Genomes and transcriptomes of partners in plant-fungal- interactions between canola (Brassica napus) and two Leptosphaeria species

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Lowe, Rohan G T ^a   Cassin, Andrew ^a   Grandaubert, Jonathan ^b   Clark, Bethany L ^a   Van De Wouw, Angela P ^a   Rouxel, Thierry ^b   Howlett, Barbara J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b INRA Institut National de la Recherche Agronomique   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE BINDING PROTEIN; ISOCHORISMATE SYNTHASE 1; JASMONIC ACID; PEPTIDASE; SALICYLIC ACID; SYNTHETASE; TRANSCRIPTOME; TRYPSIN; UNCLASSIFIED DRUG; PEPTIDE HYDROLASE;

ACS2A GENE; ARTICLE; AVRLM1 GENE; AVRLM4 7 GENE; AVRLMJ1 GENE; CBM50 GENE; CHI GENE; CONTROLLED STUDY; COTYLEDON; FUNGAL CELL WALL; FUNGAL GENOME; FUNGAL VIRULENCE; GENE; GENETIC TRAIT; GENETIC TRANSCRIPTION; HEL GENE; HOST; HOST RESISTANCE; ICS1 GENE; IMMUNE EVASION; IN VITRO STUDY; INNATE IMMUNITY; LEPTOSPHAERIA; LEPTOSPHAERIA BIGLOBOSA; LEPTOSPHAERIA MACULANS; LIFESTYLE; LM5LYSM GENE; METABOLISM; NCED3 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PDF1.2 GENE; PHOTOSYNTHESIS; PLANT DEFENSE; PLANT DISEASE; PLANT FUNGUS INTERACTION; PLANT GENOME; PR 1 GENE; PROTEIN DOMAIN; PROTEIN LOCALIZATION; RAPESEED; RNA SEQUENCE; UPREGULATION; WRKY70 GENE; ASCOMYCETES; CHEMISTRY; CLUSTER ANALYSIS; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; HOST PATHOGEN INTERACTION; MICROBIOLOGY; PHENOTYPE;

ASCOMYCOTA; BRASSICA NAPUS; CLUSTER ANALYSIS; COTYLEDON; GENE EXPRESSION REGULATION, FUNGAL; GENE EXPRESSION REGULATION, PLANT; GENOME, FUNGAL; GENOME, PLANT; GENOMICS; HOST-PATHOGEN INTERACTIONS; PEPTIDE HYDROLASES; PHENOTYPE; PLANT DISEASES; TRANSCRIPTOME;

EID: 84904861402     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0103098     Document Type: Article

References (52)

1. Oliver RP, Solomon PS (2010) New developments in pathogenicity and virulence of necrotrophs. Curr Opin Plant Biol 13: 415-419.
2. Rouxel T, Grandaubert J, Hane JK, Hoede C, van de Wouw AP, et al. (2011) Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations. Nat Comm 2: 202.
3. Shoemaker RA, Brun H (2001) The teleomorph of the weakly aggressive segregate of Leptosphaeria maculans. Can J Bot 79: 412-419. (Pubitemid 32783838)
4. Voigt K, Cozijnsen AJ, Kroymann J, Pöggeler S, Howlett BJ (2005) Phylogenetic relationships between members of the crucifer pathogenic Leptosphaeria maculans species complex as shown by mating type (MAT1-2), actin, and β-tubulin sequences. Mol Phylogenet Evol 37: 541-557. (Pubitemid 41434039)
5. de Gruyter J, Woudenberg JHC, Aveskamp MM, Verkley GJM, Groenewald JZ, et al. (2013) Redisposition of phoma-like anamorphs in Pleosporales. Stud Mycol 75: 1-36.
6. Howlett BJ (2004) Current knowledge of the interaction between Brassica napus and Leptosphaeria maculans. Can J Plant Pathol 26: 245-252.
7. Van de Wouw A, Thomas V, Cozijnsen A, Marcroft S, Salisbury P, et al. (2008) Identification of Leptosphaeria biglobosa 'canadensis' on Brassica juncea stubble from northern New South Wales, Australia. Australas Plant D Notes 3: 124-128.
8. Gout L, Fudal I, Kuhn ML, Blaise F, Eckert M, et al. (2006) Lost in the middle of nowhere: the AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans. Mol Microbiol 60: 67-80. (Pubitemid 43363288)
9. Fudal I, Ross S, Gout L, Blaise F, Kuhn ML, et al. (2007) Heterochromatin-like regions as ecological niches for avirulence genes in the Leptosphaeria maculans genome: map-based cloning of AvrLm6. Mol Plant Microbe Interact 20: 459-470. (Pubitemid 46449404)
10. Balesdent MH, Fudal I, Ollivier B, Bally P, Grandaubert J, et al. (2013) The dispensable chromosome of Leptosphaeria maculans shelters an effector gene conferring avirulence towards Brassica rapa. New Phytol 198: 887-898.
11. Parlange F, Daverdin G, Fudal I, Kuhn ML, Balesdent MH, et al. (2009) Leptosphaeria maculans avirulence gene AvrLm4-7 confers a dual recognition specificity by the Rlm4 and Rlm7 resistance genes of oilseed rape, and circumvents Rlm4-mediated recognition through a single amino acid change. Mol Microbiol 71: 851-863.
12. Van de Wouw AP, Lowe RGT, Elliott CE, Dubois DJ, Howlett BJ (2013) An avirulence gene, AvrLmJ1, from the blackleg fungus, Leptosphaeria maculans, confers avirulence to Brassica juncea cultivars. Mol Plant Pathol doi:10.1111/mpp.12105.
13. Larkan NJ, Lydiate DJ, Parkin IAP, Nelson MN, Epp DJ, et al. (2013) The Brassica napus blackleg resistance gene LepR3 encodes a receptor-like protein triggered by the Leptosphaeria maculans effector AVRLM1. New Phytol 197: 595-605.
14. Rubartelli A, Lotze MT (2007) Inside, outside, upside down: damage-associated molecular-pattern molecules (DAMPs) and redox. Trends Immunol 28: 429-436. (Pubitemid 47444554)
15. Baxter L, Tripathy S, Ishaque N, Boot N, Cabral A, et al. (2010) Signatures of Adaptation to Obligate Biotrophy in the Hyaloperonospora arabidopsidis Genome. Science 330: 1549-1551.
16. Duplessis S, Cuomo CA, Lin Y, Aerts A, Tisserant E, et al. (2011) Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci U S A 108: 9166-9171.
17. Spanu PD, Abbott JC, Amselem J, Burgis TA, Soanes DM, et al. (2010) Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330: 1543-1546.
18. Ohm RA, Feau N, Henrissat B, Schoch CL, Horwitz BA, et al. (2012) Diverse Lifestyles and Strategies of Plant Pathogenesis Encoded in the Genomes of Eighteen Dothideomycetes Fungi. Plos Pathog 8: e1003037.
19. Palmer CL, Skinner W (2002) Mycosphaerella graminicola: latent infection, crop devastation and genomics. Mol Plant Pathol 3: 63-70.
20. Solomon PS, Lowe RG, Tan KC, Waters OD, Oliver RP (2006) Stagonospora nodorum: cause of stagonospora nodorum blotch of wheat. Mol Plant Pathol 7: 147-156.
21. Liu Z, Ellwood SR, Oliver RP, Friesen TL (2011) Pyrenophora teres: profile of an increasingly damaging barley pathogen. Mol Plant Pathol 12: 1-19.
22. Westermann AJ, Gorski SA, Vogel J (2012) Dual RNA-seq of pathogen and host. Nat Rev Micro 10: 618-630.
23. Kawahara Y, Oono Y, Kanamori H, Matsumoto T, Itoh T, et al. (2012) Simultaneous RNA-seq analysis of a mixed transcriptome of rice and blast fungus interaction. PLoS One 7: e49423.
24. Yazawa T, Kawahigashi H, Matsumoto T, Mizuno H (2013) Simultaneous Transcriptome Analysis of Sorghum and Bipolaris sorghicola by Using RNA-seq in Combination with De Novo Transcriptome Assembly. PLoS One 8: e62460.
25. Purwantara A, Salisbury PA, Burton WA, Howlett BJ (1998) Reaction of Brassica juncea (Indian mustard) lines to Australian isolates of Leptosphaeria maculans under glasshouse and field conditions. Eur J Plant Pathol 104: 895-902. (Pubitemid 29158050)
26. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
27. Love CG, Graham NS, ÓLochlainn S, Bowen HC, May ST, et al. (2010) A Brassica Exon Array for Whole-Transcript Gene Expression Profiling. PLoS One 5: e12812.
28. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotech 28: 511-515.
29. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, et al. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37: D233-D238.
30. Yin Y, Mao X, Yang J, Chen X, Mao F, et al. (2012) dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 40: W445-W451.
31. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Meth 8: 785-786.
32. Eddy SR (2011) Accelerated Profile HMM Searches. Plos Comput Biol 7: e1002195.
33. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, et al. (2012) The Pfam protein families database. Nucleic Acids Res 40: D290-D301.
34. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, et al. (2011) Integrative genomics viewer. Nat Biotech 29: 24-26.
35. de Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y, et al. (2010) Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329: 953-955.
36. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
37. Rawlings ND, Barrett AJ, Bateman A (2012) MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 40: D343-D350.
38. Epple P, Apel K, Bohlmann H (1997) ESTs reveal a multigene family for plant defensins in Arabidopsis thaliana. Febs Lett 400: 168-172. (Pubitemid 27036315)
39. Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, et al. (2004) Mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37: 914-939. (Pubitemid 38370342)
40. Eckert M, Maguire K, Urban M, Foster S, Fitt B, et al. (2005) Agrobacterium tumefaciens-mediated transformation of Leptosphaeria spp. and Oculimacula spp. with the reef coral gene DsRed and the jellyfish gene gfp. Fems Microbiol Lett 253: 67-74. (Pubitemid 41605396)
41. Zablackis E, Huang J, Muller B, Darvill AG, Albersheim P (1995) Characterization of the cell-wall polysaccharides of Arabidopsis thaliana leaves. Plant Physiol 107: 1129-1138.
42. Ipcho SV, Hane JK, Antoni EA, Ahren D, Henrissat B, et al. (2012) Transcriptome analysis of Stagonospora nodorum: gene models, effectors, metabolism and pantothenate dispensability. Mol Plant Pathol 13: 531-545.
43. Levasseur A, Drula E, Lombard V, Coutinho PM, Henrissat B (2013) Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnology for biofuels 6: 41.
44. Brunner PC, Torriani SFF, Croll D, Stukenbrock EH, McDonald BA (2013) Coevolution and life cycle specialization of plant cell wall degrading enzymes in a hemibiotrophic pathogen. Mol Biol Evol 30: 1337-1347.
45. Feng J, Zhang H, Strelkov SE, Hwang SF (2014) The LmSNF1 gene is required for pathogenicity in the canola blackleg pathogen Leptosphaeria maculans. PLoS One 9: e92503.
46. O'Connell RJ, Thon MR, Hacquard S, Amyotte SG, Kleemann J, et al. (2012) Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet.
47. Rypniewski WR, Hastrup S, Betzel C, Dauter M, Dauter Z, et al. (1993) The sequence and X-ray structure of the trypsin from Fusarium oxysporum. Protein Eng 6: 341-348. (Pubitemid 23197392)
48. Showalter AM, Keppler B, Lichtenberg J, Gu D, Welch LR (2010) A bioinformatics approach to the identification, classification, and analysis of hydroxyproline-rich glycoproteins. Plant Physiol 153: 485-513.
49. Persson M, Staal J, Oide S, Dixelius C (2009) Layers of defense responses to Leptosphaeria maculans below the RLM1- and camalexin-dependent resistances. New Phytol 182: 470-482.
50. Šašek V, Nováková M, Jindř ichová B, Bóka K, Valentová O, et al. (2012) Recognition of Avirulence Gene AvrLm1 from Hemibiotrophic Ascomycete Leptosphaeria maculans Triggers Salicylic Acid and Ethylene Signaling in Brassica napus. Mol Plant Microbe Interact 25: 1238-1250.
51. Vogel JP (2002) PMR6, a Pectate Lyase-Like Gene Required for Powdery Mildew Susceptibility in Arabidopsis. Plant Cell 14: 2095-2106.
52. Grandaubert J, Lowe RGT, Soyer JL, Schoch CL, Fudal I, et al. (2014) Transposable Element-assisted evolution and adaptation to host plant within the Leptosphaeria maculans-Leptosphaeria biglobosa species complex of fungal pathogens. Biomed Cent Genomics. In press.