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Genome-wide identification, characterization, and evolutionary analysis of NBS-encoding resistance genes in barley

Abstract

In this study, a systematic analysis of Nucleotide-Binding Site (NBS) disease resistance (R) gene family in the barley, Hordeum vulgare L. cv. Bowman, genome was performed. Using multiple computational analyses, we could identify 96 regular NBS-encoding genes and characterize them on the bases of structural diversity, conserved protein signatures, genomic distribution, gene duplications, differential expression, selection pressure, codon usage, regulation by microRNAs and phylogenetic relationships. Depending on the presence or absence of CC and LRR domains; the identified NBS genes were assigned to four distinct groups; NBS–LRR (53.1%), CC-NBS–LRR (14.6%), NBS (26%), and CC-NBS (6.3%). NBS-associated domain analysis revealed the presence of signal peptides, zinc fingers, diverse kinases, and other structural features. Eighty-five of the identified NBS-encoding genes were mapped onto the seven barley chromosomes, revealing that 50% of them were located on chromosomes 7H, 2H, and 3H, with a tendency of NBS genes to be clustered in the distal telomeric regions of the barley chromosomes. Nine gene clusters, representing 22.35% of total mapped barley NBS-encoding genes, were found, suggesting that tandem duplication stands for an important mechanism in the expansion of this gene family in barley. Phylogenetic analysis determined 31 HvNBS orthologs from rice and Brachypodium. 87 out of 96 HvNBSs were supported by expression evidence, exhibiting various and quantitatively uneven expression patterns across distinct tissues, organs, and development stages. Fourteen potential miRNA-R gene target pairs were further identified, providing insight into the regulation of NBS genes expression. These findings offer candidate target genes to engineer disease-resistant barley genotypes, and promote our understanding of the evolution of NBS-encoding genes in Poaceae crops.

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Abbreviations

CC:

Coiled-coil (domain)

IBSC:

The International Barley Genome Sequencing Consortium

LRR:

Leucine-rich repeat (domain)

NBS:

Nucleotide-binding site (domain)

NLR:

NOD-like receptors

miRNA:

MicroRNAs

TIR:

Toll-interleukin-1 receptor (domain)

References

  • Abdel-Ghani AH, Al-Ameiri NS, Karajeh MR (2008) Resistance of barley landraces and wild barley populations to powdery mildew in Jordan. Phytopathol Mediterr 47:92–97

    Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    CAS  Article  Google Scholar 

  • Andersen EJ, Ali S, Reese RN, Yen Y, Neupane S, Nepal MP (2016) Diversity and evolution of disease resistance genes in Barley (Hordeum vulgare L.). Evol Bioinform 12:99–108. https://doi.org/10.4137/EBO.S38085

    CAS  Article  Google Scholar 

  • Badr A, Müller K, Schäfer-Pregl R, El Rabey H, Effgen S, Ibrahim HH, Pozzi C, Rohde W, Salamini F (2000) On the origin and domestication history of Barley (Hordeum vulgare). Mol Biol Evol 17:499–510

    CAS  Article  Google Scholar 

  • Bai B, Shi B, Hou N, Cao Y, Meng Y, Bian H, Zhu M, Han N (2017) microRNAs participate in gene expression regulation and phytohormone cross-talk in barley embryo during seed development and germination. BMC Plant Biol 17:150. https://doi.org/10.1186/s12870-017-1095-2

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. In: Proceedings of the second international conference on intelligent systems for molecular biology, AAAI Press, Menlo Park, pp 28–36

  • Biruma M, Martin T, Fridborg I, Okori P, Dixelius C (2012) Two loci in sorghum with NB-LRR encoding genes confer resistance to Colletotrichum sublineolum. Theor Appl Genet 124:1005–1015

    CAS  Article  Google Scholar 

  • Blanc G, Wolfe KH (2004) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16:1679–1691

    CAS  Article  Google Scholar 

  • Bonardi V, Tang S, Stallmann A, Roberts M, Cherkis K, Dangl JL (2011) Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors. Proc Natl Acad Sci USA 108:16463–16468

    CAS  Article  Google Scholar 

  • Borrelli GM, Mazzucotelli E, Marone D, Crosatti C, Michelotti V, Valè G, Mastrangelo AM (2018) Regulation and evolution of NLR genes: a close interconnection for plant immunity. Int J Mol Sci 19:1662. https://doi.org/10.3390/ijms19061662

    Article  PubMed Central  Google Scholar 

  • Buschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der Lee T, Diergaarde P, Groenendijk J, Topsch S, Vos P, Salamini F, Schulze-Lefert P (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695–705

    CAS  Article  Google Scholar 

  • Cantalapiedra CP, Boudiar R, Casas AM, Igartua E, Contreras-Moreira B (2015) BARLEYMAP: physical and genetic mapping of nucleotide sequences and annotation of surrounding loci in barley. Mol Breed 35:13. https://doi.org/10.1007/s11032-015-0253-1

    CAS  Article  Google Scholar 

  • Carlson M (1999) Glucose repression in yeast. Curr Opin Microbiol 2:202–207

    CAS  Article  Google Scholar 

  • Cheng X, Jiang H, Zhao Y, Qian Y, Zhu S, Cheng B (2010) A genomic analysis of disease-resistance genes encoding nucleotide binding sites in Sorghum bicolor. Genet Mol Biol 33:292–297

    CAS  Article  Google Scholar 

  • Cheng Y, Li X, Jiang H, Ma W, Miao W, Yamada T, Zhang M (2012) Systematic analysis and comparison of nucleotide-binding site disease resistance genes in maize. FEBS J 279:2431–2443

    CAS  Article  Google Scholar 

  • Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host–microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

    CAS  Article  Google Scholar 

  • Colmsee C, Beier S, Himmelbach A, Schmutzer T, Stein N, Scholz U, Mascher M (2015) BARLEX—the Barley draft genome explorer. Mol Plant 8:964–966. https://doi.org/10.1016/j.molp.2015.03.009

    CAS  Article  PubMed  Google Scholar 

  • Collins N, Drake J, Ayliffe M, Sun Q, Ellis J, Hulbert S, Pryor T (1999) Molecular characterization of the maize Rp1-D rust resistance haplotype and its mutants. Plant Cell 11:1365–1376

    CAS  Article  Google Scholar 

  • Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res. https://doi.org/10.1093/nar/gkr319

    Article  PubMed  PubMed Central  Google Scholar 

  • Dangl JL, Jones JDG (2001) Plant pathogens and integrated defense responses to infection. Nature 411:826–833

    CAS  Article  Google Scholar 

  • Das SS, Karmakar P, Nandi AK, Sanan-Mishra N (2015) Small RNA mediated regulation of seed germination. Front Plant Sci 6:828. https://doi.org/10.3389/fpls.2015.00828.eCollection2015

    Article  PubMed  PubMed Central  Google Scholar 

  • Duret L (2002) Evolution of synonymous codon usage in metazoans. Curr Opin Genet Dev 12:640–649

    CAS  Article  Google Scholar 

  • Ellis JG (2016) Integrated decoys and effector traps: how to catch a plant pathogen. BMC Biol 14:13. https://doi.org/10.1186/s12915-016-0235-8

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Fei Q, Zhang Y, Xia R, Meyers BC (2016) Small RNAs add zing to the zig-zag-zig model of plant defenses. Mol Plant Microbe Interact 29:165–169

    CAS  Article  Google Scholar 

  • Flor HH (1971) Current status of the gene-for-gene concept. Ann Rev Phytopathol 9:275–296

    Article  Google Scholar 

  • Friedman AR, Baker BJ (2007) The evolution of resistance genes in multiprotein plant resistance systems. Curr Opin Genet Dev 17:493–499

    CAS  Article  Google Scholar 

  • Gissot L, Polge C, Jossier M, Girin T, Bouly J-P, Kreis M, Thomas M (2006) AKINβγ contributes to SnRK1 heterotrimeric complexes and interacts with two proteins implicated in plant pathogen resistance through its KIS/GBD sequence. Plant Physiol 142:931–944

    CAS  Article  Google Scholar 

  • Gu Z, Cavalcanti A, Chen FC, Bouman P, Li WH (2002) Extent of gene duplication in the genomes of Drosophila, nematode and yeast. Mol Biol Evol 19:256–262

    CAS  Article  Google Scholar 

  • Gu L, Si W, Zhao L, Yang S, Zhang X (2015) Dynamic evolution of NBS–LRR genes in bread wheat and its progenitors. Mol Genet Genom 290:727–738

    CAS  Article  Google Scholar 

  • Guo HS, Xie Q, Fei JF, Chua NH (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17:1376–1386

    CAS  Article  Google Scholar 

  • Halterman DA, Wise RP (2004) A single-amino acid substitution in the sixth leucine-rich repeat of barley MLA6 and MLA13 alleviates dependence on RAR1 for disease resistance signalling. Plant J 38:215–226

    CAS  Article  Google Scholar 

  • Holub EB (2001) The arms race is ancient history in Arabidopsis, the wildflower. Nat Rev Genet 2:516–527

    CAS  Article  Google Scholar 

  • Habachi-Houimli Y, Khalfallah Y, Makni H, Makni M, Bouktila D (2016) Large-scale bioinformatic analysis of the regulation of the disease resistance NBS gene family by microRNAs in Poaceae. C R Biol 339:347–356

    Article  Google Scholar 

  • Ingvarsson PK (2010) Natural selection on synonymous and nonsynonymous mutations shapes patterns of polymorphism in Populus tremula. Mol Biol Evol 27:650–660

    CAS  Article  Google Scholar 

  • International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800. https://doi.org/10.1038/nature03895

    CAS  Article  Google Scholar 

  • Jia J, Zhao S, Kong X, Li Y, Zhao G, He W, Appels R, Pfeifer M, Tao Y, Zhang X, Jing R, Zhang C, Ma Y, Gao L, Gao C, Spannagl M, Mayer KFX, Li D, Pan S, Zheng F, Hu Q, Xia X, Li J, Liang Q, Chen J, Wicker T, Gou C, Kuang H, He G, Luo Y, Keller B, Xia Q, Lu P, Wang J, Zou H, Zhang R, Xu J, Gao J, Middleton C, Quan Z, Liu G, Wang J, International Wheat Genome Sequencing Consortium, Yang H, Liu X, He Z, Mao L, Wang J (2013) Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 496:91–95

    CAS  Article  Google Scholar 

  • Joshi RJ, Nayak S (2013) Perspectives of genomic diversification and molecular recombination towards R-gene evolution in plants. Physiol Mol Biol Plants 19:1–9. https://doi.org/10.1007/s12298-012-0138-2

    CAS  Article  PubMed  Google Scholar 

  • Kawabe A, Miyashita NT (2003) Patterns of codon usage bias in three dicot and four monocot plant species. Genes Genet Syst 78:343–352

    CAS  Article  Google Scholar 

  • Krattinger SG, Keller B (2016) Trapping the intruder—immune receptor domain fusions provide new molecular leads for improving disease resistance in plants. Genome Biol 17:23. https://doi.org/10.1186/s13059-016-0891-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Li J, Ding J, Zhang W, Zhang Y, Tang P, Chen J-Q, Tian D, Yang S (2010) Unique evolutionary pattern of numbers of gramineous NBS–LRR genes. Mol Genet Genom 283:427–438

    CAS  Article  Google Scholar 

  • Li F, Pignatta D, Bendix C, Brunkard JO, Cohn MM, Tung J, Sun H, Kumar P, Bakker B (2012) MicroRNA regulation of plant innate immune receptors. Proc Natl Acad Sci USA 109:1790–1795

    CAS  Article  Google Scholar 

  • Ling HQ, Zhao S, Liu D, Wang J, Sun H, Zhang C, Fan H, Li D, Dong L, Tao Y, Gao C, Wu H, Li Y, Cui Y, Guo X, Zheng S, Wang B, Yu K, Liang Q, Yang W, Lou X, Chen J, Feng M, Jian J, Zhang X, Luo G, Jiang Y, Liu J, Wang Z, Sha Y, Zhang B, Wu H, Tang D, Shen Q, Xue P, Zou S, Wang X, Liu X, Wang F, Yang Y, An X, Dong Z, Zhang K, Zhang X, Luo MC, Dvorak J, Tong Y, Wang J, Yang H, Li Z, Wang D, Zhang A, Wang J (2013) Draft genome of the wheat A-genome progenitor Triticum urartu. Nature 496:87–90

    CAS  Article  Google Scholar 

  • Liu Q, Feng Y, Zhao X, Dong H, Xue Q (2004) Synonymous codon usage bias in Oryza sativa. Plant Sci 167:101–105

    CAS  Article  Google Scholar 

  • Liu H, He R, Zhang H, Huang Y, Tian M, Zhang J (2010) Analysis of synonymous codon usage in Zea mays. Mol Biol Rep 37:677–684

    CAS  Article  Google Scholar 

  • Liu H, Huang Y, Du X, Chen Z, Zeng X, Chen Y, Zhang H (2012) Patterns of synonymous codon usage bias in the model grass Brachypodium distachyon. Genet Mol Res 11:4695–4706

    CAS  Article  Google Scholar 

  • Loveland JE, Gilbert JG, Griffiths E, Harrow JL (2012) Community gene annotation in practice. J Biol Databases Curation 2012:bas009. https://doi.org/10.1093/database/bas009

    CAS  Article  Google Scholar 

  • Lozano R, Hamblin MT, Prochnik S, Jannink JL (2015) Identification and distribution of the NBS–LRR gene family in the Cassava genome. BMC Genom 16:360. https://doi.org/10.1186/s12864-015-1554-9

    CAS  Article  Google Scholar 

  • Lukasik E, Takken FL (2009) STANDing strong, resistance proteins instigators of plant defence. Curr Opin Plant Biol 12:427–436

    CAS  Article  Google Scholar 

  • Luo Y, Caldwell KS, Wroblewski T, Wright ME, Michelmore RW (2009) Proteolysis of a negative regulator of innate immunity is dependent on resistance genes in tomato and Nicotiana benthamiana and induced by multiple bacterial effectors. Plant Cell 21:2458–2472

    CAS  Article  Google Scholar 

  • Marone D, Russo MA, Laidò G, De Leonardis AM, Mastrangelo AM (2013) Plant nucleotide binding site-leucine-rich repeat (NBS–LRR) genes: active guardians in host defense responses. Int J Mol Sci 14:7302–7326

    CAS  Article  Google Scholar 

  • Martin T, Biruma M, Fridborg I, Okori P, Dixelius C (2011) A highly conserved NB-LRR encoding gene cluster effective against Setosphaeria turcica in sorghum. BMC Plant Biol 11:151. https://doi.org/10.1186/1471-2229-11-151

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Meyers BC, Dickerman AW, Michelmore RW, Sivaramakrishnan S, Sobral BW, Yong ND (1999) Plant disease resistance genes encode members of an ancient and diverse protein family within nucleotide-binding superfamily. Plant J 20:317–332

    CAS  Article  Google Scholar 

  • Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS–LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834

    CAS  Article  Google Scholar 

  • Meyers BC, Kaushik S, Nandety RS (2005) Evolving disease resistance genes. Curr Opin Plant Biol 8:129–134

    CAS  Article  Google Scholar 

  • Mirlohi A, Brueggeman R, Drader T, Nirmala J, Steffenson BJ, Kleinhofs A (2008) Allele sequencing of the barley stem rust resistance gene Rpg1 identifies regions relevant to disease resistance. Phytopathology 98:910–918

    CAS  Article  Google Scholar 

  • Mun JH, Yu HJ, Park S, Park BS (2009) Genome-wide identification of NBS-encoding resistance genes in Brassica rapa. Mol Genet Genom 282:617–631

    CAS  Article  Google Scholar 

  • Naqvi AR, Choudhury NR, Mukherjee SK, Haq QM (2011) In silico analysis reveals that several tomato microRNA/microRNA* sequences exhibit propensity to bind to tomato leaf curl virus (ToLCV) associated genomes and most of their encoded open reading frames (ORFs). Plant Physiol Biochem 49:13–17

    CAS  Article  Google Scholar 

  • Nevo E (1992) Origin, evolution, population genetics, and resources for breeding of wild barley, Hordeum spontaneum, in the fertile crescent. In: Showrey PR (ed) Barley, genetics, biochemistry, molecular biology and biotechnology. C.A.B. International, Wallingford, pp 19–43

    Google Scholar 

  • Nevo E, Fu Y-B, Pavlicek T, Khalifa S, Tavasi M, Beiles A (2012) Evolution of wild cereals during 28 years of global warming in Israel. Proc Natl Acad Sci USA 109:3412–3415

    CAS  Article  Google Scholar 

  • Nikovics K, Blein T, Peaucelle A, Ishida T, Morin H, Aida M, Laufs P (2006) The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell 18:2929–2945

    CAS  Article  Google Scholar 

  • Nobuta K, Ashfield T, Kim S, Innes RW (2005) Diversification of non-TIR class NB-LRR genes in relation to whole-genome duplication events in Arabidopsis. Mol Plant Microbe Interact 18:103–109

    CAS  Article  Google Scholar 

  • Pan Q, Wendel J, Fluhr R (2000) Divergent evolution of plant NBS–LRR resistance gene homologues in dicot and cereal genomes. J Mol Evol 50:203–213

    CAS  Article  Google Scholar 

  • Porter BW, Paidi M, Ming R, Alam M, Nishijima WT, Zhu YJ (2009) Genome-wide analysis of Carica papaya reveals a small NBS resistance gene family. Mol Genet Genom 281:609–626

    CAS  Article  Google Scholar 

  • Ruane J, Sonnino A (2007) Marker-assisted selection as a tool for genetic improvement of crops, livestock, forestry and fish in developing countries: an overview of the issues. In: Guimaraes E, Ruane J, Sonnino A, Scherf B, Dargie JD (eds) Marker-assisted selection: current status and future perspectives in crops, livestock, forestry and fish. Food and Agriculture Organization of the United Nations, Rome, ISBN: 978-92-5-105717-9

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  Google Scholar 

  • Sarris PF, Cevik V, Dagdas G, Jones JDG, Krasileva KV (2016) Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens. BMC Biol 14:8. https://doi.org/10.1186/s12915-016-0228-7

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183

    CAS  Article  Google Scholar 

  • Schulte D, Close TJ, Graner A, Langridge P, Matsumoto T, Muehlbauer G, Sato K, Schulman AH, Waugh R, Wise RP, Stein N (2009) The International Barley Sequencing Consortium—at the threshold of efficient access to the barley genome. Plant Physiol 149:142–147

    CAS  Article  Google Scholar 

  • Seeholzer S, Tsuchimatsu T, Jordan T, Bieri S, Pajonk S, Yang W, Jahoor A, Shimizu KK, Keller B, Schulze-Lefert P (2010) Diversity at the Mla powdery mildew resistance locus from cultivated barley reveals sites of positive selection. Mol Plant Microbe Interact 23:497–509

    CAS  Article  Google Scholar 

  • Shivaprasad PV, Chen HM, Patel K, Bond DM, Santos BA, Baulcombe DC (2012) A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24:859–874

    CAS  Article  Google Scholar 

  • Sueoka N (1999a) Translation-coupled violation of Parity Rule 2 in human genes is not the cause of heterogeneity of the DNA G + C content of third codon position. Gene 238:53–58

    CAS  Article  Google Scholar 

  • Sueoka N (1999b) Two aspects of DNA base composition: G + C content and translation-coupled deviation from intra-strand rule of A = T and G = C. J Mol Evol 49:49–62

    CAS  Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Steecher G, NeiMand Kumar S (2011) MEGA: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    CAS  Article  Google Scholar 

  • Tan S, Wu S (2012) Genome wide analysis of nucleotide-binding site disease resistance genes in Brachypodium distachyon. Comp Funct Genom. https://doi.org/10.1155/2012/418208 (Article ID 418208)

    Article  Google Scholar 

  • The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • The International Barley Genome Sequencing Consortium (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–716

    Article  Google Scholar 

  • The International Wheat Genome Sequencing Consortium (2014) A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345:1251788. https://doi.org/10.1126/science.1251788

    CAS  Article  Google Scholar 

  • Thelander M, Olson MA, Ronne H (2004) Snf1-related protein kinase 1 is needed for growth in a normal day–night light cycle. EMBO J 23:1900–1910

    CAS  Article  Google Scholar 

  • Timmerman-Vaughan GM, Frew TJ, Weeden NF (2000) Characterization and linkage mapping of R-gene analogous DNA sequences in pea (Pisum sativum L.). Theor Appl Genet 101:241–247

    CAS  Article  Google Scholar 

  • van der Hoorn RAL, Kamoun S (2008) From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20:2009–2017

    Article  Google Scholar 

  • Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury J, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse Y, Allan AC, Bus V, Chagne D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouze P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel CE, Gutin A, Bumgarner RE, Gardiner SE, Skolnick M, Egholm M, Van de Peer Y, Salamini F, Viola R (2010) The genome of the domesticated apple (Malus × domestica Borkh). Nat Genet 42:833–839

    CAS  Article  Google Scholar 

  • Wan H, Yuan W, Bo K, Shen J, Pang X, Chen J (2013)) Genome-wide analysis of NBS-encoding disease resistance in Cucumis sativus and phylogenetic study of NBS-encoding genes in Cucurbitaceae crops. BMC Genom 14:109. https://doi.org/10.1186/1471-2164-14-109

    CAS  Article  Google Scholar 

  • Wicker T, Taudien S, Houben A, Keller B, Graner A, Platzer M, Stein N (2009) A whole-genome snapshot of 454 sequences exposes the composition of the barley genome and provides evidence for parallel evolution of genome size in wheat and barley. Plant J 59:712–722

    CAS  Article  Google Scholar 

  • Wright F (1990) The effective number of codons used in a gene. Gene 87:23–29

    CAS  Article  Google Scholar 

  • Yandell M, Ence D (2012) A beginner’s guide to eukaryotic genome annotation. Nat Rev Genet 13:329–342

    CAS  Article  Google Scholar 

  • Yang X, Wang J (2016) Genome-wide analysis of NBS–LRR genes in sorghum genome revealed several events contributing to NBS–LRR gene evolution in grass species. Evol Bioinform Online 12:9–21

    CAS  Article  Google Scholar 

  • Yang SH, Zhang XH, Yue JX, Tian DC, Chen JQ (2008) Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Genet Genom 280:187–198

    CAS  Article  Google Scholar 

  • Yoshimura S, Yamanouchi U, Katayose Y, Toki S, Wang ZX, Kono I, Kurata N, Yano M, Iwata N, Sasaki T (1998) Expression of Xa1 a bacterial blight-resistance gene in rice is induced by bacterial inoculation. Proc Natl Acad Sci USA 95:1663–1668

    CAS  Article  Google Scholar 

  • Yu J, Hu S, Wang J, Wong GK, Li S, Liu B, Deng Y et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296:79–92

    CAS  Article  Google Scholar 

  • Zeng XQ, Luo XM, Wang YL, Xu QJ, Bai LJ, Yuan HJ, Tashi N (2014) Transcriptome sequencing in a Tibetan barley landrace with high resistance to powdery mildew. Sci World J. https://doi.org/10.1155/2014/594579 (ID 594579)

    Article  Google Scholar 

  • Zhai J, Jeong DH, De Paoli E, Park S, Rosen BD et al (2011) MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev 25:2540–2553

    CAS  Article  Google Scholar 

  • Zhang R, Murat F, Pont C, Langin T, Salse J (2014) Paleo-evolutionary plasticity of plant disease resistance genes. BMC Genom 15:187

    Article  Google Scholar 

  • Zhang Y, Xia R, Kuang H, Meyers BC (2016) The diversification of plant defense genes directs the evolution of microRNAs that target them. Mol Biol Evol 33:2692–2705

    CAS  Article  Google Scholar 

  • Zhou T, Wang Y, Chen JQ, Araki H, Jing Z, Jiang K, Shen J, Tian D (2004) Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS–LRR genes. Mol Genet Genom 271:402–415

    CAS  Article  Google Scholar 

  • Zhu Q-H, Fan L, Liu Y, Xu H, Llewellyn D, Wilson I (2013) miR482 regulation of NBS–LRR defense genes during fungal pathogen infection in cotton. PLoS One 8:e84390. https://doi.org/10.1371/journal.pone.0084390

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Zipfel C (2008) Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20:10–16

    CAS  Article  Google Scholar 

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Acknowledgements

We gratefully acknowledge Abdennour Sébéi (Centre Régional de Recherches sur les Grandes Cultures, CRRGC, Béja, Tunisia), for his permanent logistic help. This study was financially supported by the Tunisian Ministry of Higher Education and Scientific Research.

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YHH analyzed data using bioinformatics tools, discussed the results and co-wrote the manuscript, under the guidance of DB. YK helped in performing bioinformatics analyses. MMK, HM, and MM helped to perform this study and contributed to discussions. DB designed this study, guided YHH in all analyses and discussions, and co-wrote the manuscript. All authors have read and approved the final manuscript.

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Correspondence to Dhia Bouktila.

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Habachi-Houimli, Y., Khalfallah, Y., Mezghani-Khemakhem, M. et al. Genome-wide identification, characterization, and evolutionary analysis of NBS-encoding resistance genes in barley. 3 Biotech 8, 453 (2018). https://doi.org/10.1007/s13205-018-1478-6

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Keywords

  • Hordeum vulgare
  • Nucleotide-binding site
  • Disease-resistance genes
  • Genome analysis