Recent Duplications Dominate NBS-encoding Gene Expansion in Two Woody Species

Overview

Journal Mol Genet Genomics

Specialty Genetics

Date 2008 Jun 20

PMID 18563445

Citations 231

Authors

Sihai Yang

Xiaohui Zhang

Jia-Xing Yue

Dacheng Tian

Jian-Qun Chen

Affiliations

Soon will be listed here.

Abstract

Most disease resistance genes in plants encode NBS-LRR proteins. However, in woody species, little is known about the evolutionary history of these genes. Here, we identified 459 and 330 respective NBS-LRRs in grapevine and poplar genomes. We subsequently investigated protein motif composition, phylogenetic relationships and physical locations. We found significant excesses of recent duplications in perennial species, compared with those of annuals, represented by rice and Arabidopsis. Consequently, we observed higher nucleotide identity among paralogs and a higher percentage of NBS-encoding genes positioned in numerous clusters in the grapevine and poplar. These results suggested that recent tandem duplication played a major role in NBS-encoding gene expansion in perennial species. These duplication events, together with a higher probability of recombination revealed in this study, could compensate for the longer generation time in woody perennial species e.g. duplication and recombination could serve to generate novel resistance specificities. In addition, we observed extensive species-specific expansion in TIR-NBS-encoding genes. Non-TIR-NBS-encoding genes were poly- or paraphyletic, i.e. genes from three or more plant species were nested in different clades, suggesting different evolutionary patterns between these two gene types.

Citing Articles

Phylogenetic, Structural, and Evolutionary Insights into Pepper NBS-LRR Resistance Genes.

Liu J, Cheng Y, Ruan M, Ye Q, Wang R, Yao Z Int J Mol Sci. 2025; 26(5).

PMID: 40076456 PMC: 11899730. DOI: 10.3390/ijms26051828.

Deep discovery in HLB resistant wild Australian limes uncovers evolutionary features and potentially important loci for hybrid breeding.

Liu J, Singh K, Huff M, Gottschalk C, Do M, Staton M Front Plant Sci. 2025; 15:1503030.

PMID: 39963358 PMC: 11831368. DOI: 10.3389/fpls.2024.1503030.

Genome-wide identification, characterization, and functional analysis of the CHX, SOS, and RLK genes in Solanum lycopersicum under salt stress.

Maghraby A, Alzalaty M Sci Rep. 2025; 15(1):1142.

PMID: 39774029 PMC: 11707246. DOI: 10.1038/s41598-024-83221-w.

Evolutionary analysis of TIR- and non-TIR-NBS-LRR disease resistance genes in wild strawberries.

Zhu N, Feng Y, Shi G, Zhang Q, Yuan B, Qiao Q Front Plant Sci. 2024; 15:1452251.

PMID: 39640992 PMC: 11617207. DOI: 10.3389/fpls.2024.1452251.

Molecular characteristics and expression pattern of the FAR1 gene during spike sprouting in quinoa.

Huang L, Zhang L, Zhang P, Liu J, Li L, Li H Sci Rep. 2024; 14(1):28485.

PMID: 39557968 PMC: 11573983. DOI: 10.1038/s41598-024-79474-0.

References

McHale L, Tan X, Koehl P, Michelmore R . Plant NBS-LRR proteins: adaptable guards. Genome Biol. 2006; 7(4):212. PMC: 1557992. DOI: 10.1186/gb-2006-7-4-212. View

van Ooijen G, van den Burg H, Cornelissen B, Takken F . Structure and function of resistance proteins in solanaceous plants. Annu Rev Phytopathol. 2007; 45:43-72. DOI: 10.1146/annurev.phyto.45.062806.094430. View

Bai J, Pennill L, Ning J, Lee S, Ramalingam J, Webb C . Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res. 2002; 12(12):1871-84. PMC: 187567. DOI: 10.1101/gr.454902. View

Meyers B, Kozik A, Griego A, Kuang H, Michelmore R . Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell. 2003; 15(4):809-34. PMC: 152331. DOI: 10.1105/tpc.009308. View

Cannon S, Zhu H, Baumgarten A, Spangler R, May G, Cook D . Diversity, distribution, and ancient taxonomic relationships within the TIR and non-TIR NBS-LRR resistance gene subfamilies. J Mol Evol. 2002; 54(4):548-62. DOI: 10.1007/s0023901-0057-2. View

Rozas J, Sanchez-DelBarrio J, Messeguer X, Rozas R . DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 2003; 19(18):2496-7. DOI: 10.1093/bioinformatics/btg359. View

Lynch M, Crease T . The analysis of population survey data on DNA sequence variation. Mol Biol Evol. 1990; 7(4):377-94. DOI: 10.1093/oxfordjournals.molbev.a040607. View

. The sequence of rice chromosomes 11 and 12, rich in disease resistance genes and recent gene duplications. BMC Biol. 2005; 3:20. PMC: 1261165. DOI: 10.1186/1741-7007-3-20. View

Tamura K, Dudley J, Nei M, Kumar S . MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 2007; 24(8):1596-9. DOI: 10.1093/molbev/msm092. View

10.

Yang S, Feng Z, Zhang X, Jiang K, Jin X, Hang Y . Genome-wide investigation on the genetic variations of rice disease resistance genes. Plant Mol Biol. 2006; 62(1-2):181-93. DOI: 10.1007/s11103-006-9012-3. View

11.

Parniske M, Hammond-Kosack K, Golstein C, Thomas C, Jones D, Harrison K . Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell. 1997; 91(6):821-32. DOI: 10.1016/s0092-8674(00)80470-5. View

12.

Holub E . The arms race is ancient history in Arabidopsis, the wildflower. Nat Rev Genet. 2001; 2(7):516-27. DOI: 10.1038/35080508. View

13.

Xiao S, Ellwood S, Calis O, Patrick E, Li T, Coleman M . Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science. 2001; 291(5501):118-20. DOI: 10.1126/science.291.5501.118. View

14.

Ding J, Zhang W, Jing Z, Chen J, Tian D . Unique pattern of R-gene variation within populations in Arabidopsis. Mol Genet Genomics. 2007; 277(6):619-29. DOI: 10.1007/s00438-007-0213-5. View

15.

Meyers B, Morgante M, Michelmore R . TIR-X and TIR-NBS proteins: two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant genomes. Plant J. 2002; 32(1):77-92. DOI: 10.1046/j.1365-313x.2002.01404.x. View

16.

Meyers B, Dickerman A, Michelmore R, Sivaramakrishnan S, Sobral B, Young N . Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J. 1999; 20(3):317-32. DOI: 10.1046/j.1365-313x.1999.t01-1-00606.x. View

17.

Jaillon O, Aury J, Noel B, Policriti A, Clepet C, Casagrande A . The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature. 2007; 449(7161):463-7. DOI: 10.1038/nature06148. View

18.

Leister D . Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. Trends Genet. 2004; 20(3):116-22. DOI: 10.1016/j.tig.2004.01.007. View

19.

. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000; 408(6814):796-815. DOI: 10.1038/35048692. View

20.

Lupas A, Van Dyke M, Stock J . Predicting coiled coils from protein sequences. Science. 1991; 252(5009):1162-4. DOI: 10.1126/science.252.5009.1162. View