Abstract
The GHMP (galactokinase, homoserine kinase, mevalonate kinase and phosphomevalonate kinase) kinase gene superfamily is a unique class of ATP-dependent enzymes. It plays a role in the metabolism of carbohydrate, biosynthesis of isoprenes, amino acids and nucleotide sugars. However, this important gene family has not been characterized in wheat (Triticum aestivum L.). In this study, total forty-seven putative GHMP kinase sequences were identified in wheat (Triticum aestivum L.) genome. Physicochemical properties, motif prediction, conserved domain and exon-intron configuration analyses revealed that these sequences were distributed in 10 subfamilies. Promoter analysis of GHMP kinase sequences showed that the cis-acting regulatory elements are involved in diverse functions such as light, stress, hormone and metabolism responsiveness, tissue-specific activation, circadian control, binding site and cell cycle regulation. Phylogenetic relationship with other monocot species has further strengthened the subfamily grouping pattern. The heat map presented by transcriptomic data analysis revealed that 25 and 12 genes showed significant differential expression against the abiotic and biotic stresses, respectively. The expression of selected genes was validated under abiotic stress conditions viz., heat, drought and their combination by qRT-PCR analysis. In conclusion, the present study provides novel information, thus enhances our understanding of the GHMP kinase gene family in wheat. The information obtained will be valuable in selecting potential candidate genes in wheat for developing cultivars with improved tolerance against biotic and abiotic stresses.
Similar content being viewed by others
References
Appels R, Eversole K, Feuillet C, Keller B, Rogers J, Stein N, Pozniak CJ, Choulet F, Distelfeld A, Poland J, Ronen G (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361(6403):eaar7191
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37(suppl_2):W202–W208
Behmüller R, Kavkova E, Düh S, Huber CG, Tenhaken R (2016) The role of arabinokinase in arabinose toxicity in plants. Plant J 87(4):376–390
Bork P, Sander C, Valencia A (1993) Convergent evolution of similar enzymatic function on different protein folds: the hexokinase, ribokinase, and galactokinase families of sugar kinases. Protein Sci 2(1):31–40
Brenchley R, Spannagl M, Pfeifer M, Barker GL, D’Amore R, Allen AM, McKenzie N, Kramer M, Kerhornou A, Bolser D, Kay S (2012) Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491(7426):705–710
Brewer HC, Hawkins ND, Hammond-Kosack KE (2014) Mutations in the Arabidopsis homoserine kinase gene DMR1 confer enhanced resistance to Fusarium culmorum and F. graminearum. BMC Plant Biol 14(1):317
De Castro E, Sigrist CJ, Gattiker A, Bulliard V, Langendijk-Genevaux PS, Gasteiger E, Bairoch A, Hulo N (2006) ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res 34(suppl_2):W362–W365
Devos KM, Dubcovsky J, Dvořák J, Chinoy CN, Gale MD (1995) Structural evolution of wheat chromosomes 4A, 5A, and 7B and its impact on recombination. Theor Appl Genet 91(2):282–288
Egert A, Peters S, Guyot C, Stieger B, Keller F (2012) An Arabidopsis T-DNA insertion mutant for galactokinase (AtGALK, At3g06580) hyperaccumulates free galactose and is insensitive to exogenous galactose. Plant Cell Physiol 53(5):921–929
Flowerika AA, Kumar J, Thakur N, Pandey A, Pandey AK, Upadhyay SK, Tiwari S (2016) Characterization and expression analysis of phytoene synthase from bread wheat (Triticum aestivum L.). PLoS One 11(10):e0162443
Fu Z, Wang M, Potter D, Miziorko HM, Kim JJ (2002) The structure of a binary complex between a mammalian mevalonate kinase and ATP insights into the reaction mechanism and human inherited disease. J Biol Chem 277(20):18134–18142
Glover NM, Redestig H, Dessimoz C (2016) Homoeologs: what are they and how do we infer them? Trends Plant Sci 21(7):609–621
Guo D, Zhou Y, Li HL, Zhu JH, Wang Y, Chen XT, Peng SQ (2017) Identification and characterization of the abscisic acid (ABA) receptor gene family and its expression in response to hormones in the rubber tree. Sci Rep 7:45157
Han Z, Liu Y, Deng X, Liu D, Liu Y, Hu Y, Yan Y (2019) Genome-wide identification and expression analysis of expansin gene family in common wheat (Triticum aestivum L.). BMC Genomics 20(1):1–9
Hernandez-Garcia CM, Finer JJ (2014) Identification and validation of promoters and cis-acting regulatory elements. Plant Sci 217:109–119
Holden HM, Thoden JB, Timson DJ, Reece RJ (2004) Galactokinase: structure, function and role in type II galactosemia. Cell Mol Life Sci 61(19–20):2471–2484
Hu B, Jin J, Guo A, Zhang H, Luo J (2015) Genome analysis GSDS 20: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297
Jiang Y, Duan Y, Yin J, Ye S, Zhu J, Zhang F, Lu W, Fan D, Luo K (2014) Genome-wide identification and characterization of the Populus WRKY transcription factor family and analysis of their expression in response to biotic and abiotic stresses. J Exp Bot 65(22):6629–6644
Kersey PJ, Allen JE, Allot A, Barba M, Boddu S, Bolt BJ, Carvalho-Silva D, Christensen M, Davis P, Grabmueller C, Kumar N (2018) Ensembl Genomes 2018: an integrated omics infrastructure for non-vertebrate species. Nucleic Acids Res 46(D1):D802–D808
Krishna SS, Zhou T, Daugherty M, Osterman A, Zhang H (2001) Structural basis for the catalysis and substrate specificity of homoserine kinase. Biochemistry 40(36):10810–10818
Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19(9):1639–1645
Lee M, Martin MN, Hudson AO, Lee J, Muhitch MJ, Leustek T (2005) Methionine and threonine synthesis are limited by homoserine availability and not the activity of homoserine kinase in Arabidopsis thaliana. Plant J 41(5):685–696
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30(1):325–327
Letunic I, Bork P (2019) Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 47(W1):W256–W259
Liu Z, Xin M, Qin J, Peng H, Ni Z, Yao Y, Sun Q (2015) Temporal transcriptome profiling reveals expression partitioning of homeologous genes contributing to heat and drought acclimation in wheat (Triticum aestivum L.). BMC Plant Biol 15(1):152
Marcussen T, Sandve SR, Heier L, Spannagl M, Pfeifer M, Jakobsen KS, Wulff BB, Steuernagel B, Mayer KF, Olsen OA, International Wheat Genome Sequencing Consortium (2014) Ancient hybridizations among the ancestral genomes of bread wheat. Science 345(6194):1250092
Miziorko HM (2011) Enzymes of the mevalonate pathway of isoprenoid biosynthesis. Arch Biochem Biophys 505(2):131–143
Petersen G, Seberg O, Yde M, Berthelsen K (2006) Phylogenetic relationships of Triticum and Aegilops and evidence for the origin of the A, B, and D genomes of common wheat (Triticum aestivum). Mol Phylogenet Evol 39(1):70–82
Petersen TN, Brunak S, Von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8(10):785
Pieslinger AM, Hoepflinger MC, Tenhaken R (2010) Cloning of glucuronokinase from Arabidopsis thaliana, the last missing enzyme of the myo-inositol oxygenase pathway to nucleotide sugars. J Biol Chem 285(5):2902–2910
Ramírez-González RH, Borrill P, Lang D, Harrington SA, Brinton J, Venturini L, Davey M, Jacobs J, Van Ex F, Pasha A, Khedikar Y (2018) The transcriptional landscape of polyploid wheat. Science 361(6403):eaar6089
Romanowski MJ, Bonanno JB, Burley SK (2002) Crystal structure of the Streptococcus pneumoniae phosphomevalonate kinase, a member of the GHMP kinase superfamily. Proteins 47(4):568–571
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C T method. Nat Protoc 3(6):1101–1108
Shivani, Kaur N, Awasthi P, Tiwari S (2018) Identification and expression analysis of genes involved in somatic embryogenesis of banana. Acta Physiol Plant 40(8):139
Timson DJ (2007) GHMP kinases-structures, mechanisms and potential for therapeutically relevant inhibition. Curr Enzym Inhib 3(1):77–94
Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and cufflinks. Nat Protoc 7(3):562–578
Tsay YH, Robinson GW (1991) Cloning and characterization of ERG8, an essential gene of Saccharomyces cerevisiae that encodes phosphomevalonate kinase. Mol Cell Biol 11(2):620–631
van Damme M, Zeilmaker T, Elberse J, Andel A, de Sain-van der Velden M, van den Ackerveken G (2009) Downy mildew resistance in Arabidopsis by mutation of homoserine kinase. Plant Cell 21(7):2179–2189
Venkateshwaran M, Jayaraman D, Chabaud M, Genre A, Balloon AJ, Maeda J, Forshey K, den Os D, Kwiecien NW, Coon JJ, Barker DG (2015) A role for the mevalonate pathway in early plant symbiotic signaling. PNAS 112(31):9781–9786
Wada T, Kuzuyama T, Satoh S, Kuramitsu S, Yokoyama S, Unzai S, Tame JR, Park SY (2003) Crystal structure of 4-(cytidine 5′-diphospho)-2-C-methyl-d-erythritol kinase, an enzyme in the non-mevalonate pathway of isoprenoid synthesis. J Biol Chem 278(32):30022–30027
Xiao W, Chang H, Zhou P, Yuan C, Zhang C, Yao R, Lu X, Cai L, He Z, Hu R, Guo X (2015) Genome-wide identification, classification and expression analysis of GHMP genes family in Arabidopsis thaliana. Plant Syst Evol 301(8):2125–2140
Xiao W, Hu S, Zhou X, Yao R, Luo J, Yuan C, Chang H, Zhang C, Huang J, Li J, Liu S (2017) A glucuronokinase gene in Arabidopsis, AtGlcAK, is involved in drought tolerance by modulating sugar metabolism. Plant Mol Biol Report 35(2):298–311
Yang D, Shipman LW, Roessner CA, Scott AI, Sacchettini JC (2002) Structure of the Methanococcus jannaschii mevalonate kinase, a member of the GHMP kinase superfamily. J Biol Chem 277(11):9462–9467
Yang T, Bar-Peled L, Gebhart L, Lee SG, Bar-Peled M (2009) Identification of galacturonic acid-1-phosphate kinase, a new member of the GHMP kinase superfamily in plants, and comparison with galactose-1-phosphate kinase. J Biol Chem 284(32):21526–21535
Yu CS, Chen YC, Lu CH, Hwang JK (2006) Prediction of protein subcellular localization. Proteins 64(3):643–651
Zhang H, Yang Y, Wang C, Liu M, Li H, Fu Y, Wang Y, Nie Y, Liu X, Ji W (2014) Large-scale transcriptome comparison reveals distinct gene activations in wheat responding to stripe rust and powdery mildew. BMC Genomics 15(1):898
Zhou T, Daugherty M, Grishin NV, Osterman AL, Zhang H (2000) Structure and mechanism of homoserine kinase: prototype for the GHMP kinase superfamily. Structure 8(12):1247–1257
Acknowledgements
We are grateful for the support and facilities provided by the National Agri-Food Biotechnology Institute (NABI), Mohali. The authors are thankful to DBT e-Library Consortium (DeLCON). N.T. and F. are thankful to the ICMR and DBT for a Senior Research Fellowship and Panjab University, Chandigarh, for Ph.D. registration.
Funding
This work was supported by NABI core grant. The funders had no role in the design of the study; in the collection, analyses and interpretation of data; in the writing of the manuscript; or in the decision to publish the results.
Author information
Authors and Affiliations
Contributions
S.T. conceived and designed the research. N.T. performed computational analysis. N.T. and P.K.S. performed transcriptomics data analysis. N.T. and F. contributed to the qRT-PCR experiments. N.T., F., P.K.S and K.K. analysed the data. N.T. and S.T wrote and revised the manuscript.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Key Message
The GHMP (galactokinase, homoserine kinase, mevalonate kinase and phosphomevalonate) kinase gene superfamily in wheat is unique as it consists of 10 different subfamilies, with each subfamily members being involved in different functions. The gene structural and functional features of the wheat-derived forty-seven GHMP kinases were predicted using various bioinformatics tools. Results from RNA-seq data analysis in this work will be helpful in selecting candidate genes for developing wheat varieties with enhanced tolerance against biotic and abiotic stresses.
Rights and permissions
About this article
Cite this article
Thakur, N., Flowerika, Singh, P.K. et al. Genome-Wide Identification and Analysis of GHMP Kinase Gene Superfamily in Bread Wheat (Triticum aestivum L.). Plant Mol Biol Rep 39, 455–470 (2021). https://doi.org/10.1007/s11105-020-01259-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-020-01259-2