Analysis of Germin-like Protein Genes (OsGLPs) Family in Rice Using Various In silico Approaches

Author(s): Muhammad Ilyas*, Muhammad Irfan, Tariq Mahmood, Hazrat Hussain, Latif-ur-Rehman, Ijaz Naeem, Khaliq-ur-Rahman.

Journal Name: Current Bioinformatics

Volume 15 , Issue 1 , 2020

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Background: Germin-like Proteins (GLPs) play an important role in various stresses. Rice contains 43 GLPs, among which many remain functionally unexplored. The computational analysis will provide significant insight into their function.

Objective: To find various structural properties, functional importance, phylogeny and expression pattern of all OsGLPs using various bioinformatics tools.

Methods: Physiochemical properties, sub-cellular localization, domain composition, Nglycosylation and Phosphorylation sites, and 3D structural models of the OsGLPs were predicted using various bioinformatics tools. Functional analysis was carried out with the Search Tool for the Retrieval of Interacting Genes/Proteins (STRING) and Blast2GO servers. The expression profile of the OsGLPs was predicted by retrieving the data for expression values from tissuespecific and hormonal stressed array libraries of RiceXPro. Their phylogenetic relationship was computed using Molecular and Evolutionary Genetic Analysis (MEGA6) tool.

Results: Most of the OsGLPs are stable in the cellular environment with a prominent expression in the extracellular region (57%) and plasma membrane (33%). Besides, 3 basic cupin domains, 7 more were reported, among which NTTNKVGSNVTLINV, FLLAALLALASWQAI, and MASSSF were common to 99% of the sequences, related to bacterial pathogenicity, peroxidase activity, and peptide signal activity, respectively. Structurally, OsGLPs are similar but functionally they are diverse with novel enzymatic activities of oxalate decarboxylase, lyase, peroxidase, and oxidoreductase. Expression analysis revealed prominent activities in the root, endosperm, and leaves. OsGLPs were strongly expressed by abscisic acid, auxin, gibberellin, cytokinin, and brassinosteroid. Phylogenetically they showed polyphyletic origin with a narrow genetic background of 0.05%. OsGLPs of chromosome 3, 8, and 12 are functionally more important due to their defensive role against various stresses through co-expression strategy.

Conclusion: The analysis will help to utilize OsGLPs in future food programs.

Keywords: OsGLPs, phylogenetic, rice, expression, in silico, peptide.

[1]
Banerjee J, Maiti MK. Functional role of rice germin-like protein1 in regulation of plant height and disease resistance. Biochem Biophys Res Commun 2010; 394(1): 178-83.
[http://dx.doi.org/10.1016/j.bbrc.2010.02.142] [PMID: 20188068]
[2]
Dunwell JM, Gibbings JG, Mahmood T, Saqlan Naqvi SM. Germin and germin-like proteins: Evolution, structure, and function. CRC. Crit Rev Plant Sci 2008; 27: 342-75.
[http://dx.doi.org/10.1080/07352680802333938]
[3]
de Freitas CDT, da Cruz WT, Silva MZR, et al. Proteomic analysis and purification of an unusual germin-like protein with proteolytic activity in the latex of Thevetia peruviana. Planta 2016; 243(5): 1115-28.
[http://dx.doi.org/10.1007/s00425-016-2468-8] [PMID: 26794967]
[4]
Ilyas M, Rasheed A, Mahmood T. Functional characterization of germin and germin-like protein genes in various plant species using transgenic approaches. Biotechnol Lett 2016; 38(9): 1405-21.
[http://dx.doi.org/10.1007/s10529-016-2129-9] [PMID: 27230937]
[5]
Kearse M, Moir R, Wilson A, et al. Geneious. Bioinformatics 2012; 28: 1647-9.
[http://dx.doi.org/10.1093/bioinformatics/bts199]
[6]
Liu B, Liu F, Wang X, Chen J, Fang L, Chou K-C. Pse-in-One: A web server for generating various modes of pseudo components of DNA, RNA, and protein sequences. Nucleic Acids Res 2015; 43: W65-71.
[http://dx.doi.org/10.1093/nar/gkv458]
[7]
Liu B, Wu H, Zhang D, Wang X, Chou K-C. Pse-Analysis: A python package for DNA/RNA and protein/ peptide sequence analysis based on pseudo components and kernel methods. Oncotarget 2017; 8: 13338-43.
[http://dx.doi.org/10.18632/oncotarget.14524] [PMID: 28076851]
[8]
Lin C, Chen W, Qiu C, Wu Y, Krishnan S, Zou Q. LibD3C: Ensemble classifiers with a clustering and dynamic selection strategy. Neurocomputing 2014; 123: 424-35.
[http://dx.doi.org/10.1016/j.neucom.2013.08.004]
[9]
Nagy T, Yosa Reyes J, Meuwly M. Multisurface Adiabatic Reactive Molecular Dynamics. J Chem Theory Comput 2014; 10: 1366-75.
[http://dx.doi.org/10.1021/ct400953f]
[10]
Tong X, Nagy T, Reyes JY, Germann M, Meuwly M, Willitsch S. State-selected ion -molecule reactions with Coulomb-crystallized molecular ions in traps. Chem Phys Lett 2012; 547: 1-8.
[http://dx.doi.org/10.1016/j.cplett.2012.06.042]
[11]
Hollebeek T, Ho TS, Rabitz H. Constructing multidimensional molecular potential energy surfaces from ab initio data. Annu Rev Phys Chem 1999; 50: 537-70.
[http://dx.doi.org/10.1146/annurev.physchem.50.1.537]
[12]
Sato Y, Antonio BA, Namiki N, Takehisa H, Minami H, Kamatsuki K, et al. RiceXPro: A platform for monitoring gene expression in japonica rice grown under natural field conditions Nucleic Acids Res. 2011; 39: D1141-D1148.
[http://dx.doi.org/10.1093/nar/gkq1085]
[13]
Davidson RM, Manosalva PM, Snelling J, Bruce M, Leung H, Leach JE. Rice germin-like proteins: Allelic diversity and relationships to early stress responses. Rice (N Y) 2010; 3: 43-55.
[http://dx.doi.org/10.1007/s12284-010-9038-7]
[14]
Lu M, Han Y-P, Gao J-G, Wang X-J, Li W-B. Identification and analysis of the germin-like gene family in soybean. BMC Genomics 2010; 11: 620.
[http://dx.doi.org/10.1186/1471-2164-11-620] [PMID: 21059215]
[15]
Sassaki FT, Bravo JP, González ER, Maia IG. Expression pattern and promoter analysis of a Eucalyptus grandis Germin-like Gene. Plant Mol Biol Report 2014; 33: 12-21.
[http://dx.doi.org/10.1007/s11105-014-0734-0]
[16]
Manosalva PM, Davidson RM, Liu B, et al. A germin-like protein gene family functions as a complex quantitative trait locus conferring broad-spectrum disease resistance in rice. Plant Physiol 2009; 149(1): 286-96.
[http://dx.doi.org/10.1104/pp.108.128348] [PMID: 19011003]
[17]
Banerjee J, Das N, Dey P, Maiti MK. Transgenically expressed rice germin-like protein1 in tobacco causes hyper-accumulation of H2O2 and reinforcement of the cell wall components. Biochem Biophys Res Commun 2010; 402(4): 637-43.
[http://dx.doi.org/10.1016/j.bbrc.2010.10.073] [PMID: 20971065]
[18]
Mahmood T, Yasmin T, Haque MI, Naqvi SMS. Characterization of a rice germin-like protein gene promoter. Genet Mol Res Genet Mol Res 2013; 12: 360-9.
[http://dx.doi.org/10.4238/2013.February.7.6]
[19]
Durrani IS, Bakht J, Swati ZA, Naqvi SMS. Cloning of OsRGLP9 gene obtained from Oryza sativa in Nicotiana tabacum. Pak J Weed Sci Res 2015; 21: 123-36.
[20]
Yasmin T, Mumtaz A, Mahmood T, Hyder MZ, Naqvi SMS. A germin-like protein gene of rice increased superoxide dismutase activity in transformed tobacco. Biol Plant 2015; 59: 456-62.
[http://dx.doi.org/10.1007/s10535-015-0524-z]
[21]
Marchler-Bauer A, Zheng C, Chitsaz F, et al. CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res 2013; 41(Database issue): D348-52.
[PMID: 23197659]
[22]
Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 1999; 41: 95-8.
[23]
Bailey TL, Boden M, Buske FA, et al. MEME SUITE: tools for motif discovery and searching Nucleic Acids Res 2009; 37(Web Server issue): W202-8.
[http://dx.doi.org/10.1093/nar/gkp335] [PMID: 19458158 ]
[24]
Pagni M, Ioannidis V, Cerutti L, Zahn-Zabal M, Jongeneel CV, Hau J, et al. MyHits: Improvements to an interactive resource for analyzing protein sequences. Nucleic Acids Res 2007; 35: W433-7.
[http://dx.doi.org/10.1093/nar/gkm352]
[25]
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30(12): 2725-9.
[http://dx.doi.org/10.1093/molbev/mst197] [PMID: 24132122]
[26]
Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A. ExPASy: The proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 2003; 31: 3784-8.
[27]
Yu C-S, Chen Y-C, Lu C-H, Hwang J-K. Prediction of protein subcellular localization. Proteins 2006; 64(3): 643-51.
[http://dx.doi.org/10.1002/prot.21018] [PMID: 16752418]
[28]
Horton P, Park KJ, Obayashi T, et al. WoLF PSORT: protein localization predictor Nucleic Acids Res 2007; 35(Web Server issue): W585-7.
[PMID: 17517783]
[29]
Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011; 8(10): 785-6.
[http://dx.doi.org/10.1038/nmeth.1701] [PMID: 21959131]
[30]
Blom N, Sicheritz-Pontén T, Gupta R, Gammeltoft S, Brunak S. Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 2004; 4(6): 1633-49.
[http://dx.doi.org/10.1002/pmic.200300771] [PMID: 15174133]
[31]
Biasini M, Bienert S, Waterhouse A, et al. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information Nucleic Acids Res 2014; 42(Web Server issue): W252-8.
[http://dx.doi.org/10.1093/nar/gku340] [PMID: 24782522]
[32]
Lovell SC, Davis IW, Arendall WB, de Bakker PIW, Word JM, Prisant MG, et al. Structure validation by Cá geometry: ϕ, ø and Câ deviation. Proteins 2003; 50: 437-50.
[http://dx.doi.org/10.1002/prot.10286] [PMID: 12557186]
[33]
Szklarczyk D, Franceschini A, Wyder S, et al. STRING v10: Protein -protein interaction networks, integrated over the tree of life. Nucleic Acids Res 2015; 43: D447-52.
[http://dx.doi.org/10.1093/nar/gku1003]
[34]
Conesa A, and Götz S. Blast2GO: A comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008; 2008619832
[http://dx.doi.org/10.1155/2008/619832]
[35]
Weinstein JN, Myers TG, O’Connor PM, et al. An information-intensive approach to the molecular pharmacology of cancer. Science 1997; 275: 343-9.
[http://dx.doi.org/10.1126/science.275.5298.343]
[36]
White ES, Baralle FE, Muro AF. New insights into form and function of fibronectin splice variants. J Pathol 2008; 216(1): 1-14.
[http://dx.doi.org/10.1002/path.2388] [PMID: 18680111]
[37]
Zimmermann G, Bäumlein H, Mock H-P, Himmelbach A, Schweizer P. The multigene family encoding germin-like proteins of barley. Regulation and function in Basal host resistance. Plant Physiol 2006; 142(1): 181-92.
[http://dx.doi.org/10.1104/pp.106.083824] [PMID: 16844832]
[38]
Breen J, Bellgard M. Germin-like proteins (GLPs) in cereal genomes: gene clustering and dynamic roles in plant defence. Funct Integr Genomics 2010; 10(4): 463-76.
[http://dx.doi.org/10.1007/s10142-010-0184-1] [PMID: 20683632]
[39]
Lai J, Li Y, Messing J, Dooner HK. Gene movement by Helitron transposons contributes to the haplotype variability of maize. Proc Natl Acad Sci USA 2005; 102(25): 9068-73.
[http://dx.doi.org/10.1073/pnas.0502923102] [PMID: 15951422 ]
[40]
Misra RC, Garg A, Roy S, Chanotiya CS, Vasudev PG, Ghosh S. Involvement of an ent-copalyl diphosphate synthase in tissue-specific accumulation of specialized diterpenes in Andrographis paniculata. Plant Sci 2015; 240: 50-64.
[http://dx.doi.org/10.1016/j.plantsci.2015.08.016] [PMID: 26475187]
[41]
Audain E, Ramos Y, Hermjakob H, Flower DR, Perez-riverol Y. Accurate estimation of isoelectric point of protein and peptide based on amino acid sequences 2016 32(6): 821-7.
[http://dx.doi.org/10.1093/bioinformatics/btv674]
[42]
Adeloye AO, Ajibade PA. A high molar extinction coefficient mono-anthracenyl bipyridyl heteroleptic ruthenium(II) complex: synthesis, photophysical and electrochemical properties. Molecules 2011; 16(6): 4615-31.
[http://dx.doi.org/10.3390/molecules16064615] [PMID: 21642936]
[43]
Ikai A. Thermostability and aliphatic index of globular proteins. J Biochem 1980; 88(6): 1895-8.
[PMID: 7462208]
[44]
Wang T, Chen X, Zhu F, et al. Characterization of peanut germin-like proteins, AhGLPs in plant development and defense. PLoS One 2013; 8(4)e61722
[http://dx.doi.org/10.1371/journal.pone.0061722] [PMID: 23626720]
[45]
Yin K, Han X, Xu Z, Xue H. Arabidopsis GLP4 is localized to the Golgi and binds auxin in vitro. Acta Biochim Biophys Sin (Shanghai) 2009; 41(6): 478-87.
[http://dx.doi.org/10.1093/abbs/gmp036] [PMID: 19499151]
[46]
Rayon C, Lerouge P, Faye L. The protein N-glycosylation in plants. J Exp Bot 1998; 49(326): 1463-72.
[http://dx.doi.org/10.1093/jxb/49.326.1463]
[47]
Pan HY, Whittaker MM, Bouveret R, Berna A, Bernier F, Whittaker JW. Characterization of wheat germin (oxalate oxidase) expressed by Pichia pastoris. Biochem Biophys Res Commun 2007; 356(4): 925-9.
[http://dx.doi.org/10.1016/j.bbrc.2007.03.097] [PMID: 17399681]
[48]
León-Galván F, de Jesús Joaquín-Ramos A, Torres-Pacheco I, et al. A germin-like protein gene (CchGLP) of Capsicum chinense Jacq. is induced during incompatible interactions and displays Mn-superoxide dismutase activity. Int J Mol Sci 2011; 12(11): 7301-13.
[http://dx.doi.org/10.3390/ijms12117301] [PMID: 22174599]
[49]
Dunwell JM, Purvis A, Khuri S. Cupins: the most functionally diverse protein superfamily? Phytochemistry 2004; 65(1): 7-17.
[http://dx.doi.org/10.1016/j.phytochem.2003.08.016] [PMID: 14697267]
[50]
Beracochea VC, Almasia NI, Peluffo L, et al. Sunflower germin-like protein HaGLP1 promotes ROS accumulation and enhances protection against fungal pathogens in transgenic Arabidopsis thaliana. Plant Cell Rep 2015; 34(10): 1717-33.
[http://dx.doi.org/10.1007/s00299-015-1819-4] [PMID: 26070410]
[51]
El-Sharkawy I, Mila I, Bouzayen M, Jayasankar S. Regulation of two germin-like protein genes during plum fruit development. J Exp Bot 2010; 61(6): 1761-70.
[http://dx.doi.org/10.1093/jxb/erq043] [PMID: 20202999]
[52]
Kim HJ, Triplett BA. Cotton fiber germin-like protein. I. Molecular cloning and gene expression. Planta 2004; 218(4): 516-24.
[http://dx.doi.org/10.1007/s00425-003-1133-1] [PMID: 14648117]
[53]
Langenbach C, Schultheiss H, Rosendahl M, Tresch N, Conrath U, Goellner K. Interspecies gene transfer provides soybean resistance to a fungal pathogen. Plant Biotechnol J 2016; 14(2): 699-708.
[http://dx.doi.org/10.1111/pbi.12418] [PMID: 26096357]
[54]
Luo Y, Frey EA, Pfuetzner RA, et al. Crystal structure of enteropathogenic Escherichia coli intimin-receptor complex. Nature 2000; 405(6790): 1073-7.
[http://dx.doi.org/10.1038/35016618] [PMID: 10890451]
[55]
Gharib B, Abdallahi OM, Dessein H, De Reggi M. Development of eosinophil peroxidase activity and concomitant alteration of the antioxidant defenses in the liver of mice infected with Schistosoma mansoni. J Hepatol 1999; 30(4): 594-602.
[http://dx.doi.org/10.1016/S0168-8278(99)80189-5] [PMID: 10207800]
[56]
Berman HM, Westbrook J, Feng Z, et al. The Protein Data Bank. Nucleic Acids Res 2000; 28(1): 235-42.
[http://dx.doi.org/10.1093/nar/28.1.235] [PMID: 10592235]
[57]
McGuffin LJ, Buenavista MT, Roche DB. The ModFOLD4 server for the quality assessment of 3D protein models. Nucleic Acids Res 2013; 41(Web Server issue): W368-72.
[http://dx.doi.org/10.1093/nar/gkt294] [PMID: 23620298]
[58]
Zhou AQ, O’Hern CS, Regan L. Revisiting the Ramachandran plot from a new angle. Protein Sci 2011; 20(7): 1166-71.
[http://dx.doi.org/10.1002/pro.644] [PMID: 21538644]
[59]
Liang H, Maynard CA, Allen RD, Powell WA. Increased Septoria musiva resistance in transgenic hybrid poplar leaves expressing a wheat oxalate oxidase gene. Plant Mol Biol 2001; 45(6): 619-29.
[http://dx.doi.org/10.1023/A:1010631318831] [PMID: 11430425]
[60]
Suzuki M, Yagi N, Gerstein M. DNA recognition and superstructure formation by helix-turn-helix proteins. Protein Eng 1995; 8(4): 329-38.
[http://dx.doi.org/10.1093/protein/8.4.329] [PMID: 7567918]
[61]
Avci MK, Yamaner C, Ayvaz M, Yazgan-Karatas A. In silico characterization and comparative analysis of Bacillus subtilis Gntr-type LutR transcription factor. EurAsian J Biosci 2014; 8: 12-28.
[http://dx.doi.org/10.5053/ejobios.2014.8.0.2]
[62]
Yusuf MA, Kumar D, Rajwanshi R, et al. Overexpression of γ-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: physiological and chlorophyll a fluorescence measurements. Biochim Biophys Acta 2010; 1797(8): 1428-38.
[http://dx.doi.org/10.1016/j.bbabio.2010.02.002] [PMID: 20144585]
[63]
Jaszek M, Grzywnowicz K, Malarczyk E, Leonowicz A. Enhanced extracellular laccase activity as a part of the response system of white rot fungi: Trametes versicolor and Abortiporus biennis to paraquat-caused oxidative stress conditions. Pestic Biochem Physiol 2006; 85: 147-54.
[http://dx.doi.org/10.1016/j.pestbp.2006.01.002]
[64]
Vinagre F, Vargas C, Schwarcz K, et al. SHR5: a novel plant receptor kinase involved in plant-N2-fixing endophytic bacteria association. J Exp Bot 2006; 57(3): 559-69.
[http://dx.doi.org/10.1093/jxb/erj041] [PMID: 16397001]
[65]
Burrell MR, Just VJ, Bowater L, et al. Oxalate decarboxylase and oxalate oxidase activities can be interchanged with a specificity switch of up to 282,000 by mutating an active site lid. Biochemistry 2007; 46(43): 12327-36.
[http://dx.doi.org/10.1021/bi700947s] [PMID: 17924657]
[66]
Ishizaki K, Larson TR, Schauer N, Fernie AR, Graham IA, Leaver CJ. The critical role of Arabidopsis electron-transfer flavoprotein:ubiquinone oxidoreductase during dark-induced starvation. Plant Cell 2005; 17(9): 2587-600.
[http://dx.doi.org/10.1105/tpc.105.035162] [PMID: 16055629]
[67]
Berna A, Bernier F. Regulated expression of a wheat germin gene in tobacco: oxalate oxidase activity and apoplastic localization of the heterologous protein. Plant Mol Biol 1997; 33(3): 417-29.
[http://dx.doi.org/10.1023/A:1005745015962] [PMID: 9049263]
[68]
Mathieu M, Neutelings G, Hawkins S, Grenier E, David H. Cloning of a pine germin-like protein (GLP) gene promoter and analysis of its activity in transgenic tobacco Bright Yellow 2 cells. Physiol Plant 2003; 117(3): 425-34.
[http://dx.doi.org/10.1034/j.1399-3054.2003.00050.x] [PMID: 12654044]
[69]
El-Sharkawy I, Mila I, Bouzayen M. Regulation of two germin-like protein genes during plum fruit development 2010 61: 1761-1770.
[http://dx.doi.org/10.1093/jxb/erq043]
[70]
Lu M, Han Y-P, Gao J-G, Wang X-J, Li W-B. Identification and analysis of the germin-like gene family in soybean. BMC Genomics 2011; 12: 16.
[http://dx.doi.org/10.1186/1471-2164-12-16] [PMID: 21059215]
[71]
Tabuchi T, Kumon T, Azuma T, Nanmori T, Yasuda T. The expression of a germin-like protein with superoxide dismutase activity in the halophyte Atriplex lentiformis is differentially regulated by wounding and abscisic acid. Physiol Plant 2003; 118: 523-31.
[http://dx.doi.org/10.1034/j.1399-3054.2003.00133.x]
[72]
Berna A, Bernier F. Regulation by biotic and abiotic stress of a wheat germin gene encoding oxalate oxidase, a H2O2-producing enzyme. Plant Mol Biol 1999; 39(3): 539-49.
[http://dx.doi.org/10.1023/A:1006123432157] [PMID: 10092181]
[73]
Livingstone DM, Hampton JL, Phipps PM, Grabau EA. Enhancing resistance to Sclerotinia minor in peanut by expressing a barley oxalate oxidase gene. Plant Physiol 2005; 137(4): 1354-62.
[http://dx.doi.org/10.1104/pp.104.057232] [PMID: 15778458]
[74]
Wisser RJ, Balint-Kurti PJ, Nelson RJ. The genetic architecture of disease resistance in maize: a synthesis of published studies. Phytopathology 2006; 96(2): 120-9.
[http://dx.doi.org/10.1094/PHYTO-96-0120] [PMID: 18943914 ]
[75]
Ilyas M, Muhammad S, Naqvi S, Mahmood T. In silico analysis of transcription factor binding sites in promoters of germin-like protein genes in rice. 2016; 38(4): 863-76.
[http://dx.doi.org/10.2298/ABS151116076I]
[76]
Druka A, Kudrna D, Kannangara CG, von Wettstein D, Kleinhofs A. Physical and genetic mapping of barley (Hordeum vulgare) germin-like cDNAs. Proc Natl Acad Sci USA 2002; 99(2): 850-5.
[http://dx.doi.org/10.1073/pnas.022627999] [PMID: 11792854]
[77]
Liu B, Li S. ProtDet-CCH: Protein remote homology detection by combining Long Short-Term Memory and ranking methods. IEEE/ACM Trans Comput Biol Bioinformatics 2018; 9: 1-1.
[http://dx.doi.org/10.1109/TCBB.2018.2789880]
[78]
Chen J, Long R, Wang X, Liu B, Chou K-C. dRHP-PseRA: Detecting remote homology proteins using profile-based pseudo protein sequence and rank aggregation. Sci Rep 2016; 6: 32333.
[79]
Rätsch G, Sonnenburg S, Schäfer C. Learning interpretable SVMs for biological sequence classification. BMC Bioinformatics 2006; 7(Suppl. 1): S9.
[80]
Chen J, Guo M, Li S, Liu B. ProtDec-LTR2.0: An improved method for protein remote homology detection by combining pseudo protein and supervised Learning to Rank. Bioinformatics 2017; 33: 3473-6.
[http://dx.doi.org/10.1093/bioinformatics/btx429]
[81]
Davidson RM, Reeves PA, Manosalva PM, Leach JE. Germins: A diverse protein family important for crop improvement. Plant Sci 2009; 177: 499-510.
[http://dx.doi.org/10.1016/j.plantsci.2009.08.012]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 15
ISSUE: 1
Year: 2020
Page: [17 - 33]
Pages: 17
DOI: 10.2174/1574893614666190722165130
Price: $65

Article Metrics

PDF: 19
HTML: 4
EPUB: 1
PRC: 1