#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

The genome of the migratory nematode, Radopholus similis, reveals signatures of close association to the sedentary cyst nematodes


Autoři: Reny Mathew aff001;  Charles H. Opperman aff001
Působiště autorů: Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC United States of America aff001
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0224391

Souhrn

Radopholus similis, commonly known as the burrowing nematode, is an important pest of myriad crops and ornamentals including banana (Musa spp.) and Citrus spp. In order to characterize the potential role of putative effectors encoded by R. similis genes we compared predicted proteins from a draft R. similis genome with other plant-parasitic nematodes in order to define the suite of excreted/secreted proteins that enable it to function as a parasite and to ascertain the phylogenetic position of R. similis in the Tylenchida order. Identification and analysis of candidate genes encoding for key plant cell-wall degrading enzymes including GH5 cellulases, PL3 pectate lyases and GH28 polygalactouranase revealed a pattern of occurrence similar to other PPNs, although with closest phylogenetic associations to the sedentary cyst nematodes. We also observed the absence of a suite of effectors essential for feeding site formation in the cyst nematodes. Clustering of various orthologous genes shared by R. similis with other nematodes showed higher overlap with the cyst nematodes than with the root-knot or other migratory endoparasitic nematodes. The data presented here support the hypothesis that R. similis is evolutionarily closer to the cyst nematodes, however, differences in the effector repertoire delineate ancient divergence of parasitism, probably as a consequence of niche specialization. These similarities and differences further underscore distinct evolutionary relationships during the evolution of parasitism in this group of nematodes.

Klíčová slova:

Bananas – Nematoda – Phylogenetic analysis – Plant pathology – Signal peptides – Cellulases – Chaperone proteins – Lyases


Zdroje

1. Coyne DL, Cortada L, Dalzell JJ, Claudius-Cole AO, Haukeland S, Luambano N, et al. Plant-Parasitic Nematodes and Food Security in Sub-Saharan Africa. Annual review of phytopathology. 2018;56: 381–403. doi: 10.1146/annurev-phyto-080417-045833 29958072

2. Gardner M, Dhroso A, Johnson N, Davis EL, Baum TJ, Korkin D, et al. Novel global effector mining from the transcriptome of early life stages of the soybean cyst nematode Heterodera glycines. Scientific reports. 2018;8: 2505. doi: 10.1038/s41598-018-20536-5 29410430

3. Masonbrink R, Maier TR, Muppirala U, Seetharam AS, Lord E, Juvale PS, et al. The genome of the soybean cyst nematode (Heterodera glycines) reveals complex patterns of duplications involved in the evolution of parasitism genes. BMC genomics. 2019;20: 119. doi: 10.1186/s12864-019-5485-8 30732586

4. Cotton JA, Lilley CJ, Jones LM, Kikuchi T, Reid AJ, Thorpe P, et al. The genome and life-stage specific transcriptomes of Globodera pallida elucidate key aspects of plant parasitism by a cyst nematode. Genome biology. 2014;15: R43. doi: 10.1186/gb-2014-15-3-r43 24580726

5. Eves-van den Akker S, Laetsch DR, Thorpe P, Lilley CJ, Danchin EG, Da Rocha M, et al. The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence. Genome biology. 2016;17: 124. doi: 10.1186/s13059-016-0985-1 27286965

6. Phillips WS, Howe DK, Brown AM, Eves-Van Den Akker S, Dettwyler L, Peetz AB, et al. The draft genome of Globodera ellingtonae. Journal of nematology. 2017;49: 127. 28706309

7. Opperman CH, Bird DM, Williamson VM, Rokhsar DS, Burke M, Cohn J, et al. Sequence and genetic map of Meloidogyne hapla: A compact nematode genome for plant parasitism. Proceedings of the National Academy of Sciences. 2008;105: 14802–14807.

8. Blanc-Mathieu R, Perfus-Barbeoch L, Aury J-M, Da Rocha M, Gouzy J, Sallet E, et al. Hybridization and polyploidy enable genomic plasticity without sex in the most devastating plant-parasitic nematodes. PLoS genetics. 2017;13: e1006777. doi: 10.1371/journal.pgen.1006777 28594822

9. Abad P, Gouzy J, Aury J-M, Castagnone-Sereno P, Danchin EG, Deleury E, et al. Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nature biotechnology. 2008;26: 909. doi: 10.1038/nbt.1482 18660804

10. Somvanshi VS, Tathode M, Shukla RN, Rao U. Nematode Genome Announcement: A Draft Genome for Rice Root-Knot Nematode, Meloidogyne graminicola. Journal of nematology. 2018;50: 111–116. doi: 10.21307/jofnem-2018-018 30451432

11. Lunt DH, Kumar S, Koutsovoulos G, Blaxter ML. The complex hybrid origins of the root knot nematodes revealed through comparative genomics. PeerJ. 2014;2: e356. doi: 10.7717/peerj.356 24860695

12. Koutsovoulos GD, Poullet M, El Ashry A, Kozlowski DK, Sallet E, Da Rocha M, et al. The polyploid genome of the mitotic parthenogenetic root-knot nematode Meloidogyne enterolobii. BioRxiv. 2019; 586818.

13. Mitchum MG, Hussey RS, Baum TJ, Wang X, Elling AA, Wubben M, et al. Nematode effector proteins: an emerging paradigm of parasitism. New Phytologist. 2013;199: 879–894. doi: 10.1111/nph.12323 23691972

14. Showmaker KC, Sanders WS, den Akker Eves-van S, Martin BE, Stokes JV, Hsu CY, et al. A genomic resource for the sedentary semi-endoparasitic reniform nematode, Rotylenchulus reniformis Linford & Oliveira. Journal of nematology. 2019;51: 1–2.

15. Moens M, Perry RN. Migratory plant endoparasitic nematodes: a group rich in contrasts and divergence. Annual Review of Phytopathology. 2009;47: 313–332. doi: 10.1146/annurev-phyto-080508-081846 19400647

16. Dochez C, Dusabe J, Whyte J, Tenkouano A, Ortiz R, De Waele D. New sources of resistance to Radopholus similis in Musa germplasm from Asia. Australasian Plant Pathology. 2006;35: 481–485.

17. Hölscher D, Dhakshinamoorthy S, Alexandrov T, Becker M, Bretschneider T, Buerkert A, et al. Phenalenone-type phytoalexins mediate resistance of banana plants (Musa spp.) to the burrowing nematode Radopholus similis. Proceedings of the National Academy of Sciences. 2014;111: 105–110.

18. Cobb NA. Nematodes, mostly Australian and Fijian. F. Cunninghame & Company, printers; 1893.

19. Marin DH, Sutton TB, Barker KR. Dissemination of Bananas in Latin America and the Caribbean and Its Relationship to the Occurrence of Radophouls similis. Plant disease. 1998;82: 964–974. doi: 10.1094/PDIS.1998.82.9.964 30856847

20. Marin DH, Kaplan DT, Opperman CH. Randomly amplified polymorphic DNA differs with burrowing nematode collection site, but not with host range. Journal of nematology. 1999;31: 232. 19270894

21. Kaplan DT, Opperman CH. Reproductive strategies and karyotype of the burrowing nematode, Radopholus similis. Journal of Nematology. 2000;32: 126. 19270958

22. Ferris H. Radopholus similis. 11 Apr 2018 [cited 28 Sep 2018]. Available: http://nemaplex.ucdavis.edu/Taxadata/G111s2.aspx

23. Haegeman A, Elsen A, De Waele D, Gheysen G. Emerging molecular knowledge on Radopholus similis, an important nematode pest of banana. Molecular plant pathology. 2010;11: 315–323. doi: 10.1111/j.1364-3703.2010.00614.x 20447280

24. Holterman M, Karssen G, Van Den Elsen S, Van Megen H, Bakker J, Helder J. Small subunit rDNA-based phylogeny of the Tylenchida sheds light on relationships among some high-impact plant-parasitic nematodes and the evolution of plant feeding. Phytopathology. 2009;99: 227–235. doi: 10.1094/PHYTO-99-3-0227 19203274

25. Sekora, S. Nicholas and Crow, William. burrowing nematode- Radopholus similis. Oct 2012 [cited 28 Sep 2018]. Available: http://entnemdept.ufl.edu/creatures/NEMATODE/Radopholus_similis.htm

26. Huettel RN, Dickson DW. Parthenogenesis in the Two Races of Radopholus similis from Florida. Journal of nematology. 1981;13: 13. 19300714

27. Sarah JL, Pinochet J, Stanton J. The burrowing nematode of bananas, Radopholus similis Cobb, 1913. Musa Pest Fact Sheet (INIBAP); Parasites et Ravageurs des Musa: Fiche Technique (INIBAP); Plagas de Musa: Hoja Divulgativa (INIBAP). 1996.

28. Plowright R, Dusabe J, Coyne D, Speijer P. Analysis of the pathogenic variability and genetic diversity of the plant-parasitic nematode Radopholus similis on bananas. Nematology. 2013;15: 41–56.

29. Mendoza AR, Sikora RA. Biological control of Radopholus similis in banana by combined application of the mutualistic endophyte Fusarium oxysporum strain 162, the egg pathogen Paecilomyces lilacinus strain 251 and the antagonistic bacteria Bacillus firmus. Biocontrol. 2009;54: 263–272.

30. Mathew R, Burke M, Opperman CH. A draft genome of the burrowing nematode Radopholus similis. Journal of Nematology. 2019;51.

31. Eves-van den Akker S, Lilley CJ, Danchin EGJ, Rancurel C, Cock PJA, Urwin PE, et al. The Transcriptome of Nacobbus aberrans Reveals Insights into the Evolution of Sedentary Endoparasitism in Plant-Parasitic Nematodes. Genome Biol Evol. 2014;6: 2181–2194. doi: 10.1093/gbe/evu171 25123114

32. Holterman M, Karegar A, Mooijman P, van Megen H, van den Elsen S, Vervoort MT, et al. Disparate gain and loss of parasitic abilities among nematode lineages. PLoS One. 2017;12: e0185445. doi: 10.1371/journal.pone.0185445 28934343

33. Haegeman A, Jacob J, Vanholme B, Kyndt T, Gheysen G. A family of GHF5 endo‐1, 4‐beta‐glucanases in the migratory plant‐parasitic nematode Radopholus similis. Plant Pathology. 2008;57: 581–590.

34. Haegeman A, Vanholme B, Gheysen G. Characterization of a putative endoxylanase in the migratory plant‐parasitic nematode Radopholus similis. Molecular Plant Pathology. 2009;10: 389–401. doi: 10.1111/j.1364-3703.2009.00539.x 19400841

35. Jacob J, Vanholme B, Haegeman A, Gheysen G. Four transthyretin-like genes of the migratory plant-parasitic nematode Radopholus similis: members of an extensive nematode-specific family. Gene. 2007;402: 9–19. doi: 10.1016/j.gene.2007.07.015 17765408

36. Huang X, Xu C-L, Chen W-Z, Chen C, Xie H. Cloning and characterization of the first serine carboxypeptidase from a plant parasitic nematode, Radopholus similis. Scientific reports. 2017;7: 4815. doi: 10.1038/s41598-017-05093-7 28684768

37. Li Y, Wang K, Xie H, Wang Y-T, Wang D-W, Xu C-L, et al. A nematode calreticulin, Rs-CRT, is a key effector in reproduction and pathogenicity of Radopholus similis. PLoS One. 2015;10: e0129351. doi: 10.1371/journal.pone.0129351 26061142

38. Wang K, Li Y, Huang X, Wang D, Xu C, Xie H. The cathepsin S cysteine proteinase of the burrowing nematode Radopholus similis is essential for the reproduction and invasion. Cell & bioscience. 2016;6: 39.

39. Li Y, Wang K, Xie H, Wang D-W, Xu C-L, Huang X, et al. Cathepsin B cysteine proteinase is essential for the development and pathogenesis of the plant parasitic nematode Radopholus similis. International journal of biological sciences. 2015;11: 1073. doi: 10.7150/ijbs.12065 26221074

40. Replogle A, Wang J, Bleckmann A, Hussey RS, Baum TJ, Sawa S, et al. Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE. The Plant Journal. 2011;65: 430–440. doi: 10.1111/j.1365-313X.2010.04433.x 21265896

41. Huang X, Xu C-L, Yang S-H, Li J-Y, Wang H-L, Zhang Z-X, et al. Life-stage specific transcriptomes of a migratory endoparasitic plant nematode, Radopholus similis elucidate a different parasitic and life strategy of plant parasitic nematodes. Scientific reports. 2019;9: 6277. doi: 10.1038/s41598-019-42724-7 31000750

42. Moffett P, Ali S, Magne M, Chen S, Obradovic N, Jamshaid L, et al. Analysis of Globodera rostochiensis effectors reveals conserved functions of SPRYSEC proteins in suppressing and eliciting plant immune responses. Frontiers in plant science. 2015;6: 623. doi: 10.3389/fpls.2015.00623 26322064

43. Jaouannet M, Magliano M, Arguel MJ, Gourgues M, Evangelisti E, Abad P, et al. The root-knot nematode calreticulin Mi-CRT is a key effector in plant defense suppression. Molecular Plant-Microbe Interactions. 2013;26: 97–105. doi: 10.1094/MPMI-05-12-0130-R 22857385

44. Lozano-Torres JL, Wilbers RH, Warmerdam S, Finkers-Tomczak A, Diaz-Granados A, van Schaik CC, et al. Apoplastic venom allergen-like proteins of cyst nematodes modulate the activation of basal plant innate immunity by cell surface receptors. PLoS pathogens. 2014;10: e1004569. doi: 10.1371/journal.ppat.1004569 25500833

45. Li X, Zhuo K, Luo M, Sun L, Liao J. Molecular cloning and characterization of a calreticulin cDNA from the pinewood nematode Bursaphelenchus xylophilus. Experimental parasitology. 2011;128: 121–126. doi: 10.1016/j.exppara.2011.02.017 21371475

46. Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS. The parasitome of the phytonematode Heterodera glycines. Molecular Plant-Microbe Interactions. 2003;16: 720–726. doi: 10.1094/MPMI.2003.16.8.720 12906116

47. Prior A, Jones JT, BEAUCHAMP J, McDERMOTT L, COOPER A, KENNEDY MW. A surface-associated retinol-and fatty acid-binding protein (Gp-FAR-1) from the potato cyst nematode Globodera pallida: lipid binding activities, structural analysis and expression pattern. Biochemical Journal. 2001;356: 387–394. doi: 10.1042/0264-6021:3560387 11368765

48. Wang X, Xue B, Dai J, Qin X, Liu L, Chi Y, et al. A novel Meloidogyne incognita chorismate mutase effector suppresses plant immunity by manipulating the salicylic acid pathway and functions mainly during the early stages of nematode parasitism. Plant pathology. 2018;67: 1436–1448.

49. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic acids research. 2008;37: D233–D238. doi: 10.1093/nar/gkn663 18838391

50. Hewezi T, Howe P, Maier TR, Hussey RS, Mitchum MG, Davis EL, et al. Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism. The Plant Cell. 2008;20: 3080–3093. doi: 10.1105/tpc.108.063065 19001564

51. Wubben MJ, Ganji S, Callahan FE. Identification and molecular characterization of a β-1, 4-endoglucanase gene (Rr-eng-1) from Rotylenchulus reniformis. Journal of nematology. 2010;42: 342. 22736868

52. van den Elsen S, Holovachov O, Karssen G, van Megen H, Helder J, Bongers T, et al. A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology. 2009;11: 927–950.

53. Haegeman A, Jones JT, Danchin EG. Horizontal gene transfer in nematodes: a catalyst for plant parasitism? Molecular Plant-Microbe Interactions. 2011;24: 879–887. doi: 10.1094/MPMI-03-11-0055 21539433

54. Almagro Armenteros JJ, Sønderby CK, Sønderby SK, Nielsen H, Winther O. DeepLoc: prediction of protein subcellular localization using deep learning. Bioinformatics. 2017;33: 3387–3395. doi: 10.1093/bioinformatics/btx431 29036616

55. Kikuchi T, Cock PJ, Helder J, Jones JT. Characterisation of the transcriptome of Aphelenchoides besseyi and identification of a GHF 45 cellulase. Nematology. 2014;16: 99–107.

56. Rehman S, Gupta VK, Goyal AK. Identification and functional analysis of secreted effectors from phytoparasitic nematodes. BMC microbiology. 2016;16: 48. doi: 10.1186/s12866-016-0632-8 27001199

57. Kikuchi T, Shibuya H, Aikawa T, Jones JT. Cloning and characterization of pectate lyases expressed in the esophageal gland of the pine wood nematode Bursaphelenchus xylophilus. Molecular plant-microbe interactions. 2006;19: 280–287. doi: 10.1094/MPMI-19-0280 16570658

58. Opperman CH, Bird DM, Williamson VM, Rokhsar DS, Burke M, Cohn J, et al. Sequence and genetic map of Meloidogyne hapla: A compact nematode genome for plant parasitism. Proceedings of the National Academy of Sciences. 2008.

59. Burke M, Scholl EH, Bird DM, Schaff JE, Colman SD, Crowell R, et al. The plant parasite Pratylenchus coffeaecarries a minimal nematode genome. Nematology. 2015;17: 621–637.

60. Zheng J, Peng D, Chen L, Liu H, Chen F, Xu M, et al. The Ditylenchus destructor genome provides new insights into the evolution of plant parasitic nematodes. Proc R Soc B. 2016;283: 20160942. doi: 10.1098/rspb.2016.0942 27466450

61. Lilley CJ, Maqbool A, Wu D, Yusup HB, Jones LM, Birch PR, et al. Effector gene birth in plant parasitic nematodes: Neofunctionalization of a housekeeping glutathione synthetase gene. PLoS genetics. 2018;14: e1007310. doi: 10.1371/journal.pgen.1007310 29641602

62. Cantarel BL, Korf I, Robb SM, Parra G, Ross E, Moore B, et al. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome research. 2008;18: 188–196. doi: 10.1101/gr.6743907 18025269

63. Zhang H, Yohe T, Huang L, Entwistle S, Wu P, Yang Z, et al. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 2018;46: W95–W101. doi: 10.1093/nar/gky418 29771380

64. Li X, Yang D, Niu J, Zhao J, Jian H. De novo analysis of the transcriptome of Meloidogyne enterolobii to uncover potential target genes for biological control. International journal of molecular sciences. 2016;17: 1442.

65. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic acids research. 2004;32: 1792–1797. doi: 10.1093/nar/gkh340 15034147

66. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Molecular biology and evolution. 2018;35: 1547–1549. doi: 10.1093/molbev/msy096 29722887

67. Nielsen H. Predicting secretory proteins with SignalP. Protein Function Prediction: Methods and Protocols. 2017; 59–73.

68. Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome research. 2003;13: 2178–2189. doi: 10.1101/gr.1224503 12952885

69. Wang Y, Coleman-Derr D, Chen G, Gu YQ. OrthoVenn: a web server for genome wide comparison and annotation of orthologous clusters across multiple species. Nucleic acids research. 2015;43: W78–W84. doi: 10.1093/nar/gkv487 25964301

70. Howe KL, Bolt BJ, Cain S, Chan J, Chen WJ, Davis P, et al. WormBase 2016: expanding to enable helminth genomic research. Nucleic acids research. 2015;44: D774–D780. doi: 10.1093/nar/gkv1217 26578572

71. Howe KL, Bolt BJ, Shafie M, Kersey P, Berriman M. WormBase ParaSite− a comprehensive resource for helminth genomics. Molecular and biochemical parasitology. 2017;215: 2–10. doi: 10.1016/j.molbiopara.2016.11.005 27899279

72. Emms DM, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome biology. 2015;16: 157. doi: 10.1186/s13059-015-0721-2 26243257


Článek vyšel v časopise

PLOS One


2019 Číslo 10
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

KOST
Koncepce osteologické péče pro gynekology a praktické lékaře
nový kurz
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Svět praktické medicíny 5/2023 (znalostní test z časopisu)

Imunopatologie? … a co my s tím???
Autoři: doc. MUDr. Helena Lahoda Brodská, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#