The transcriptome of Nacobbus aberrans reveals insights into the evolution of sedentary endoparasitism in plant-parasitic nematodes

Genome Biology and Evolution

Volumn 6, Issue 9, 2014, Pages 2181-2194

  Eves Van Den Akker, Sebastian ^a,b   Lilley, Catherine J ^a   Danchin, Etienne G J ^c   Rancurel, Corinne ^c   Cock, Peter J A ^b   Urwin, Peter E ^a   Jones, John T ^b  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^c CNRS   (France)

Author keywords

Effectors; Host mimics; Lateral gene transfer; Phylogenetics; Plant parasitic nematode; RNAseq

Indexed keywords

HELMINTH PROTEIN; TRANSCRIPTOME;

ANIMAL; CLASSIFICATION; EVOLUTION; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; HOST RANGE; METABOLISM; MOLECULAR GENETICS; PARASITOLOGY; PHYLOGENY; PHYSIOLOGY; PLANT DISEASE; SEQUENCE ALIGNMENT; TOBACCO; TYLENCHOIDEA;

ANIMALS; BIOLOGICAL EVOLUTION; FEMALE; HELMINTH PROTEINS; HOST SPECIFICITY; HOST-PARASITE INTERACTIONS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT DISEASES; SEQUENCE ALIGNMENT; TOBACCO; TRANSCRIPTOME; TYLENCHOIDEA;

EID: 84907572840     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evu171     Document Type: Article

References (65)

1. Abad P, et al. 2008. Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol. 26:909-915.
2. Anthoine G, Gauthier JP, Mugniéry D. 2006. Éléments de biologie chez Nacobbus aberrans (Thorne, 1935) Thorne & Allen, 1944 (Nematoda: Pratylenchidae):1-Capacités de quiescence et de diapause. EPPO Bull. 36:359-364.
3. Atkinson HJ, Urwin PE, Hansen E, McPherson MJ. 1995. Designs for engineered resistance to root-parasitic nematodes. Trends Biotechnol. 13:369-374.
4. Bailey TL, et al. 2009. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37:W202-W208.
5. Bateman A, et al. 2004. The Pfam protein families database. Nucleic Acids Res. 32:D138-D141.
6. Bauters L, Haegeman A, Kyndt T, Gheysen G. 2014. Analysis of the transcriptome of Hirschmanniella oryzae to explore potential survival strategies and host-nematode interactions. Mol Plant Pathol. 15:352-363.
7. Bird DM, Jones JT, Opperman CH, Kikuchi T, Danchin EG. 2014. Signatures of adaptation to plant parasitism in nematode genomes. Parasitology 1-14.
8. Bobay BG, et al. 2013. Solution NMR studies of the plant peptide hormone CEP inform function. FEBS Lett. 587:3979-3985.
9. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114-2120.
10. Boratyn GM, et al. 2013. BLAST: a more efficient report with usability improvements. Nucleic Acids Res. 41:W29-W33.
11. Brodie BB, Evans K, Franco J. 1993. Nematode parasites of potatoes. In: Nickle WR, editor. Plant and insect nematodes. New York and Basel: Marcell Dekker, Inc. p. 169-181.
12. Conesa A, et al. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674-3676.
13. Consortium S. 1998. Genome sequence of the nematode C. Elegans: a platform for investigating biology. Science 282:2012-2018.
14. Cotton JA, et al. 2014. The genome and life-stage specific transcriptomes of Globodera pallida elucidate key aspects of plant parasitism by a cyst nematode. Genome Biol. 15:R43.
15. Danchin EGJ, et al. 2010. Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc Natl Acad Sci USA. 107:17651-17656.
16. De Almeida Engler J, et al. 1999. Molecular markers and cell cycle inhibitors show the importance of cell cycle progression in nematode-induced galls and syncytia. Plant Cell 11:793-807.
17. De Almeida Engler J, Gheysen G. 2013. Nematode-induced endoreduplication in plant host cells: why and how? Mol Plant Microbe Interact. 26:17-24.
18. Doncaster C. 2012. Feeding in plant parasitic nematodes: mechanisms and behavior. In: Zuckerman B, editor. Plant parasitic nematodes, Vol. 2. Elsevier. p. 137-157.
19. Eddy SR. 2011. Accelerated profile HMM searches. PLoS Comput Biol. 7:e1002195.
20. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
21. Flot J-F, et al. 2013. Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. Nature 500:453-457.
22. Franco J. 1994. Nematode potato production problems in temperate climates of the Andean region. Nematropica 24:179-195.
23. Gao BL, et al. 2003. The parasitome of the phytonematode Heterodera glycines. Mol Plant Microbe Interact. 16:720-726.
24. Geraert E. 1994. The origin of the gelatinous matrix in plant-parasitic nematodes. Nematologica 40:150-151.
25. Gladyshev EA, Meselson M, Arkhipova IR. 2008. Massive horizontal gene transfer in bdelloid rotifers. Science 320:1210-1213.
26. Grabherr MG, et al. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 29:644-652.
27. Haas BJ, et al. 2013. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 8:1494-1512.
28. Haegeman A, Jones JT, Danchin EGJ. 2011. Horizontal gene transfer in nematodes: a catalyst for plant parasitism? Mol Plant Microbe Interact. 24:879-887.
29. Haegeman A, Joseph S, Gheysen G. 2011. Analysis of the transcriptome of the root lesion nematode Pratylenchus coffeae generated by 454 sequencing technology. Mol Biochem Parasitol. 178:7-14.
30. Haegeman A, Mantelin S, Jones JT, Gheysen G. 2012. Functional roles of effectors of plant-parasitic nematodes. Gene 492:19-31.
31. Hewezi T, Baum TJ. 2013. Manipulation of plant cells by cyst and root-knot nematode effectors. Mol Plant Microbe Interact. 26:9-16.
32. Holterman M, et al. 2006. Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Mol Biol Evol. 23:1792-1800.
33. Holterman M, et al. 2009. Small Subunit rDNA-based phylogeny of the tylenchida sheds light on relationships among some high-impact plantparasitic nematodes and the evolution of plant feeding. Phytopathology 99:227-235.
34. Huang G, et al. 2003. A profile of putative parasitism genes expressed in the esophageal gland cells of the root-knot nematode Meloidogyne incognita. Mol Plant Microbe Interact. 16:376-381.
35. Huang X, Madan A. 1999. CAP3: a DNA sequence assembly program. Genome Res. 9:868-877.
36. Imin N, Mohd-Radzman NA, Ogilvie HA, Djordjevic MA. 2013. The peptide-encoding CEP1 gene modulates lateral root and nodule numbers in Medicago truncatula. J Exp Bot. 64:5395-5409.
37. Jaubert S, Laffaire JB, Abad P, Rosso MN. 2002. A polygalacturonase of animal origin isolated from the root-knot nematode Meloidogyne incognita. FEBS Lett. 522:109-112.
38. Jones JT, et al. 2013. Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol. 14:946-961.
39. Jones MGK, Payne HL. 1977. Structure of syncytia induced by phytoparasitic nematode Nacobbus aberrans in tomato roots, and possible role of plasmodesmata in their nutrition. J Cell Sci. 23:299-313.
40. Lax P, Rondan Dueñas JC, Gardenal CN, Doucet ME. 2013. Phylogenetic relationships among populations of the Nacobbus aberrans (Nematoda, Pratylenchidae) complex reveal the existence of cryptic species. Zool Scr. 43:184-192.
41. Lehman P. 2004. Cost-benefits of nematode management through regulatory programs. In: Chen ZX, Chen SY, Dickson DW, editors. Nematology: advances and perspectives, Vol. 2. CABI Publishing. p. 1133-1177.
42. Li B, Dewey CN. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323.
43. Lu S-W, et al. 2009. Structural and Functional Diversity of CLAVATA3/ESR (CLE)-like genes from the potato cyst nematode Globodera rostochiensis. Mol Plant Microbe Interact. 22:1128-1142.
44. Manzanilla-López RH. 2010. Speciation within Nacobbus: consilience or controversy? Nematology 12:321-334.
45. Manzanilla-López RH, et al. 2002. The genus Nacobbus Thorne & Allen, 1944 (Nematoda: Pratylenchidae): systematics, distribution, biology and management. Nematropica 32:149-227.
46. Milne I, et al. 2009. TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics 25:126-127.
47. Nicol JM, 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. Springer. p. 21.
48. Opperman CH, et al. 2008. Sequence and genetic map of Meloidogyne hapla: a compact nematode genome for plant parasitism. Proc Natl Acad Sci USA. 105:14802-14807.
49. Parra G, Bradnam K, Korf I. 2007. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23:1061-1067.
50. Postma WJ, et al. 2012. The effector SPRYSEC-19 of Globodera rostochiensis suppresses CC-NB-LRR-mediated disease resistance in plants. Plant Physiol. 160:944-954.
51. Qin L, et al. 2000. An efficient cDNA-AFLP-based strategy for the identification of putative pathogenicity factors from the potato cyst nematode Globodera rostochiensis. Mol Plant Microbe Interact. 13:830-836.
52. Replogle A, et al. 2011. Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE. PlJ. 65:430-440.
53. Robinson AF, Inserra RN, Caswell-Chen EP, Vovlas N, Troccoli A. 1998. Rotylenchulus species: identification, distribution, host ranges, and crop plant resistance. Nematropica 27:127-180.
54. Robinson MD, McCarthy DJ, Smyth GK. 2010. EdgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139-140.
55. Sanderson MJ, Shaffer HB. 2002. Troubleshooting molecular phylogenetic analyses. Annu Rev Ecol Syst. 33:49-72.
56. Schliesky S, Gowik U, Weber AP, Bräutigam A. 2012. RNA-seq assembly-are we there yet? Front Plant Sci. 3:220.
57. Smith IM, McNamara DG, Scott PR, Harris KM. 1992. In: Smith IM, McNamara DG, Scott PR, Holderness M, editors, Quarantine pests for Europe: data sheets on quarantine pests for the European Communities and for the European and Mediterranean Plant Protection Organization. Wallingford (United Kingdom): CAB International.
58. Trapnell C, et al. 2013. Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol. 31:46-53.
59. Van Megen H, et al. 2009. A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11:927-950.
60. Vanholme B, Haegeman A, Jacob J, Cannoot B, Gheysen G. 2009. Arabinogalactan endo-1, 4-galactosidase: a putative plant cell walldegrading enzyme of plant-parasitic nematodes. Nematology 11:739-747.
61. Vovlas N, Nico AI, De Luca F, De Giorgi C, Castillo P. 2007. Diagnosis and molecular variability of an Argentinean population of Nacobbus aberrans with some observations on histopathology in tomato. J Nematol. 39:17.
62. Wang J, et al. 2011. Identification of potential host plant mimics of CLAVATA3/ESR (CLE)-like peptides from the plant-parasitic nematode Heterodera schachtii. Mol Plant Pathol. 12:177-186.
63. Wang XH, et al. 2005. A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Mol Plant Pathol. 6:187-191.
64. Wyss U, Grundler FMW. 1992. Feeding-behavior of sedentary plant parasitic nematodes. Neth J Plant Pathol 98:165-173.
65. Yang Y, Smith SA. 2013. Optimizing de novo assembly of short-read RNA-seq data for phylogenomics. BMC Genomics 14:328.