Identification and Characterisation of a Hyper-Variable Apoplastic Effector Gene Family of the Potato Cyst Nematodes

English version České info

Sedentary plant parasitic nematodes are pathogens that invade plant roots and establish a feeding site. The feeding site is a specialist structure used by the nematode to support its development within the plant. The nematode secretes a suite of proteins, termed ‘effector proteins’ that are responsible for initiating and maintaining the feeding site. The nematode must also evade recognition by the plant defence systems throughout its lifecycle that can last for many weeks. We describe a diverse and variable effector gene family (HYP), the products of which are secreted into the plant by the nematode and are required for successful infection. The variability and modular structure of this gene family can lead to the production of a large array of effector proteins. This diversity may allow the nematodes to combat any resistance mechanisms developed by the plant. Each nematode tested within a population is genetically unique in terms of these effector genes. We found huge variation in the number, size and type of HYP effectors at the level of the individual. This may explain some of the difficulties in breeding nematode resistant plants and has profound implications for those working with other plant pathogens.

Vyšlo v časopise: Identification and Characterisation of a Hyper-Variable Apoplastic Effector Gene Family of the Potato Cyst Nematodes. PLoS Pathog 10(9): e32767. doi:10.1371/journal.ppat.1004391
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004391

Souhrn

Zdroje

1. TrudgillDL (1997) Parthenogenetic root-knot nematodes (Meloidogyne spp); How can these biotrophic endoparasites have such an enormous host range? Plant Pathology 46: 26–32.

2. Nicol JM, Turner SJ, Coyne DL, den Nijs L, Hockland S, et al. (2011) Current Nematode Threats to World Agriculture. In: Jones J, Gheysen G, Fenoll C, editors. Genomics and Molecular Genetics of Plant-Nematode Interactions. pp. 21–43.

3. van MegenH, van den ElsenS, HoltermanM, KarssenG, MooymanP, et al. (2009) A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11: 927–950.

4. WyssU (1992) Observations on the feeding behaviour of Heterodera schachtii throughout development including events during moulting. Fundamental and Applied Nematology 15: 75–89.

5. HaegemanA, MantelinS, JonesJT, GheysenG (2012) Functional roles of effectors of plant-parasitic nematodes. Gene 492: 19–31.

6. HeweziT, BaumTJ (2013) Manipulation of plant cells by cyst and root-knot nematode effectors. Molecular Plant-Microbe Interactions 26: 9–16.

7. LilleyCJ, UrwinPE, AtkinsonHJ, McPhersonMJ (1997) Characterization of cDNAs encoding serine proteinases from the soybean cyst nematode Heterodera glycines. Molecular and Biochemical Parasitology 89: 195–207.

8. GheysenG, FenollC (2002) Gene expression in nematode feeding sites. Annual Review of Phytopathology 40: 191–219.

9. WangXH, MitchumMG, GaoBL, LiCY, DiabH, et al. (2005) A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Molecular Plant Pathology 6: 187–191.

10. ReplogleA, WangJ, BleckmannA, HusseyRS, BaumTJ, et al. (2011) Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE. The Plant Journal 65: 430–440.

11. SemblatJ-P, RossoM-N, HusseyRS, AbadP, Castagnone-SerenoP (2001) Molecular cloning of a cDNA encoding an amphid-secreted putative avirulence protein from the root-knot nematode Meloidogyne incognita. Molecular Plant-Microbe Interactions 14: 72–79.

12. VieiraP, DanchinEGJ, NeveuC, CrozatC, JaubertS, et al. (2011) The plant apoplasm is an important recipient compartment for nematode secreted proteins. Journal of Experimental Botany 62: 1241–1253.

13. RossoM-N, VieiraP, de Almeida-EnglerJ, Castagnone-SerenoP (2011) Proteins secreted by root-knot nematodes accumulate in the extracellular compartment during root infection. Plant Signal Behav 6: 1232–1234.

14. EndoBY (1978) Feeding plug formation in soybean roots infected with the soybean cyst nematode. Phytopathology 68: 1022–1031.

15. SobczakM, GolinowskiWA, GrundlerFMW (1999) Ultrastructure of feeding plugs and feeding tubes formed by Heterodera schachtii. Nematology 1: 363–374.

16. GaoBL, AllenR, MaierT, DavisEL, BaumTJ, et al. (2003) The parasitome of the phytonematode Heterodera glycines. Molecular Plant-Microbe Interactions 16: 720–726.

17. HuangG, GaoB, MaierT, AllenR, DavisEL, et al. (2003) A profile of putative parasitism genes expressed in the esophageal gland cells of the root-knot nematode Meloidogyne incognita. Molecular Plant-Microbe Interactions 16: 376–381.

18. PerryRN (1996) Chemoreception in plant parasitic nematodes. Annual Review of Phytopathology 34: 181–199.

19. JonesJT, PerryRN, JohnstonMRL (1994) Changes in the ultrastructure of the amphids of the potato cyst-nematode, Globodera rostochiensis, during development and infection. Fundamental and Applied Nematology 17: 369–382.

20. TomalovaI, IachiaC, MuletK, Castagnone-SerenoP (2012) The map-1 gene family in root-knot nematodes, Meloidogyne spp.: a set of taxonomically restricted genes specific to clonal species. Plos One 7: e38656.

21. JonesJ, ReavyB, SmantG, PriorA (2004) Glutathione peroxidases of the potato cyst nematode Globodera Rostochiensis. Gene 324: 47–54.

22. CottonJA, LilleyCJ, JonesLM, KikuchiT, ReidAJ, et al. (2014) The genome and life-stage specific transcriptomes of Globodera pallida elucidate key aspects of plant parasitism by a cyst nematode. Genome Biology 15: R43.

23. WubbenMJ, CallahanFE, SchefflerBS (2010) Transcript analysis of parasitic females of the sedentary semi-endoparasitic nematode Rotylenchulus reniformis. Molecular and Biochemical Parasitology 172: 31–40.

24. JacobJ, MitrevaM, VanholmeB, GheysenG (2008) Exploring the transcriptome of the burrowing nematode Radopholus similis. Molecular Genetics and Genomics 280: 1–17.

25. AbadP, GouzyJ, AuryJ-M, Castagnone-SerenoP, DanchinEGJ, et al. (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nature Biotechnology 26: 909–915.

26. OppermanCH, BirdDM, WilliamsonVM, RokhsarDS, BurkeM, et al. (2008) Sequence and genetic map of Meloidogyne hapla: A compact nematode genome for plant parasitism. Proceedings of the National Academy of Sciences 105: 14802–14807.

27. Castagnone-SerenoP, SemblatJ-P, CastagnoneC (2009) Modular architecture and evolution of the map-1 gene family in the root-knot nematode Meloidogyne incognita. Molecular Genetics and Genomics 282: 547–554.

28. RutterWB, HeweziT, MaierTR, MitchumMG, DavisEL, et al. (2014) Members of the Meloidogyne Avirulence protein family contain multiple plant ligand-like motifs. Phytopathology 104: 879–885.

29. DoyleEL, StoddardBL, VoytasDF, BogdanoveAJ (2013) TAL effectors: highly adaptable phytobacterial virulence factors and readily engineered DNA-targeting proteins. Trends in Cell Biology 23: 390–398.

30. StamR, HowdenAJ, Delgado-CerezoM, AmaroTM, MotionGB, et al. (2013) Characterization of cell death inducing Phytophthora capsici CRN effectors suggests diverse activities in the host nucleus. Frontiers in plant science 4: 387.

31. StamR, JupeJ, HowdenAJ, MorrisJA, BoevinkPC, et al. (2013) Identification and characterisation CRN Effectors in Phytophthora capsici shows modularity and functional diversity. PLoS ONE 8: e59517.

32. WhissonSC, BoevinkPC, MolelekiL, AvrovaAO, MoralesJG, et al. (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450: 115–118.

33. ScottJA, CollinsFH, FeyereisenR (1994) Diversity of cytochrome-p450 genes in the mosquito, Anopheles albimanus. Biochemical and biophysical research communications 205: 1452–1459.

34. RansonH, NikouD, HutchinsonM, WangX, RothCW, et al. (2002) Molecular analysis of multiple cytochrome P450 genes from the malaria vector, Anopheles gambiae. Insect Molecular Biology 11: 409–418.

35. WondjiCS, IrvingH, MorganJ, LoboNF, CollinsFH, et al. (2009) Two duplicated P450 genes are associated with pyrethroid resistance in Anopheles funestus, a major malaria vector. Genome Research 19: 452–459.

36. DjouakaRF, BakareAA, CoulibalyON, AkogbetoMC, RansonH, et al. (2008) Expression of the cytochrome P450s, CYP6P3 and CYP6M2 are significantly elevated in multiple pyrethroid resistant populations of Anopheles gambiae s.s. from Southern Benin and Nigeria. Bmc Genomics 9: 538.

37. BaroneA, RitterE, SchachtschabelU, DebenerT, SalaminiF, et al. (1990) Localization by restriction-fragment-length-polymorphism mapping in potato of a major dominant gene conferring resistance to the potato cyst nematode Globodera rostochiensis. Molecular & General Genetics 224: 177–182.

38. SasagawaY, NikaidoI, HayashiT, DannoH, UnoKD, et al. (2013) Quartz-Seq: a highly reproducible and sensitive single-cell RNA sequencing method, reveals non-genetic gene-expression heterogeneity. Genome Biology 14: R31.

39. AlendaC, Gallot-LegrandA, FouvilleD, GrenierE (2013) Sequence polymorphism of nematode effectors highlights molecular differences among the subspecies of the tobacco cyst nematode complex. Physiological and Molecular Plant Pathology 84: 107–114.

40. PlantardO, PicardD, ValetteS, ScurrahM, GrenierE, et al. (2008) Origin and genetic diversity of Western European populations of the potato cyst nematode (Globodera pallida) inferred from mitochondrial sequences and microsatellite loci. Molecular Ecology 17: 2208–2218.

41. ThieryM, FouvilleD, MugnieryD (1997) Intra- and interspecific variability in Globodera, parasites of Solanaceous plants, revealed by random amplified polymorphic DNA (RAPD) and correlation with biological features. Fundamental and Applied Nematology 20: 495–504.

42. BlokVC, MallochG, HarrowerB, PhillipsMS, VrainTC (1998) Intraspecific variation in ribosomal DNA in populations of the potato cyst nematode Globodera pallida. Journal of Nematology 30: 262–274.

43. LilleyCJ, BakhetiaM, CharltonWL, UrwinPE (2007) Recent progress in the development of RNA interference for plant parasitic nematodes. Molecular Plant Pathology 8: 701–711.

44. LilleyC, DaviesL, UrwinP (2012) RNA interference in plant parasitic nematodes: a summary of the current status. Parasitology 139: 630–640.

45. WubbenMJ, CallahanFE, TriplettBA, JenkinsJN (2009) Phenotypic and molecular evaluation of cotton hairy roots as a model system for studying nematode resistance. Plant Cell Reports 28: 1399–1409.

46. TriplettBA, MossSC, BlandJM, DowdMK (2008) Induction of hairy root cultures from Gossypium hirsutum and Gossypium barbadense to produce gossypol and related compounds. In Vitro Cellular & Developmental Biology-Plant 44: 508–517.

47. DalzellJJ, McVeighP, WarnockND, MitrevaM, BirdDM, et al. (2011) RNAi effector diversity in nematodes. PLoS neglected tropical diseases 5: e1176.

48. JonesJT, HaegemanA, DanchinEGJ, GaurHS, HelderJ, et al. (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology 14: 946–961.

49. HoltermanM, KarssenG, van den ElsenS, van MegenH, BakkerJ, et al. (2009) 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 99: 227–235.

50. BarrettLW, FletcherS, WiltonSD (2012) Regulation of eukaryotic gene expression by the untranslated gene regions and other non-coding elements. Cellular and Molecular Life Sciences 69: 3613–3634.

51. ZhaoW, BlagevD, PollackJL, ErleDJ (2011) Toward a systematic understanding of mRNA 3′ untranslated regions. Proceedings of the American Thoracic Society 8: 163–166.

52. SuarezZ, MossCS, InserraRN (1985) Anatomical changes induced by Punctodera chalcoensis in corn roots. Journal of Nematology 17: 242–244.

53. CohnE, MordechaiM (1982) Biology and host parasite relations of a species of Meloidoderita nematoda criconematoidea. Revue de Nematologie 5: 247–256.

54. VovlasN, InserraRN (1986) Morphometrics, illustration, and histopathology of Sphaeronema rumicis on cottonwood in Utah. Journal of Nematology 18: 239–246.

55. JonesMGK, PayneHL (1977) Structure of syncytia induced by phytoparasitic nematode Nacobbus aberrans in tomato roots, and possible role of plasmodesmata in their nutrition. Journal of Cell Science 23: 299–313.

56. Eves-van den AkkerS, LilleyC, DanchinE, RancurelC, CockP, et al. (2014) The transcriptome of Nacobbus aberrans reveals insights into the evolution of sedentary endoparasitism in plant-parasitic nematodes. Genome Biology and Evolution evu171.

57. TriantDA, WhiteheadA (2009) Simultaneous extraction of high-quality RNA and DNA from small tissue samples. Journal of Heredity 100: 246–250.

58. de BoerJM, YanY, SmantG, DavisEL, BaumTJ (1998) In situ hybridization to messenger RNA in Heterodera glycines. J Nematol 30: 309–312.

59. DaviesLJ, LilleyCJ, KnoxJP, UrwinPE (2012) Syncytia formed by adult female Heterodera schachtii in Arabidopsis thaliana roots have a distinct cell wall molecular architecture. New Phytologist 196: 238–246.

60. HoppTP, WoodsKR (1981) Prediction of protein antigenic determinants from amino acid sequences. Proceedings of the National Academy of Sciences 78: 3824–3828.

61. WesleySV, HelliwellCA, SmithNA, WangM, RouseDT, et al. (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. The Plant Journal 27: 581–590.

62. GleaveAP (1992) A versatile binary vector system with a T-DNA organizational-structure conducive to efficient integration of cloned DNA into the plant genome. Plant Molecular Biology 20: 1203–1207.

63. PetersenTN, BrunakS, von HeijneG, NielsenH (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods 8: 785–786.

64. Bird AF, Bird J (1991) The structure of nematodes. San Diego (California): Academic Press.