138,500.88 | 38.41 | 95.01 | −0.239 | 20 | 10 |
R. communis | GWD2 | 1300 | 146,401.26 | 40.44 | 94.83 | −0.205 | 27 | 13 |
G. hirsutum | GWD2 | 1303 | 146,156.91 | 41.26 | 96.57 | −0.192 | 23 | 11 |
T. cacao | GWD2 | 1246 | 140,321.26 | 38.25 | 92.54 | −0.235 | 24 | 12 |
C. clementina | GWD2 | 1244 | 141,040.53 | 44.60 | 93.63 | −0.253 | 25 | 12 |
M. maritima | GWD2 | 1276 | 144,304.40 | 41.83 | 92.79 | −0.294 | 28 | 14 |
C. rubella | GWD2 | 1278 | 144,939.00 | 41.05 | 92.34 | −0.302 | 20 | 10 |
A. thaliana | GWD2 | 1278 | 144,811.75 | 43.11 | 92.34 | −0.308 | 22 | 11 |
M. perfoliatum | GWD2 | 1243 | 140,157.32 | 38.33 | 91.65 | −0.287 | 25 | 12 |
B. oleracea | GWD2 | 1400 | 158,307.56 | 41.00 | 91.60 | −0.278 | 31 | 15 |
B. rapa | GWD2 | 1281 | 144,354.66 | 38.83 | 92.73 | −0.264 | 27 | 13 |
A. trichopoda | GWD1 | 1385 | 155,862.42 | 45.67 | 91.28 | −0.400 | 10 | 5 |
D. alata | GWD1 | 1515 | 169,131.63 | 43.87 | 89.46 | −0.374 | 11 | 5 |
M. acumulata | GWD1 | 1611 | 181,353.26 | 46.94 | 92.58 | −0.331 | 15 | 7 |
A. comosus | GWD1 | 1474 | 165,093.79 | 45.80 | 93.32 | −0.332 | 14 | 7 |
P. miliaceum | GWD1 | 1468 | 163,391.24 | 47.62 | 91.39 | −0.343 | 11 | 5 |
S. bicolor | GWD1 | 1469 | 164,264.97 | 47.06 | 88.90 | −0.385 | 10 | 5 |
Z. mays | GWD1 | 1469 | 163,962.14 | 47.30 | 87.71 | −0.394 | 9 | 4 |
O. sativa | GWD1 | 1203 | 134,156.82 | 43.91 | 89.34 | −0.364 | 11 | 5 |
B. distachyon | GWD1 | 1455 | 162,600.00 | 46.05 | 90.10 | −0.349 | 11 | 5 |
H. vulgare | GWD1 | 1410 | 157,590.85 | 42.25 | 88.57 | −0.375 | 9 | 4 |
T. aestivum | GWD1 | 1374 | 154,082.86 | 42.83 | 89.68 | −0.372 | 9 | 4 |
A. hypochondriacus | GWD1 | 1398 | 156,105.95 | 44.12 | 89.88 | −0.380 | 12 | 6 |
H. annuus | GWD1 | 1456 | 163,484.38 | 41.30 | 90.36 | −0.394 | 13 | 6 |
C. arabica | GWD1 | 1474 | 165,508.56 | 48.40 | 88.06 | −0.439 | 11 | 5 |
N. tabacum | GWD1 | 1464 | 163,426.17 | 44.00 | 90.78 | −0.370 | 10 | 5 |
C. annuum | GWD1 | 1464 | 163,598.62 | 40.00 | 91.78 | −0.351 | 9 | 4 |
S. lycopersicum | GWD1 | 1465 | 163,791.47 | 41.29 | 91.31 | −0.356 | 11 | 5 |
S. chacoense | GWD1 | 1432 | 159,732.07 | 40.65 | 91.85 | −0.351 | 10 | 5 |
S. tuberosum | GWD1 | 1463 | 163,261.11 | 40.90 | 92.05 | −0.351 | 10 | 5 |
V. vinifera | GWD1 | 1478 | 165,452.70 | 39.46 | 91.79 | −0.353 | 12 | 6 |
F. vesca | GWD1 | 1400 | 155,592.13 | 41.59 | 91.84 | −0.359 | 13 | 6 |
M. domestica | GWD1 | 1405 | 156,915.34 | 39.52 | 87.72 | −0.426 | 8 | 4 |
C. melo | GWD1 | 1471 | 164,902.74 | 42.29 | 93.06 | −0.370 | 10 | 5 |
G. max | GWD1 | 1459 | 163,761.56 | 40.49 | 89.80 | −0.406 | 10 | 5 |
P. vulgaris | GWD1 | 1456 | 163,484.38 | 41.30 | 90.36 | −0.394 | 13 | 6 |
V. unguiculata | GWD1 | 1455 | 163,535.52 | 41.22 | 91.19 | −0.386 | 11 | 5 |
L. usitatissimum | GWD1 | 1480 | 164,831.39 | 46.33 | 87.55 | −0.384 | 12 | 6 |
M. esuculenta | GWD1 | 1409 | 157,838.14 | 45.03 | 91.34 | −0.346 | 9 | 4 |
R. communis | GWD1 | 1469 | 164,321.24 | 46.37 | 90.13 | −0.388 | 9 | 4 |
G. hirsutum | GWD1 | 1471 | 164,719.18 | 42.70 | 90.74 | −0.399 | 12 | 6 |
T. cacao | GWD1 | 1470 | 164,632.01 | 42.34 | 89.82 | −0.386 | 12 | 6 |
C. clementina | GWD1 | 1388 | 155,729.81 | 44.94 | 91.97 | −0.361 | 11 | 5 |
C. papaya | GWD1 | 1473 | 165,710.38 | 40.31 | 92.52 | −0.391 | 11 | 5 |
M. perfoliatum | GWD1 | 1413 | 158,428.12 | 41.53 | 89.89 | −0.407 | 10 | 5 |
B. oleracea | GWD1 | 1396 | 156,676.20 | 44.73 | 89.16 | −0.428 | 11 | 5 |
B. rapa | GWD1 | 1399 | 156,557.78 | 42.31 | 90.09 | −0.390 | 11 | 5 |
M. maritima | GWD1 | 1401 | 156,892.19 | 42.20 | 90.31 | −0.401 | 10 | 5 |
C. rubella | GWD1 | 1392 | 155,931.95 | 44.29 | 89.29 | −0.429 | 10 | 5 |
A. thaliana | GWD1 | 1399 | 156,581.78 | 41.14 | 89.74 | −0.414 | 10 | 5 |
Species | Protein | TargetP 2.0 | Multiloc2 | |||||||
---|---|---|---|---|---|---|---|---|---|---|
cTP | mTP | Others | Loc | TPlen | Ch | Cy | M | SP | ||
P. umbilicalis | GWD1 | 0.00 | 0.00 | 1.00 | _ | 0.54 | 0.29 | 0.08 | 0.00 | |
C. crispus | GWD1 | 0.00 | 0.00 | 1.00 | _ | 0.21 | 0.72 | 0.03 | 0.00 | |
C. zofingiensis | GWD1 | 0.13 | 0.00 | 0.87 | _ | 0.11 | 0.70 | 0.01 | 0.16 | |
A. protothecoides | GWD1 | 0.00 | 0.00 | 0.99 | 0.28 | 0.65 | 0.04 | 0.00 | ||
C. reinhardtii | GWD1 | 0.78 | 0.19 | 0.06 | C | 75–76 | 0.96 | 0.02 | 0.02 | 0.0 |
S. moellendorffi | GWD1 | 0.00 | 0.00 | 1.00 | _ | 0.48 | 0.06 | 0.45 | 0.01 | |
M. polymorpha | GWD1 | 0.00 | 0.00 | 1.00 | _ | 0.84 | 0.07 | 0.06 | 0.00 | |
S. magellanicum | GWD1 | 0.02 | 0.00 | 0.98 | _ | 0.89 | 0.04 | 0.06 | 0.00 | |
P. patens GWDa | GWD1 | 0.00 | 0.40 | 0.53 | _ | 0.87 | 0.05 | 0.06 | 0.00 | |
P. patens GWDb | GWD1 | 0.27 | 0.47 | 0.26 | M | 68–69 | 0.60 | 0.02 | 0.35 | 0.00 |
A. trichopoda | GWD2 | 0.00 | 0.00 | 1.00 | _ | 0.73 | 0.19 | 0.03 | 0.00 | |
L. usitatissimum | GWD2 | 0.00 | 0.00 | 0.98 | _ | 0.06 | 0.28 | 0.02 | 0.63 | |
M. esculenta | GWD2 | 0.01 | 0.00 | 0.99 | _ | 0.32 | 0.50 | 0.04 | 0.12 | |
R. communis | GWD2 | 0.00 | 0.00 | 0.99 | _ | 0.34 | 0.51 | 0.04 | 0.00 | |
G. hirsutum | GWD2 | 0.02 | 0.o1 | 0.95 | _ | 0.64 | 0.24 | 0.09 | 0.00 | |
T. cacao | GWD2 | 0.00 | 0.00 | 0.99 | _ | 0.70 | 0.17 | 0.09 | 0.01 | |
C. clementina | GWD2 | 0.00 | 0.00 | 1.00 | _ | 0.28 | 0.38 | 0.04 | 0.24 | |
M. maritima | GWD2 | 0.01 | 0.12 | 0.87 | _ | 0.71 | 0.17 | 0.08 | 0.00 | |
C. rubella | GWD2 | 0.00 | 0.00 | 1.00 | _ | 0.12 | 0.6 | 0.07 | 0.00 | |
A. thaliana | GWD2 | 0.00 | 0.00 | 1.00 | _ | 0.15 | 0.67 | 0.13 | 0.00 | |
M. perfoliatum | GWD2 | 0.00 | 0.00 | 1.00 | _ | 0.13 | 0.6 | 0.07 | 0.00 | |
B. oleracea | GWD2 | 0.00 | 0.00 | 1.00 | _ | 0.09 | 0.33 | 0.11 | 0.03 | |
B. rapa | GWD2 | 0.00 | 0.05 | 0.93 | _ | 0.19 | 0.59 | 0.14 | 0.00 | |
A. trichopoda | GWD1 | 0.00 | 0.00 | 1.00 | _ | 0.16 | 0.76 | 0.03 | 0.00 | |
D. alata | GWD1 | 0.71 | 0.00 | 0.28 | C | 96–97 | 0.70 | 0.19 | 0.07 | 0.00 |
M. acumulata | GWD1 | 0.07 | 0.00 | 0.79 | _ | 0.80 | 0.10 | 0.07 | 0.02 | |
A. comosus | GWD1 | 0.91 | 0.00 | 0.08 | C | 85–86 | 0.94 | 0.01 | 0.04 | 0.00 |
P. miliaceum | GWD1 | 0.97 | 0.00 | 0.03 | C | 61–62 | 0.95 | 0.02 | 0.03 | 0.00 |
S. bicolor | GWD1 | 0.99 | 0.00 | 0.00 | C | 65–66 | 0.94 | 0.03 | 0.03 | 0.00 |
Z. mays | GWD1 | 0.97 | 0.00 | 0.03 | C | 65–66 | 0.94 | 0.03 | 0.03 | 0.00 |
O. sativa | GWD1 | 0.96 | 0.01 | 0.03 | C | 62–63 | 0.90 | 0.01 | 0.04 | 0.00 |
B. distachyon | GWD1 | 0.96 | 0.00 | 0.04 | C | 57–58 | 0.94 | 0.01 | 0.05 | 0.00 |
H. vulgare | GWD1 | 0.03 | 0.59 | 0.39 | M | 16–17 | 0.47 | 0.04 | 0.49 | 0.00 |
T. aestivum | GWD1 | 0.00 | 0.00 | 1.00 | _ | 0.48 | 0.37 | 0.1 | 0.01 | |
A. hypochondriacus | GWD1 | 0.00 | 0.05 | 0.95 | _ | 0.70 | 0.16 | 0.02 | 0.00 | |
H. annuus | GWD1 | 0.91 | 0.02 | 0.07 | C | 81–82 | 0.92 | 0.01 | 0.02 | 0.00 |
C. arabica | GWD1 | 0.00 | 0.00 | 1.0 | _ | 0.74 | 0.02 | 0.23 | 0.00 | |
N. tabacum | GWD1 | 0.81 | 0.03 | 0.16 | C | 76–77 | 0.97 | 0.01 | 0.02 | 0.00 |
C. annuum | GWD1 | 0.90 | 0.02 | 0.07 | C | 76–77 | 0.44 | 0.50 | 0.03 | 0.00 |
S. lycopersicum | GWD1 | 0.76 | 0.02 | 0.21 | C | 77–78 | 0.94 | 0.03 | 0.03 | 0.00 |
S. chacoense | GWD1 | 0.81 | 0.04 | 0.16 | C | 76–77 | 0.96 | 0.01 | 0.02 | 0.00 |
S. tuberosum | GWD1 | 0.76 | 0.03 | 0.2 | C | 76–77 | 0.96 | 0.02 | 0.01 | 0.00 |
V. vinifera | GWD1 | 0.51 | 0.26 | 0.23 | C | 79–80 | 0.91 | 0.03 | 0.05 | 0.00 |
F. vesca | GWD1 | 1.00 | 0.00 | 0.00 | C | 69–70 | 0.94 | 0.01 | 0.04 | 0.00 |
M. domestica | GWD1 | 0.93 | 0.00 | 0.06 | C | 76–77 | 0.94 | 0.01 | 0.04 | 0.00 |
C. melo | GWD1 | 0.61 | 0.11 | 0.28 | C | 84–85 | 0.92 | 0.01 | 0.07 | 0.00 |
G. max | GWD1 | 0.68 | 0.01 | 0.24 | C | 72–73 | 0.95 | 0.01 | 0.04 | 0.00 |
P. vulgaris | GWD1 | 0.74 | 0.00 | 0.16 | C | 54–55 | 0.89 | 0.05 | 0.04 | 0.01 |
V. unguiculata | GWD1 | 0.50 | 0.00 | 0.4786 | C | 60–61 | 0.95 | 0.07 | 0.02 | 0.00 |
L. usitatissimum | GWD1 | 0.80 | 0.00 | 0.19 | C | 91–92 | 0.96 | 0.01 | 0.03 | 0.00 |
M. esuculenta | GWD1 | 0.88 | 0.02 | 0.10 | C | 83–84 | 0.93 | 0.04 | 0.03 | 0.00 |
R. communis | GWD1 | 0.66 | 0.04 | 0.29 | C | 82–83 | 0.92 | 0.03 | 0.04 | 0.00 |
G. hirsutum | GWD1 | 0.77 | 0.01 | 0.23 | C | 84–85 | 0.94 | 0.01 | 0.05 | 0.00 |
T. cacao | GWD1 | 0.90 | 0.00 | 0.10 | C | 84–85 | 0.87 | 0.05 | 0.06 | 0.00 |
C. clementina | GWD1 | 0.51 | 0.08 | 0.41 | C | 91–92 | 0.28 | 0.38 | 0.04 | 0.00 |
C. papaya | GWD1 | 0.01 | 0.00 | 0.99 | _ | 0.93 | 0.01 | 0.05 | 0.00 | |
M. perfoliatum | GWD1 | 0.26 | 0.02 | 0.72 | _ | 0.91 | 0.01 | 0.05 | 0.00 | |
B. oleracea | GWD1 | 0.81 | 0.10 | 0.10 | C | 74–75 | 0.77 | 0.05 | 0.15 | 0.01 |
B. rapa | GWD1 | 0.42 | 0.40 | 0.17 | C | 75–76 | 0.84 | 0.01 | 0.11 | 0.00 |
M. maritima | GWD1 | 0.37 | 0.54 | 0.08 | M | 40–41 | 0.91 | 0.01 | 0.03 | 0.00 |
C. rubella | GWD1 | 0.58 | 0.22 | 0.20 | C | 67–68 | 0.85 | 0.05 | 0.08 | 0.00 |
A. thaliana | GWD1 | 0.53 | 0.22 | 0.25 | C | 74–75 | 0.80 | 0.08 | 0.11 | 0.01 |
Species | CBM45−1 | CBM45−2 | CFACT | |||
---|---|---|---|---|---|---|
Position | Score | Position | Score | Position | Score | |
Irish moss | W139R | −5.506 | F520A | −5.14 | C1079G | −5.57 |
F536L | −3.65 | F1080L | −4.20 | |||
A1081V | −3.70 | |||||
C. zofingiensis | W129del | −11.64 | C1079L | 0.27 | ||
W139del | −9.03 | |||||
F184del | −7.88 | |||||
W194del | −10.49 | |||||
F202del | −7.56 | |||||
G. hirsutum | W129del | −11.64 | ||||
W139del | −9.03 | |||||
F184del | −7.88 | |||||
W194del | −10.49 | |||||
F202del | −7.56 | |||||
A. protothecoides | W129L | −7.45 | F536Y | −1.18 | C1079L | 0.27 |
W139T | −5.82 | |||||
F184T | −4.62 | |||||
W194del | −10.49 | |||||
F202E | −2.95 | |||||
P. miliaceum | W194C | −7.55 | F520del | −8.40 | C1079L | 0.27 |
F202del | −7.56 | W528del | −12.34 | |||
F536del | −7.40 | |||||
C. arabica | W129del | −11.64 | ||||
M. esculenta/GWD2 | W129del | −11.06 | ||||
C. reinhardtii | W129R | −8.04 | C1079L | 0.27 | ||
W139L | −6.078 | |||||
S. bicolor | C1079L | 0.27 | ||||
Z. mays | C1079L | 0.27 | ||||
O. sativa | C1079L | 0.27 | ||||
B. distachyon | C1079L | 0.27 | ||||
H. vulgare | C1079L | 0.27 | ||||
T. aestivum | C1079L | 0.27 | ||||
P. umbilicalis | W139S | −5.93 | F520A | −5.14 | C1079G | −5.57 |
F536M | −3.72 | F1080L | −4.20 | |||
A1081V | −3.70 | |||||
S. moellendorffi | C1079L | 0.27 | ||||
M. polymorpha | F536Y | −1.18 | ||||
S. magellanicum | F536Y | −1.18 | ||||
P. patens (GWDA and B) | F536Y | −1.18 | ||||
T. cacao | F520del | −8.40 | ||||
W528del | −12.34 | |||||
F536del | −7.40 |
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Adegbaju, M.S.; Morenikeji, O.B.; Borrego, E.J.; Hudson, A.O.; Thomas, B.N. Differential Evolution of α-Glucan Water Dikinase (GWD) in Plants. Plants 2020, 9, 1101. https://doi.org/10.3390/plants9091101
Adegbaju MS, Morenikeji OB, Borrego EJ, Hudson AO, Thomas BN. Differential Evolution of α-Glucan Water Dikinase (GWD) in Plants. Plants. 2020; 9(9):1101. https://doi.org/10.3390/plants9091101
Chicago/Turabian StyleAdegbaju, Muyiwa S., Olanrewaju B. Morenikeji, Eli J. Borrego, André O. Hudson, and Bolaji N. Thomas. 2020. "Differential Evolution of α-Glucan Water Dikinase (GWD) in Plants" Plants 9, no. 9: 1101. https://doi.org/10.3390/plants9091101