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Identification and Distribution of NBS-Encoding Resistance Genes of Dactylis glomerata L. and Its Expression Under Abiotic and Biotic Stress

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Abstract

Orchardgrass (Dactylis glomerata L.) is drought resistant and tolerant to barren landscapes, making it one of the most important forages for animal husbandry, as well as ecological restoration of rocky landscapes that are undergoing desertification. However, orchardgrass is susceptible to rust, which can significantly reduce its yield and quality. Therefore, understanding the genes that underlie resistance against rust in orchardgrass is critical. The evolution, cloning of plant disease resistance genes, and the analysis of pathogenic bacteria induced expression patterns are important contents in the study of interaction between microorganisms and plants. Genes with nucleotide binding site (NBS) structure are disease-resistant genes ubiquitous in plants and play an important role in plant attacks against various pathogens. Using sequence analysis and re-annotation, we identified 413 NBS resistance genes in orchardgrass. Similar to previous studies, NBS resistance genes containing TIR (toll/interleukin-1 receptor) domain were not found in orchardgrass. The NBS resistance genes can be divided into four types: NBS (up to 264 homologous genes, accounting for 64% of the total number of NBS genes in orchardgrass), NBS-LRR, CC-NBS, and CC-NBS-LRR (minimum of 26 homologous genes, only 6% of the total number of NBS genes in orchardgrass). These 413 NBS resistance genes were unevenly distributed across seven chromosomes where chromosome 5 had up to 99 NBS resistance genes. There were 224 (54%) NBS resistance genes expressed in different tissues (roots, stems, leaves, flowers, and spikes), and we did not detect expression for 45 genes (11%). The remaining 145 (35%) were expressed in some tissues. And we found that 11 NBS resistance genes were differentially expressed under waterlogging stress, 5 NBS resistance genes were differentially expressed under waterlogging and drought stress, and 1 NBS resistance was is differentially expressed under waterlogging and heat stress. Most importantly, we found that 65 NBS resistance genes were significantly expressed in different control groups. On the 7th day of inoculation, 23 NBS resistance genes were differentially expressed in high resistance materials alone, of which 7 NBS resistance genes regulate the “plant–pathogen interaction” pathway by encoding RPM1. At the same time, 2 NBS resistance genes that were differentially expressed in the high resistance material after inoculation were also differentially expressed in abiotic stress. In summary, the NBS resistance gene plays a crucial role in the resistance of orchardgrass to rust.

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References

  • Altschul SF, Madden TL et al (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ameline-Torregrosa C, Wang BB, O’Bleness MS et al (2008) Identification and characterization of nucleotide-binding site-leucine-rich repeat genes in the model plant Medicago truncatula. Plant Physiol 146(1):5–21

    CAS  PubMed  PubMed Central  Google Scholar 

  • Anders S (2010) HTSeq: analysing high-throughput sequencing data with Python. Bioinformatics 31(166):169

    Google Scholar 

  • Anders S, Pyl PT, Huber W (2015) HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31(2):166–169

    CAS  PubMed  Google Scholar 

  • Andrea C, Grant JJ et al (2004) Drought tolerance established by enhanced expression of the CC-NBS-LRR gene, ADR1, requires salicylic acid, EDS1 and ABI1. Plant J 38(5):810–822

    Google Scholar 

  • Bai JF, Pennill LA, Ning JC et al (2002) Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res 12(12):1871–1884

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bailey TL, Elkan C (1995) The value of prior knowledge in discovering motifs with MEME. Proc Int Conf Intell Syst Mol Biol 3:21–29

    CAS  PubMed  Google Scholar 

  • Bateman A et al (2000) The Pfam protein families database. Nucleic Acids Res 28(1):263–266

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bresson A, Jorge V, Dowkiw A et al (2011) Qualitative and quantitative resistances to leaf rust finely mapped within two nucleotide-binding site leucine-rich repeat (NBS-LRR)-rich genomic regions of chromosome 19 in poplar. New Phytol 192(1):151–163

    CAS  PubMed  Google Scholar 

  • Cheng X, Jiang H, Zhao Y et al (2010) A genomic analysis of disease-resistance genes encoding nucleotide binding sites in Sorghum bicolor. Genet Mol Biol 33(2):292–297

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng Y, Li X, Jiang H et al (2012) Systematic analysis and comparison of nucleotide-binding site disease resistance genes in maize. FEBS J 279(13):2431–2443

    CAS  PubMed  Google Scholar 

  • Dang JL, Jones JDG (2001) Plant pathogens and integrated defense responses to infection. Nature 411(6839):826–833

    Google Scholar 

  • Dempsey DMA, Silva H, Klessig DF (1998) Engineering disease and pest resistance in plants. Trends Microbiol 6(2):54–61

    CAS  PubMed  Google Scholar 

  • Ellis JG, Jones DA (2003) Plant disease resistance genes. Springer, New York

    Google Scholar 

  • Feng G, Huang L, Li J et al (2017) Comprehensive transcriptome analysis reveals distinct regulatory programs during vernalization and floral bud development of orchardgrass (Dactylis glomerata L). BMC Plant Biol 17:216

    PubMed  PubMed Central  Google Scholar 

  • Finn RD, Tate J, Mistry J et al (2016) The Pfam protein families database. Nucleic Acids Res 44:D281–D288

    Google Scholar 

  • France D et al (2014) The coffee genome provides insight into the convergent evolution of Caffeine biosynthesis. Science 345(6201):1181–1184

    Google Scholar 

  • Fujisawa M et al (2011) The map-based sequence of the rice genome. Nature 436(7052):793–800

    Google Scholar 

  • Gattani ML (1962) A technique for inoculating wheat with rusts for glass-house and test-tube culture. Nature 196(4850):190–191

    Google Scholar 

  • Grant MR, Godiard L, Straube E et al (1995) Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269(5225):843–846

    CAS  PubMed  Google Scholar 

  • Grant M, Brown I, Adams S et al (2000) The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J 23(4):441–450

    CAS  PubMed  Google Scholar 

  • Guo AY, Zhu QH, Chen X et al (2007) GSDS: a gene structure display server. Hereditas 29(8):1023–1026

    CAS  PubMed  Google Scholar 

  • Guo YL, Fitz J, Schneeberger K et al (2011) Genome-wide comparison of nucleotide-binding site-leucine-rich repeat-encoding genes in Arabidopsis. Plant Physiol 157(2):757–769

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hall TA (1999) Bio Edit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nuclear Acids Symp Ser 41:95–98

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Huang L, Yan H, Jiang X et al (2014a) Reference gene selection for quantitative real-time reverse-transcriptase PCR in orchardgrass subjected to various abiotic stresses. Gene 553:158–165

    CAS  PubMed  Google Scholar 

  • Huang L, Yan H, Fu C et al (2014b) Chloroplast DNA variation and genetic structure of Miscanthus sinensis in southwest China. Biochem Syst Ecol 58:132–138

    Google Scholar 

  • Huang L, Yan H, Zhao X et al (2015) Identifying differentially expressed genes under heat stress and developing molecular markers in orchardgrass (Dactylis glomerata L.) through transcriptome analysis. Mol Ecol Resour 15:1497–1509

    CAS  PubMed  Google Scholar 

  • Huang L, Feng G, Yan H et al (2019) Genome assembly provides insights into the genome evolution and flowering regulation of orchardgrass. Plant Biotechnol J 17:216

    Google Scholar 

  • Jafari A, Naseri H (2007) Genetic variation and correlation among yield and quality traits in cocksfoot. J Agric Sci 145(6):599–610

    CAS  Google Scholar 

  • Jane G et al (2003) Plant disease resistance genes. Annu Rev Plant Physiol Plant Mol Biol 48(48):575

    Google Scholar 

  • Ji Y, Chen P, Chen J et al (2018) Combinations of small RNA, RNA, and degradome sequencing uncovers the expression pattern of microRNA–mRNA pairs adapting to drought stress in leaf and root of Dactylis glomerata L. Int J Mol Sci 19:3114

    PubMed Central  Google Scholar 

  • Joobeur T et al (2010) The fusarium wilt resistance locus Fom-2 of melon contains a single resistance gene with complex features. Plant Journal 39(3):283–297

    Google Scholar 

  • Katoh K, Kuma K, Toh H et al (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33(2):511–518

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim D et al (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14(4):R36

    PubMed  PubMed Central  Google Scholar 

  • Kohler A, Rinaldi C, Duplessis S et al (2008) Genome-wide identification of NBS resistance genes in Populus trichocarpa. Plant Mol Biol 66(6):619–636

    CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C et al (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lancashire JA, Latch GC (1969) Some effects of stem rust (Puccinia graminis Pers.) on the growth of cocksfoot (Dactylis glomerata L. ‘Grasslands Apanui’). N Z J Agric Res 12(4):697–702

    Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9(4):357–359

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Ding J, Zhang W et al (2010) Unique evolutionary pattern of numbers of gramineous NBS–LRR genes. Mol Genet Genom 283(5):27–38

    Google Scholar 

  • Li X, Zhang Y et al (2017) Overexpression of pathogen-induced grapevine TIR-NB-LRR geneVaRGA1enhances disease resistance and drought and salt tolerance in Nicotiana benthamiana. Protoplasma 254(2):957–969

    CAS  PubMed  Google Scholar 

  • Liu J, Qiao L, Zhang X et al (2017) Genome-wide identification and resistance expression analysis of the NBS gene family in Triticum urartu. Genes Genom 39(6):1–11

    Google Scholar 

  • Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):550

    PubMed  PubMed Central  Google Scholar 

  • Lupas A (1997) Predicting coiled-coil regions in proteins. Curr Opin Struct Biol 7(3):388–393

    CAS  PubMed  Google Scholar 

  • Mace E, Tai S, Innes D et al (2014) The plasticity of NBS resistance genes in sorghum is driven by multiple evolutionary processes. BMC Plant Biol 14:253

    PubMed  PubMed Central  Google Scholar 

  • Marioni JC et al (2008) RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 18(9):1509–1517

    CAS  PubMed  PubMed Central  Google Scholar 

  • McHale L, Tan X, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7(4):1–11

    Google Scholar 

  • Meyers BC, Dickerman AW et al (1999) Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J 20:317–332

    CAS  PubMed  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(4):809–834

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meyers BC, Morgante M, Michelmore RW (2010) TIR-X and TIRNBS proteins: two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant genomes. Plant Journal 32(1):77–92

    Google Scholar 

  • Mortazavi A, Williams BA et al (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621

    CAS  PubMed  Google Scholar 

  • Moser LE, Buxton DR, Casler MD (1997) Cool-season forage grasses. Cambridge University Press, Cambridge

    Google Scholar 

  • Mur LA (1992) Functional homologs of the Arabidopsis RPM1 disease resistance gene in bean and pea. Plant Cell 4(11):1359–1369

    PubMed  PubMed Central  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R, Dubchak I et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457(7229):551–556

    CAS  PubMed  Google Scholar 

  • Plocik A, Layden J, Kesseli R (2004) Comparative analysis of NBS domain sequences of NBS-LRR disease resistance genes from sunflower, lettuce, and chicory. Mol Phylogenet Evol 31(1):153–163

    CAS  PubMed  Google Scholar 

  • Qi LL, Hulke BS, Vick BA, Gulya TJ (2011) Molecular mapping of the rust resistance gener4to a large NBS-LRR cluster on linkage group 13 of sunflower. Theor Appl Genet 123(2):351–358

    CAS  PubMed  Google Scholar 

  • Sanada Y, Tamura K, Yamada T et al (2010) Relationship between water-soluble carbohydrates in fall and spring and vigor of spring regrowth in orchardgrass. Crop Sci 50(50):380–390

    Google Scholar 

  • Seah S, Sivasithamparam K et al (1998) Cloning and characterisation of a family of disease resistance gene analogs from wheat and barley. Theor Appl Genet 97(5–6):937–945

    CAS  Google Scholar 

  • Spielmeyer W, Huang L, Bariana H, Laroche A, Gill BS, Lagudah ES (2000) Nbs-lrr sequence family is associated with leaf and stripe rust resistance on the end of homoeologous chromosome group 1s of wheat. Theor Appl Genet 101(7):1139–1144

    CAS  Google Scholar 

  • Staskawicz BJ, Ausubel FM, Baker BJ et al (1995) Molecular genetics of plant disease resistance. Scinece 268(5211):661–667

    CAS  Google Scholar 

  • Tamayo-Ordónez MC, Rodriguez-Zapata LC, Narváez-Zapata J et al (2016) Morphological features of different polyploids for adaptation and molecular characterization of CC-NBS-LRR and LEA gene families in Agave L. J Plant Physiol 195:80–94

    PubMed  Google Scholar 

  • Tameling WIL, Elzinga SDJ et al (2002) The tomato R gene products I-2 and Mi-1 are functional atp binding proteins with ATPase activity. Plant Cell 14(11):2929–2939

    CAS  PubMed  PubMed Central  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  Google Scholar 

  • Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25(9):1105–1111

    CAS  PubMed  PubMed Central  Google Scholar 

  • Traut TW (1994) The functions and consensus motifs of nine types of peptide segments that form different types of nucleotide-binding sites. Springer, New York

    Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009) RNA-Seq : a revolutionary tool for transcriptomics. Nat Rev Genet 10(1):57–63

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang GZ, Zuo FY, Zeng B et al (2011) Comparison on seed production of various orchardgrass. Anim Feed Sci 4:34–38

    Google Scholar 

  • Wang X, Richards J, Gross T et al (2013) The rpg4-mediated resistance to wheat stem rust (Puccinia graminis) in barley (Hordeum vulgare) requires Rpg5, a second NBS-LRR gene, and an actin depolymerization factor. Mol Plant-Microbe Int 26(4):407–418

    CAS  Google Scholar 

  • Xie W, Robins JG, Escribano S et al (2012) A genetic linkage map of tetraploid Orchardgrass (Dactylis glomerata L.) and quantitative trait loci for heading date. Genome 55(5):360–369

    CAS  PubMed  Google Scholar 

  • Xie W, Bushman BS, Ma Y et al (2014) Genetic Diversity and Variation in North American Orchardgrass (Dactylis glomerata L.) cultivars and breeding lines. Grassl Sci 60:185–193

    Google Scholar 

  • Yan GP, Chen XM, Line RF, Wellings CR (2003) Resistance gene-analog polymorphism markers co-segregating with the yr5 gene for resistance to wheat stripe rust. Theor Appl Genet 106(4):636–643

    CAS  PubMed  Google Scholar 

  • Yang X, Wang J (2015) Genome-wide analysis of NBS-LRR genes in sorghum genome revealed several events contributing to NBS-LRR gene evolution in grass species. Evol Bioinform 12(12):9–21

    CAS  Google Scholar 

  • Yang S, Zhang X, Yue J-X, Tian D, Chen J-Q (2008) Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Genet Genom 280(3):187–198

    CAS  Google Scholar 

  • Zhao XX, Huang LK, Zhang XQ et al (2014) Effects of heat acclimation on photosynthesis, antioxidant enzyme activities, and gene expression in orchardgrass under heat stress. Molecules 19(9):13564–13576

    PubMed  PubMed Central  Google Scholar 

  • Zhou T, Wang Y, Chen JQ et al (2004) Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol Genet Genom 271(4):402–415

    CAS  Google Scholar 

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Acknowledgements

This study was funded by the National Natural Science Foundation of China (31771866) and the Sichuan Province Breeding Research Grant and Modern Agricultural Industry System Sichuan Forage Innovation Team.

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Correspondence to Linkai Huang or Bing Zeng.

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Ren, S., Sun, M., Yan, H. et al. Identification and Distribution of NBS-Encoding Resistance Genes of Dactylis glomerata L. and Its Expression Under Abiotic and Biotic Stress. Biochem Genet 58, 824–847 (2020). https://doi.org/10.1007/s10528-020-09977-8

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