Skip to main content
SpringerLink
Log in

Phylogenetic and evolutionary analysis of NBS-encoding genes in Rutaceae fruit crops

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

The nucleotide-binding site leucine-rich repeat (NBS-LRR) genes are the largest class of disease resistance genes in plants. However, our understanding of the evolution of NBS-LRR genes in Rutaceae fruit crops is rather limited. We report an evolutionary study of 103 NBS-encoding genes isolated from Poncirus trifoliata (trifoliate orange), Citrus reticulata (tangerine) and their F1 progeny. In all, 58 of the sequences contained a continuous open reading frame. Phylogenetic analysis classified the 58 NBS genes into nine clades, eight of which were genus specific. This was taken to imply that most of the ancestors of these NBS genes evolved after the genus split. The motif pattern of the 58 NBS-encoding genes was consistent with their phylogenetic profile. An extended phylogenetic analysis, incorporating citrus NBS genes from the public database, classified 95 citrus NBS genes into six clades, half of which were genus specific. RFLP analysis showed that citrus NBS-encoding genes have been evolving rapidly, and that they are unstable when passed through an intergeneric cross. Of 32 NBS-encoding genes tracked by gene-specific PCR, 24 showed segregation distortion among a set of 94 F1 individuals. This study provides new insight into the evolution of Rutaceae NBS genes and their behaviour following an intergeneric cross.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ameline-Torregrosa C, Wang BB, O’Bleness MS, Deshpande S, Zhu H, Roe B, Young ND, Cannon SB (2008) Identification and characterization of nucleotide-binding site-leucine-rich repeat genes in the model plant Medicago truncatula. Plant Physiol 146:5–21

    Article  CAS  PubMed  Google Scholar 

  • Aswati Nair R, Thomas G (2007) Isolation, characterization and expression studies of resistance gene candidates (RGCs) from Zingiber spp. Theor Appl Genet 116:123–134

    Article  CAS  PubMed  Google Scholar 

  • Bai J, Pennill LA, Ning J, Lee SW, Ramalingam J, Webb CA, Zhao B, Sun Q, Nelson JC, Leach JE, Hulbert SH (2002) Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res 12:1871–1884

    Article  CAS  PubMed  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 

  • Belkhadir Y, Subramaniam R, Dangl JL (2004) Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr Opin Plant Biol 7:391–399

    Article  CAS  PubMed  Google Scholar 

  • Bernet GP, Fernandez-Ribacoba J, Carbonell EA, Asins MJ (2010) Comparative genome-wide segregation analysis and map construction using a reciprocal cross design to facilitate citrus germplasm utilization. Mol Breed 25:659–673

    Article  Google Scholar 

  • Cannon SB, Zhu HY, Baumgarten AM, Spangler R, May G, Cook DR, Young ND (2002) Diversity, distribution, and ancient taxonomic relationships within the TIR and non-TIR NBS-LRR resistance gene subfamilies. J Mol Evol 54:548–562

    Article  CAS  PubMed  Google Scholar 

  • Cheng YJ, Guo WW, Yi HL, Pang XM, Deng XX (2003) An efficient protocol for genomic DNA extraction from Citrus species. Plant Mol Biol Rep 21:177a–177g

    Article  Google Scholar 

  • Collins NC, Webb CA, Seah S, Ellis JG, Hulbert SH, Pryor A (1998) The isolation and mapping of disease resistance gene analogs in maize. Mol Plant Microbe Interact 11:968–978

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Deng Z, Huang S, Ling P, Chen C, Yu C, Weber CA, Moore GA, Gmitter FG (2000) Cloning and characterization of NBS-LRR class resistance-gene candidate sequences in citrus. Theor Appl Genet 101:814–822

    Article  CAS  Google Scholar 

  • DeYoung BJ, Innes RW (2006) Plant NBS-LRR proteins in pathogen sensing and host defense. Nat Immunol 7:1243–1249

    Article  CAS  PubMed  Google Scholar 

  • Duan YX, Fan J, Guo WW (2010) Regeneration and characterization of transgenic kumquat plants containing the Arabidopsis APETALA1 gene. Plant Cell Tiss Organ Cult 100:273–281

    Article  CAS  Google Scholar 

  • Geffroy V, Macadre C, David P, Pedrosa-Harand A, Sevignac M, Dauga C, Langin T (2009) Molecular analysis of a large subtelomeric nucleotide-binding-site-leucine-rich-repeat family in two representative genotypes of the major gene pools of Phaseolus vulgaris. Genetics 181:405–419

    Article  CAS  PubMed  Google Scholar 

  • Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:1121–1137

    CAS  PubMed  Google Scholar 

  • Guidetti-Gonzalez S, Carrer H (2007) Putative resistance genes in the CitEST database. Genet Mol Biol 30:931–942

    CAS  Google Scholar 

  • Hayes AJ, Jeong SC, Gore MA, Yu YG, Buss GR, Tolin SA, Maroof MAS (2004) Recombination within a nucleotide-binding-site/leucine-rich-repeat gene cluster produces new variants conditioning resistance to soybean mosaic virus in soybeans. Genetics 166:493–503

    Article  CAS  PubMed  Google Scholar 

  • Huang D, Wu W, Lu L (2004) Microdissection and molecular manipulation of single chromosomes in woody fruit trees with small chromosomes using pomelo (Citrus grandis) as a model. II. Cloning of resistance gene analogs from single chromosomes. Theor Appl Genet 108:1371–1377

    Article  CAS  PubMed  Google Scholar 

  • Kanazin V, Marek LF, Shoemaker RC (1996) Resistance gene analogs are conserved and clustered in soybean. Proc Natl Acad Sci USA 93:11746–11750

    Article  CAS  PubMed  Google Scholar 

  • Kohler A, Rinaldi C, Duplessis S, Baucher M, Geelen D, Duchaussoy F, Meyers BC, Boerjan W, Martin F (2008) Genome-wide identification of NBS resistance genes in Populus trichocarpa. Plant Mol Biol 66:619–636

    Article  CAS  PubMed  Google Scholar 

  • Kuang H, Woo SS, Meyers BC, Nevo E, Michelmore RW (2004) Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell 16:2870–2894

    Article  CAS  PubMed  Google Scholar 

  • Lee SY, Seo JS, Rodriguez-Lanetty M, Lee DH (2003) Comparative analysis of superfamilies of NBS-encoding disease resistance gene analogs in cultivated and wild apple species. Mol Genet Genomics 269:101–108

    CAS  PubMed  Google Scholar 

  • Leister D, Ballvora A, Salamini F, Gebhardt C (1996) A PCR-based approach for isolating pathogen resistance genes from potato with potential for wide application in plants. Nat Genet 14:421–429

    Article  CAS  PubMed  Google Scholar 

  • Martinez Zamora MG, Castagnaro AP, Diaz Ricci JC (2004) Isolation and diversity analysis of resistance gene analogues (RGAs) from cultivated and wild strawberries. Mol Genet Genomics 272:480–487

    Article  CAS  PubMed  Google Scholar 

  • McHale L, Tan X, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7:212

    Article  PubMed  Google Scholar 

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

    Article  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 15:809–834

    Article  CAS  PubMed  Google Scholar 

  • Monosi B, Wisser RJ, Pennill L, Hulbert SH (2004) Full-genome analysis of resistance gene homologues in rice. Theor Appl Genet 109:1434–1447

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Noël L, Moores TL, van Der Biezen EA, Parniske M, Daniels MJ, Parker JE, Jones JD (1999) Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell 11:2099–2112

    Article  PubMed  Google Scholar 

  • Palomino C, Satovic Z, Cubero JI, Torres AM (2006) Identification and characterization of NBS-LRR class resistance gene analogs in faba bean (Vicia faba L.) and chickpea (Cicer arietinum L.). Genome 49:1227–1237

    Article  CAS  PubMed  Google Scholar 

  • Pan Q, Liu YS, Budai-Hadrian O, Sela M, Carmel-Goren L, Zamir D, Fluhr R (2000a) Comparative genetics of nucleotide binding site-leucine rich repeat resistance gene homologues in the genomes of two dicotyledons: tomato and arabidopsis. Genetics 155:309–322

    CAS  PubMed  Google Scholar 

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

    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 31:153–163

    Article  CAS  PubMed  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 Genomics 281:609–626

    Article  CAS  PubMed  Google Scholar 

  • Radwan O, Gandhi S, Heesacker A, Whitaker B, Taylor C, Plocik A, Kesseli R, Kozik A, Michelmore RW, Knapp SJ (2008) Genetic diversity and genomic distribution of homologs encoding NBS-LRR disease resistance proteins in sunflower. Mol Genet Genomics 280:111–125

    Article  CAS  PubMed  Google Scholar 

  • Roose ML, Close TJ (2008) Genomics of Citrus, a major fruit crop of tropical and subtropical regions. Genomics Trop Crop Plants, pp 187–202

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2rd edn edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Smith SM, Hulbert SH (2005) Recombination events generating a novel Rp1 race specificity. Mol Plant-Microbe Interact 18:220–228

    Article  CAS  PubMed  Google Scholar 

  • Sudupak MA, Bennetzen JL, Hulbert SH (1993) Unequal exchange and meiotic instability of disease-resistance genes in the Rp1 region of maize. Genetics 133:119–125

    CAS  PubMed  Google Scholar 

  • Talon M, Gmitter FG Jr (2008) Citrus genomics. Int J Plant Genomics 2008:528361

    PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Xu Q, Wen XP, Deng XX (2005) Isolation of TIR and nonTIR NBS-LRR resistance gene analogues and identification of molecular markers linked to a powdery mildew resistance locus in chestnut rose (Rosa roxburghii Tratt). Theor Appl Genet 111:819–830

    Article  CAS  PubMed  Google Scholar 

  • Xu Q, Wen XP, Deng XX (2007) Phylogenetic and evolutionary analysis of NBS-encoding genes in Rosaceae fruit crops. Mol Phylogenet Evol 44:315–324

    Article  CAS  PubMed  Google Scholar 

  • Xu Q, Wen XP, Deng XX (2008) Genomic organization, rapid evolution and meiotic instability of nucleotide-binding-site-encoding genes in a new fruit crop, “Chestnut rose”. Genetics 178:2081–2091

    Article  CAS  PubMed  Google Scholar 

  • Yang ZN, Ye XR, Molina J, Roose ML, Mirkov TE (2003) Sequence analysis of a 282-kilobase region surrounding the citrus Tristeza virus resistance gene (Ctv) locus in Poncirus trifoliata L. Raf. Plant Physiol 131:482–492

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Yi H, Richards EJ (2008) Phenotypic instability of Arabidopsis alleles affecting a disease resistance gene cluster. BMC Plant Biol 8:36

    Article  PubMed  Google Scholar 

  • Yu YG, Buss GR, Maroof MA (1996) Isolation of a superfamily of candidate disease-resistance genes in soybean based on a conserved nucleotide-binding site. Proc Natl Acad Sci USA 93:11751–11756

    Article  CAS  PubMed  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 Genomics 271:402–415

    Article  CAS  PubMed  Google Scholar 

  • Zhu H, Cannon SB, Young ND, Cook DR (2002) Phylogeny and genomic organization of the TIR and non-TIR NBS-LRR resistance gene family in Medicago truncatula. Mol Plant Microbe Interact 15:529–539

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National 863 project, and Natural Science Foundation of China (NSFC Nos. 30800745, 31071779, and 30921002).

Author information

Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, People’s Republic of China

    Qiang Xu, Manosh Kumar Biswas, Hong Lan, Wenfang Zeng, Chaoyang Liu, Jidi Xu & Xiuxin Deng

Authors
  1. Qiang Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Manosh Kumar Biswas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hong Lan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wenfang Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chaoyang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jidi Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiuxin Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qiang Xu.

Additional information

Communicated by Y. Van de Peer.

Q. Xu and M. K. Biswas contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. 1. Alignment of deduced amino acid sequences of Rutaceae NBS-encoding genes (PDF 229 kb)

438_2010_593_MOESM2_ESM.tif

Supplementary Fig. 2. Segregation of seven NBS genes among 94 intergeneric F1 individuals. Gene names shown on the left side. P1: C. reticulata; P2: P. trifoliata; 1-94: the set of F1 progeny(TIFF 1142 kb)

438_2010_593_MOESM3_ESM.xls

Supplementary Table 1. Primer sequences used to amplify 32 gene-specific NBS gene fragments among the C. reticulata × P. trifoliata F1 population (XLS 25 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xu, Q., Biswas, M.K., Lan, H. et al. Phylogenetic and evolutionary analysis of NBS-encoding genes in Rutaceae fruit crops. Mol Genet Genomics 285, 151–161 (2011). https://doi.org/10.1007/s00438-010-0593-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-010-0593-9

Keywords

Search

Navigation