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Analysis of the Rdr1 gene family in different Rosaceae genomes reveals an origin of an R-gene cluster after the split of Rubeae within the Rosoideae subfamily


Autoři: Ina Menz aff001;  Deepika Lakhwani aff002;  Jérémy Clotault aff002;  Marcus Linde aff001;  Fabrice Foucher aff002;  Thomas Debener aff001
Působiště autorů: Institute for Plant Genetics, Leibniz Universität Hannover, Hannover, Germany aff001;  IRHS, Agrocampus-Ouest, INRA, Université d’Angers, Beaucouzé, France aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0227428

Souhrn

The Rdr1 gene confers resistance to black spot in roses and belongs to a large TNL gene family, which is organized in two major clusters at the distal end of chromosome 1. We used the recently available chromosome scale assemblies for the R. chinensis ‘Old Blush’ genome, re-sequencing data for nine rose species and genome data for Fragaria, Rubus, Malus and Prunus to identify Rdr1 homologs from different taxa within Rosaceae. Members of the Rdr1 gene family are organized into two major clusters in R. chinensis and at a syntenic location in the Fragaria genome. Phylogenetic analysis indicates that the two clusters existed prior to the split of Rosa and Fragaria and that one cluster has a more recent origin than the other. Genes belonging to cluster 2, such as the functional Rdr1 gene muRdr1A, were subject to a faster evolution than genes from cluster 1. As no Rdr1 homologs were found in syntenic positions for Prunus persica, Malus x domestica and Rubus occidentalis, a translocation of the Rdr1 clusters to the current positions probably happened after the Rubeae split from other groups within the Rosoideae approximately 70–80 million years ago during the Cretaceous period.

Klíčová slova:

Amino acid sequence analysis – Genome analysis – Genomic medicine – Homologous chromosomes – Phylogenetic analysis – Plant genomics – Sequence alignment – Roses


Zdroje

1. Brands SJ Systema Naturae 2000: The Taxonomicon. [cited 06.04.2018] Available from: http://taxonomicon.taxonomy.nl/.

2. Koopman WJM, Wissemann V, Cock K de, van Huylenbroeck J, Riek J de, Sabatino GJ et al. AFLP markers as a tool to reconstruct complex relationships: A case study in Rosa (Rosaceae). Am J Bot. 2011; 95 (3): 353–366.

3. Terefe D, Debener T. An SSR from the leucine-rich repeat region of the rose Rdr1 gene family is a useful resistance gene analogue marker for roses and other Rosaceae. Plant Breed. 2011; 130 (2): 291–293.

4. Wissemann V, Ritz CM. The genus Rosa (Rosoideae, Rosaceae) revisited: Molecular analysis of nrITS-1 and atpB-rbcL intergenic spacer (IGS) versus conventional taxonomy. Bot J Linn Soc. 2005; 147 (3): 275–290.

5. Wissemann V. Conventional Taxonomy (Wild Roses). In: Roberts A, editor. Encyclopedia of rose science. Cambridge: Academic Press; 2003. pp. 111–117.

6. Debener T, Linde M. Exploring Complex Ornamental Genomes: The Rose as a Model Plant. CRC Crit Rev Plant Sci. 2009; 28 (4): 267–280.

7. Nakamura N, Hirakawa H, Sato S, Otagaki S, Matsumoto S, Tabata S et al. Genome structure of Rosa multiflora, a wild ancestor of cultivated roses. DNA res. 2018; 25 (2): 113–121. doi: 10.1093/dnares/dsx042 29045613

8. Raymond O, Gouzy J, Just J, Badouin H, Verdenaud M, Lemainque A et al. The Rosa genome provides new insights into the domestication of modern roses. Nat genet. 2018; 50 (6): 772–777. doi: 10.1038/s41588-018-0110-3 29713014

9. Hibrand Saint-Oyant L, Ruttink T, Hamama L, Kirov I, Lakhwani D, Zhou NN et al. A high-quality genome sequence of Rosa chinensis to elucidate ornamental traits. Nat plants. 2018; 4 (7): 473–484. doi: 10.1038/s41477-018-0166-1 29892093

10. Terefe-Ayana D, Kaufmann H, Linde M, Debener T. Evolution of the Rdr1 TNL-cluster in roses and other Rosaceous species. BMC Genomics. 2012; 13: 409. doi: 10.1186/1471-2164-13-409 22905676

11. Belkhadir Y, Subramaniam R, Dangl JL. Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr Opin Plant Biol. 2004; 7 (4): 391–399. doi: 10.1016/j.pbi.2004.05.009 15231261

12. Jones DA, Jones JDG. The Role of Leucine-Rich Repeat Proteins in Plant Defences. In: Tommerup IC, Andrews JH, editors. Advances in botanical research: Incorporating advances in plant pathology. London: Academic. 1997. pp. 89–167.

13. Leipe DD, Koonin EV, Aravind L. STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: Multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer. J Mol Biol. 2004; 343 (1): 1–28. doi: 10.1016/j.jmb.2004.08.023 15381417

14. McHale L, Tan X, Koehl P, Michelmore RW. Plant NBS-LRR proteins: Adaptable guards. Genome Biol. 2006; 7 (4): 212. doi: 10.1186/gb-2006-7-4-212 16677430

15. Pan Q, Wendel J, Fluhr R. Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes. J Mol Evol. 2000; 50 (3): 203–213. doi: 10.1007/s002399910023 10754062

16. van Eck L, Bradeen JM. The NB-LRR Disease Resistance Genes of Fragaria and Rubus. In: Hytönen T, Graham J, Harrison R, editors. The Genomes of Rosaceous Berries and Their Wild Relatives. Heidelberg: Springer; 2018. pp. 63–75.

17. Sekhwal MK, Li P, Lam I, Wang X, Cloutier S, You FM. Disease Resistance Gene Analogs (RGAs) in Plants. Int J Mol Med Sci. 2015; 16 (8): 19248–19290.

18. Jia YX, Yuan Y, Zhang Y, Yang S, Zhang X. Extreme expansion of NBS-encoding genes in Rosaceae. BMC Genetics. 2015; 16: 48. doi: 10.1186/s12863-015-0208-x 25935646

19. Zhang M, Wu Y-H, Lee M-K, Liu Y-H, Rong Y, Santos TS et al. Numbers of genes in the NBS and RLK families vary by more than four-fold within a plant species and are regulated by multiple factors. Nucleic acids res. 2010; 38 (19): 6513–6525. doi: 10.1093/nar/gkq524 20542917

20. Kuang H, Woo S-S, Meyers BC, Nevo E, Michelmore RW. Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell. 2004; 16 (11): 2870–2894. doi: 10.1105/tpc.104.025502 15494555

21. Yang S, Zhang X, Yue J-X, Tian D, Chen J-Q. Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Genet Genomics. 2008; 280 (3): 187–198. doi: 10.1007/s00438-008-0355-0 18563445

22. Ameline-Torregrosa C, Wang B-B, O’Bleness MS, Deshpande S, Zhu H, Roe B et al. Identification and characterization of nucleotide-binding site-leucine-rich repeat genes in the model plant Medicago truncatula. Plant Physio. 2008;146 (1): 5–21.

23. Ma F-F, Wu M, Liu Y-N, Feng X-Y, Wu X-Z, Chen J-Q et al. Molecular characterization of NBS-LRR genes in the soybean Rsv3 locus reveals several divergent alleles that likely confer resistance to the soybean mosaic virus. Theor Appl Genet. 2018; 131 (2): 253–265. doi: 10.1007/s00122-017-2999-9 29038948

24. Menz I, Straube J, Linde M, Debener T. The TNL gene Rdr1 confers broad-spectrum resistance to Diplocarpon rosae. Mol Plant Pathol. 2018; 19 (5): 1104–1113. doi: 10.1111/mpp.12589 28779550

25. Terefe-Ayana D, Yasmin A, Le TL, Kaufmann H, Biber A et al. Mining disease-resistance genes in roses: functional and molecular characterization of the Rdr1 locus. Front Plant Sci. 2011; 2: 35. doi: 10.3389/fpls.2011.00035 22639591

26. Xiang Y, Huang C-H, Hu Y, Wen J, Li S, Yi T et al. Evolution of Rosaceae Fruit Types Based on Nuclear Phylogeny in the Context of Geological Times and Genome Duplication. Mol Biol Evol. 2017; 34 (2): 262–281. doi: 10.1093/molbev/msw242 27856652

27. VanBuren R, Wai CM, Colle M, Wang J, Sullivan S, Bushakra JM et al. A near complete, chromosome-scale assembly of the black raspberry (Rubus occidentalis) genome. Gigascience. 2018; 7 (8).

28. Perazzolli M, Malacarne G, Baldo A, Righetti L, Bailey A, Fontana P et al. Characterization of resistance gene analogues (RGAs) in apple (Malus × domestica Borkh.) and their evolutionary history of the Rosaceae family. PloS One. 2014; 9 (2): e83844. doi: 10.1371/journal.pone.0083844 24505246

29. Nieri D, Di Donato A, Ercolano MR. Analysis of tomato meiotic recombination profile reveals preferential chromosome positions for NB-LRR genes. Euphytica. 2017; 213 (9): 1027.

30. Chavan S, Gray J, Smith SM. Diversity and evolution of Rp1 rust resistance genes in four maize lines. Theor Appl Genet. 2015; 128 (5): 985–998. doi: 10.1007/s00122-015-2484-2 25805314

31. Edger PP, VanBuren Rt, Colle M, Poorten TJ, Wai CM, Niederhuth CE et al. Single-molecule sequencing and optical mapping yields an improved genome of woodland strawberry (Fragaria vesca) with chromosome-scale contiguity. Gigascience. 2018; 7 (2): 1–7.

32. Daccord N, Celton J-M, Linsmith G, Becker C, Choisne N, Schijlen E et al. High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat Genet. 2017; 49 (7): 1099–1106. doi: 10.1038/ng.3886 28581499

33. Verde I, Abbott AG, Scalabrin S, Jung S, Shu S, Marroni F et al. The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet. 2013; 45 (5): 487–494. doi: 10.1038/ng.2586 23525075

34. Verde I, Jenkins J, Dondini L, Micali S, Pagliarani G, Vendramin E et al. The Peach v2.0 release: High-resolution linkage mapping and deep resequencing improve chromosome-scale assembly and contiguity. BMC Genomics. 2017; 18 (1): 225. doi: 10.1186/s12864-017-3606-9 28284188

35. Buti M, Moretto M, Barghini E, Mascagni F, Natali L, Brilli M et al. The genome sequence and transcriptome of Potentilla micrantha and their comparison to Fragaria vesca (the woodland strawberry). Gigascience. 2018; 7 (4): 1–14.

36. Hall TA, others. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999; 95–98. doi: 10.1093/nass/42.1.95

37. Mistry J, Bateman A, Finn RD. Predicting active site residue annotations in the Pfam database. BMC Bioinformatics. 2007; 8: 298. doi: 10.1186/1471-2105-8-298 17688688

38. Edgar RC. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004; 32 (5): 1792–1797. doi: 10.1093/nar/gkh340 15034147

39. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol Biol Evol. 2018; 35 (6): 1547–1549. doi: 10.1093/molbev/msy096 29722887

40. Nei M, Kumar S. Molecular evolution and phylogenetics. Oxford University Press; 2000.

41. Letunic I, Bork P. Interactive tree of life (iTOL) v3: An online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 2016; 44 (W1): W242–5. doi: 10.1093/nar/gkw290 27095192

42. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986; 3 (5): 418–426. doi: 10.1093/oxfordjournals.molbev.a040410 3444411

43. VanBuren R, Bryant D, Bushakra JM, Vining KJ, Edger PP, Rowley ER et al. The genome of black raspberry (Rubus occidentalis). Plant J. 2016; 87 (6): 535–547. doi: 10.1111/tpj.13215 27228578

44. Jung S, Lee T, Cheng C-H, Buble K, Zheng P, Yu J et al. 15 years of GDR: New data and functionality in the Genome Database for Rosaceae. Nucleic Acids Res. 2019; 47 (D1): D1137–D1145. doi: 10.1093/nar/gky1000 30357347

45. Li Y., Pi M., Gao Q., Liu Z. & Kang C. Updated annotation of the wild strawberry Fragaria vesca V4 genome. Hortic Res. 2019; 6 (61): doi: 10.1038/s41438-019-0142-6 31069085


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