Elucidating the molecular bases of epigenetic inheritance in non-model invertebrates: The case of the root-knot nematode Meloidogyne incognita

Frontiers in Physiology

Volumn 5 JUN, Issue , 2014, Pages

  Perfus Barbeoch, Laetitia ^a   Castagnone Sereno, Philippe ^a   Reichelt, Michael ^b   Fneich, Sara ^c,d   Roquis, David ^c,d   Pratx, Loris ^a   Cosseau, Céline ^c,d   Grunau, Christoph ^c,d   Abad, Pierre ^a  

^a Institut Sophia Agrobiotech   (France)

^b IMB Jena   (Germany)

^c UNIVERSITÉ DE PERPIGNAN   (France)

^d University Via Domitia   (France)

Author keywords

Chromatin; DNA methylation; Epigenetics; Histone modification; Meloidogyne incognita

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; 5 METHYLCYTOSINE; GENOMIC DNA; HISTONE;

ARTICLE; BIOINFORMATICS; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; HISTONE MODIFICATION; INHERITANCE; LIQUID CHROMATOGRAPHY; MELOIDOGYNE INCOGNITA; NONHUMAN; NUCLEOSOME; NUCLEOTIDE SEQUENCE; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING;

EID: 84904423778     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2014.00211     Document Type: Article

References (64)

1. Abad, P., Gouzy, J., Aury, J. M., Castagnone-Sereno, P., Danchin, E. G., Deleury, E., et al. (2008). Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat. Biotechnol. 26, 909-915. doi: 10.1038/nbt.1482
2. Azzi, A., Cosseau, C., and Grunau, C. (2009). Schistosoma mansoni: developmental arrest of miracidia treated with histone deacetylase inhibitors. Exp. Parasitol. 121, 288-291. doi: 10.1016/j.exppara.2008.11.010
3. Bártová, E., Pacherník, J., Harnicarová, A., Kovarík, A., Kovaríková, M., Hofmanová, J., et al. (2005). Nuclear levels and patterns of histone H3 modification and HP1 proteins after inhibition of histone deacetylases. J. Cell Sci. 118, 5035-5046. doi: 10.1242/jcs.02621
4. Bird, A. (1980). DNA methylation and the frequency of CpG in animal DNA. Nucleic Acids Res. 8, 1499-1504. doi: 10.1093/nar/8.7.1499
5. Caby, S., and Pierce, R. J. (2009). Quantitative chromatin immunoprecipitation (Q-ChIP) applied to Schistosoma mansoni. Mol. Biochem. Parasitol. 166, 77-80. doi: 10.1016/j.molbiopara.2009.02.014
6. Caillaud, M. C., Dubreuil, G., Quentin, M., Perfus-Barbeoch, L., Lecomte, P., de Almeida Engler, J., et al. (2008). Root-knot nematodes manipulate plant cell functions during a compatible interaction. J. Plant Physiol. 165, 104-113. doi: 10.1016/j.jplph.2007.05.007
7. Castagnone-Sereno, P. (2006). Genetic variability and adaptive evolution in parthenogenetic root-knot nematodes. Heredity 96, 282-289. doi: 10.1038/sj.hdy.6800794
8. Castagnone-Sereno, P., Wajnberg, E., Bongiovanni, M., Leroy, F., and Dalmasso, A. (1994). Genetic variation in Meloidogyne incognita virulence against the tomato Mi resistance gene: evidence from isofemale line selection studies. Theor. Appl. Genet. 88, 749-753. doi: 10.1007/BF01253980
9. Chookajorn, T., Dzikowski, R., Frank, M., Li, F., Jiwani, A. Z., Hartl, D. L., et al. (2007). Epigenetic memory at malaria virulence genes. Proc. Natl. Acad. Sci. U.S.A. 104, 899-902. doi: 10.1073/pnas.0609084103
10. Cosseau, C., Azzi, A., Smith, K., Freitag, M., Mitta, G., and Grunau, C. (2009). Native chromatin immunoprecipitation (N-ChIP) and ChIP-Seq of Schistosoma mansoni: Critical experimental parameters. Mol. Biochem. Parasitol. 166, 70-76. doi: 10.1016/j.molbiopara.2009.02.015
11. Danchin, E. G., Rosso, M. N., Vieira, P., de Almeida-Engler, J., Coutinho, P. M., Henrissat, B., et al. (2010). Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc. Natl. Acad. Sci. U.S.A. 107, 17651-17656. doi: 10.1073/pnas.1008486107
12. Dernburg, A. F. (2001). Here, there, and everywhere: kinetochore function on holocentric chromosomes. J. Cell Biol. 153, F33-F38. doi: 10.1083/jcb.153.6.F33
13. Du, Z., Li, H., Wei, Q., Zhao, X., Wang, C., Zhu, Q., et al. (2013). Genome-wide analysis of histone modifications: H3K4me2, H3K4me3, H3K9ac, and H3K27ac in Oryza sativa L. Japonica. Mol. Plant. 6, 1463-1472. doi: 10.1093/mp/sst018
14. Elango, N., Hunt, B. G., Goodisman, M. A., and Yi, S. V. (2009). DNA methylation is widespread and associated with differential gene expression in castes of the honeybee, Apis mellifera. Proc. Natl. Acad. Sci. U.S.A. 106, 11206-11211. doi: 10.1073/pnas.0900301106
15. Fneich, S., Dheilly, N., Adema, C., Rognon, A., Reichelt, M., Bulla, J., et al. (2013). 5-methyl-cytosine and 5-hydroxy-methyl-cytosine in the genome of Biomphalaria glabrata, a snail intermediate host of Schistosoma mansoni. Parasit. Vectors 6:167. doi: 10.1186/1756-3305-6-167
16. Freitas-Junior, L. H., Hernandez-Rivas, R., Ralph, S. A., Montiel-Condado, D., Ruvalcaba-Salazar, O. K., Rojas-Meza, A. P., et al. (2005). Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites. Cell. 121, 25-36. doi: 10.1016/j.cell.2005.01.037
17. Gao, F., Liu, X., Wu, X. P., Wang, X. L., Gong, D., Lu, H., et al. (2012). Differential DNA methylation in discrete developmental stages of the parasitic nematode Trichinella spiralis. Genome Biol. 13, R100. doi: 10.1186/gb-2012-13-10-r100
18. Gao, F., Wang, R., and Liu, M. (2014). Trichinella spiralis, potential model nematode for epigenetics and its implication in metazoan parasitism. Front. Physiol. 4:410. doi: 10.3389/fphys.2013.00410
19. Goll, M. G., and Bestor, T. H. (2005). Eukaryotic cytosine methyltransferases. Annu. Rev. Biochem. 74, 481-514. doi: 10.1146/annurev.biochem.74.010904.153721
20. Gómez-Díaz, E., Jordà, M., Peinado, M. A., and Rivero, A. (2012). Epigenetics of host-pathogen interactions: the road ahead and the road behind. PLoS Pathog. 8:e1003007. doi: 10.1371/journal.ppat.1003007
21. Gutierrez, A., and Sommer, R. J. (2004). Evolution of dnmt-2 and mbd-2-like genes in the free-living nematodes Pristionchus pacificus, Caenorhabditis elegans and Caenorhabditis briggsae. Nucleic Acids Res. 32, 6388-6396. doi: 10.1093/nar/gkh982
22. Hendrich, B., and Tweedie, S. (2003). The methyl-CpG binding domain and the evolving role of DNA methylation in animals. Trends Genet. 19, 269-277. doi: 10.1016/S0168-9525(03)00080-5
23. Jabbari, K., and Bernardi, G. (2004). Cytosine methylation and CpG, TpG (CpA) and TpA frequencies. Gene 333, 143-149. doi: 10.1016/j.gene.2004.02.043
24. Jablonka, E., and Lamb, M. J. (2002). The changing concept of epigenetics. Ann. N. Y. Acad. Sci. 981, 82-96. doi: 10.1111/j.1749-6632.2002.tb04913.x
25. Jack, A. P., Bussemer, S., Hahn, M., Pünzeler, S., Snyder, M., Wells, M., et al. (2013). H3K56me3 is a novel, conserved heterochromatic mark that largely but not completely overlaps with H3K9me3 in both regulation and localization. PLoS ONE 8:e51765. doi: 10.1371/journal.pone.0051765
26. Jaouannet, M., Perfus-Barbeoch, L., Deleury, E., Magliano, M., Engler, G., Vieira, P., et al. (2012). A root-knot nematode-secreted protein is injected into giant cells and targeted to the nuclei. New Phytol. 194, 924-931 doi: 10.1111/j.1469-8137.2012.04164.x
27. Jenuwein, T., and Allis, C. D. (2001). Translating the histone code. Science 293, 1074-1080. doi: 10.1126/science.1063127
28. Jiang, L., Mu, J., Zhang, Q., Ni, T., Srinivasan, P., Rayavara, K., et al. (2013). PfSETvs methylation of histone H3K36 represses virulence genes in Plasmodium falciparum. Nature 499, 223-227. doi: 10.1038/nature12361
29. Kornberg, R. D., and Thomas, J. O. (1974). Chromatin structure; oligomers of the histones. Science 184, 865-868. doi: 10.1126/science.184.4139.865
30. Kumar, S., Cheng, X., Klimasauskas, S., Mi, S., Posfai, J., Roberts, R. J., et al. (1994). The DNA (cytosine-5) methyltransferases. Nucleic Acids Res. 22, 1-10. doi: 10.1093/nar/22.1.1
31. Kunert, N., Marhold, J., Stanke, J., Stach, D., and Lyko, F. (2003). A Dnmt2-like protein mediates DNA methylation in Drosophila. Development 130, 5083-5090. doi: 10.1242/dev.00716
32. Lancelot, J., Caby, S., Dubois-Abdesselem, F., Vanderstraete, M., Trolet, J., OliveiraG., et al. (2013). Schistosoma mansoni Sirtuins: characterization and potential as chemotherapeutic targets. PLoS Negl. Trop. Dis. 7:e2428. doi: 10.1371/journal.pntd.0002428
33. Lepesant, J. M., Cosseau, C., Boissier, J., Freitag, M., Portela, J., Climent, D., et al. (2012). Chromatin structural changes around satellite repeats on the female sex chromosome in Schistosoma mansoni and their possible role in sex chromosome emergence. Genome Biol. 13, R14. doi: 10.1186/gb-2012-13-2-r14
34. Lepesant, J. M., Grunau, C., and Cosseau, C. (2011). Towards an understanding of the epigenetics of schistosomes: a comparative epigenomic study. Mem. Inst. Oswaldo Cruz. 106, 823-830. doi: 10.1590/S0074-02762012000100022
35. Li, B., Carey, M., and Workman, J. L. (2007). The role of chromatin during transcription. Cell 128, 707-719. doi: 10.1016/j.cell.2007.01.015
36. Luger, K., Dechassa, M. L., and Tremethick, D. J. (2012). New insights into nucleosome and chromatin structure: an ordered state or a disordered affair? Nat. Rev. Mol. Cell Biol. 13, 436-447. doi: 10.1038/nrm3382
37. Luger, K., Mäder, A. W., Richmond, R. K., Sargent, D. F., and Richmond, T. J. (1997). Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389, 251-260. doi: 10.1038/38444
38. Lyko, F., Ramsahoye, B. H., and Jaenisch, R. (2000). DNA methylation in Drosophila melanogaster. Nature 408, 538-540. doi: 10.1038/35046205
39. Malmquist, N. A., Moss, T. A., Mecheri, S., Scherf, A., and Fuchter, M. J. (2012). Small-molecule histone methyltransferase inhibitors display rapid antimalarial activity against all blood stage forms in Plasmodium falciparum. Proc. Natl. Acad. Sci. U.S.A. 109, 16708-16713. doi: 10.1073/pnas.1205414109
40. Marek, M., Kannan, S., Hauser, A. T., Moraes Mourão, M., Caby, S., Cura, V., et al. (2013). Structural basis for the inhibition of histone deacetylase 8 (HDAC8), a key epigenetic player in the blood fluke Schistosoma mansoni. PLoS Pathog. 9:e1003645. doi: 10.1371/journal.ppat.1003645
41. Mariño-Ramírez, L., Jordan, I. K., and Landsman, D. (2006). Multiple independent evolutionary solutions to core histone gene regulation. Genome Biol. 7:R122. doi: 10.1186/gb-2006-7-12-r122
42. Melters, D. P., Paliulis, L. V., Korf, I. F., and Chan, S. W. (2012). Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis. Chromosome Res. 20, 579-593. doi: 10.1007/s10577-012-9292-1
43. Mourão, M. M., Grunau, C., LoVerde, P. T., Jones, M. K., and Oliveira, G. (2012). Recent advances in Schistosoma genomics. Parasite Immunol. 34, 151-162. doi: 10.1111/j.1365-3024.2011.01349.x
44. Niu, W., Lu, Z. J., Zhong, M., Sarov, M., Murray, J. I., Brdlik, C. M., et al. (2011). Diverse transcription factor binding features revealed by genome-wide ChIP-seq in C. elegans. Genome Res. 21, 245-254. doi: 10.1101/gr.114587.110
45. Perrin, C., Lepesant, J. M., Roger, E., Duval, D., Fneich, S., Thuillier, V., et al. (2013). Schistosoma mansoni mucin gene (SmPoMuc) expression: epigenetic control to shape adaptation to a new host. PLoS Pathog. 9:e1003571. doi: 10.1371/journal.ppat.1003571
46. Pierce, R. J., Dubois-Abdesselem, F., Lancelot, J., Andrade, L., and Oliveira, G. (2012). Targeting schistosome histone modifying enzymes for drug development. Curr. Pharm. Des. 18, 3567-3578. doi: 10.2174/138161212801327248
47. Rando, O. J. (2011). Genome-wide measurement of histone H3 replacement dynamics in yeast. Methods Mol. Biol. 759, 41-60. doi: 10.1007/978-1-61779-173-4_3
48. Rosso, M. N., Favery, B., Piotte, C., Arthaud, L., De Boer, J. M., Hussey, R. S., et al. (1999). Isolation of a cDNA encoding a beta-1,4-endoglucanase in the root-knot nematode Meloidogyne incognita and expression analysis during plant parasitism. Mol. Plant-Microbe Interact. 12, 585-591. doi: 10.1094/MPMI.1999.12.7.585
49. Semblat, J. P., Bongiovanni, M., Wajnberg, E., Dalmasso, A., Abad, P., and Castagnone-Sereno, P. (2000). Virulence and molecular diversity of parthenogenetic root-knot nematodes, Meloidogyne spp. Heredity 84, 81-89. doi: 10.1046/j.1365-2540.2000.00633.x
50. Simpson, V. J., Johnson, T. E., and Hammen, R. F. (1986). Caenorhabditis elegans DNA does not contain 5-methylcytosine at any time during development or aging. Nucleic Acids Res. 14, 6711-6719. doi: 10.1093/nar/14.16.6711
51. Strahl, B. D., and Allis, C. D. (2000). The language of covalent histone modifications. Nature 403, 41-45. doi: 10.1038/47412
52. Subirana, J. A., and Messeguer, X. (2013). A satellite explosion in the genome of holocentric nematodes. PLoS ONE 8:e62221. doi: 10.1371/journal.pone.0062221
53. Suzuki, M. M., and Bird, A. (2008). DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet. 9, 465-476. doi: 10.1038/nrg2341
54. Triantaphyllou, A. C. (1981). Oogenesis and the Chromosomes of the Parthenogenic Root-knot Nematode Meloidogyne incognita. J. Nematol. 13, 95-104.
55. Triantaphyllou, A. C. (1983). "Cytogenetic aspects of nematode evolution," in Concepts in Nematode Systematics, eds A. R. Stone, H. M. Platt, and L. F. Khalil (London: Academic Press), 55-71.
56. Trojer, P., and Reinberg, D. (2007). Facultative heterochromatin: is there a distinctive molecular signature? Mol. Cell 28, 1-13. doi: 10.1016/j.molcel.2007.09.011
57. Turner, B. M. (1993). Decoding the nucleosome. Cell 75, 5-8. doi: 10.1016/0092-8674(93)90673-E
58. Turner, B. M. (2005). Reading signals on the nucleosome with a new nomenclature for modified histones. Nat. Struct. Mol. Biol. 12, 110-112. doi: 10.1038/nsmb0205-110
59. Turner, B. M. (2012). The adjustable nucleosome: an epigenetic signaling module. Trends Genet. 28, 436-444. doi: 10.1016/j.tig.2012.04.003
60. Urieli-Shoval, S., Gruenbaum, Y., Sedat, J., and Razin, A. (1982). The absence of detectable methylated bases in Drosophila melanogaster DNA. FEBS Lett. 146, 148-152. doi: 10.1016/0014-5793(82)80723-0
61. Verhoeven, K. J., and Preite, V. (2014). Epigenetic variation in asexually reproducing organisms. Evolution 68, 644-655. doi: 10.1111/evo.12320
62. Wenzel, D., Palladino, F., and Jedrusik-Bode, M. (2011). Epigenetics in C. elegans: facts and challenges. Genesis 49, 647-661. doi: 10.1002/dvg.20762
63. Winnepenninckx, B., Backeljau, T., and De Wachter, R. (1993). Extraction of high molecular weight DNA from molluscs. Trends Genet. 9, 407. doi: 10.1016/0168-9525(93)90102-N
64. Youngson, N. A., and Whitelaw, E. (2008). Transgenerational epigenetic effects. Annu. Rev. Genomics Hum. Genet. 9, 233-257. doi: 10.1146/annurev.genom.9.081307.164445