Abstract
Recent comparisons of the increasing number of genome sequences have revealed that variation in gene content is considerably more prevalent than previously thought. This variation is likely to have a pronounced effect on phenotypic diversity and represents a crucial target for the assessment of genomic diversity. Leptosphaeria maculans, a causative agent of phoma stem canker, is the most devastating fungal pathogen of Brassica napus (oilseed rape/canola). A number of L. maculans genes are known to be present in some isolates but lost in the others. We analyse gene content variation within three L. maculans isolates using a hybrid mapping and genome assembly approach and identify genes which are present in one of the isolates but missing in the others. In total, 57 genes are shown to be missing in at least one isolate. The genes encode proteins involved in a range of processes including oxidative processes, DNA maintenance, cell signalling and sexual reproduction. The results demonstrate the effectiveness of the method and provide new insight into genomic diversity in L. maculans.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bhatnagar D, Ehrlich KC, Cleveland TE (2003) Molecular genetic analysis and regulation of aflatoxin biosynthesis. Appl Microbiol Biotechnol 61:83–93. doi:10.1007/s00253-002-1199-x
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinforma 10:421. doi:10.1186/1471-2105-10-421
Carvunis A-R et al (2012) Proto-genes and de novo gene birth. Nature 487:370–374. doi:10.1038/nature11184
Cerniglia CE, Hebert RL, Szaniszlo PJ, Gibson DT (1978) Fungal transformation of naphthalene. Arch Microbiol 117:135–143. doi:10.1007/BF00402301
Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics (Oxford, England) 21:3674–3676. doi:10.1093/bioinformatics/bti610
Cozijnsen AJ, Howlett BJ (2003) Characterisation of the mating-type locus of the plant pathogenic ascomycete Leptosphaeria maculans. Curr Genet 43:351–357. doi:10.1007/s00294-003-0391-6
Crešnar B, Petrič S (2011) Cytochrome P450 enzymes in the fungal kingdom. Biochim Biophys Acta (BBA) - Proteins Proteomics 1814:29–35. doi:10.1016/j.bbapap.2010.06.020
da Silva M, Esposito E, Moody JD, Canhos VP, Cerniglia CE (2004) Metabolism of aromatic hydrocarbons by the filamentous fungus Cyclothyrium sp. Chemosphere 57:943–952. doi:10.1016/j.chemosphere.2004.07.051
Devos KM, Brown JKM, Bennetzen JL (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12:1075–1079. doi:10.1101/gr.132102
Fitt BD, Evans N, Howlett BJ, Cooke M (2006) Sustainable strategies for managing Brassica napus (oilseed rape) resistance to Leptosphaeria maculans (phoma stem canker) vol 114. Springer
Foissac S et al (2008) Genome annotation in plants and fungi: EuGene as a model platform. Curr Bioinforma 3:87–97
Fudal I et al (2009) Repeat-induced point mutation (RIP) as an alternative mechanism of evolution toward virulence in Leptosphaeria maculans. Mol Plant-Microbe Interact 22:932–941. doi:10.1094/MPMI-22-8-0932
George H, Hirschi K, VanEtten H (1998) Biochemical properties of the products of cytochrome P450 genes (PDA) encoding pisatin demethylase activity in Nectria haematococca. Arch Microbiol 170:147–154. doi:10.1007/s002030050627
Gout L et al (2006) Lost in the middle of nowhere: the AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans. Mol Microbiol 60:67–80. doi:10.1111/j.1365-2958.2006.05076.x
Gout L et al (2007) Genome structure impacts molecular evolution at the AvrLm1 avirulence locus of the plant pathogen Leptosphaeria maculans. Environ Microbiol 9:2978–2992. doi:10.1111/j.1462-2920.2007.01408.x
Hardie DG (1999) Plant protein serine/threonine kinases: classification and functions. Annu Rev Plant Physiol Plant Mol Biol 50:97–131. doi:10.1146/annurev.arplant.50.1.97
Huang J, Si W, Deng Q, Li P, Yang S (2014) Rapid evolution of avirulence genes in rice blast fungus Magnaporthe oryzae. BMC Genet 15:45
Keeling PJ, Palmer JD (2008) Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 9:605–618. doi:10.1038/nrg2386
Lander ES, Waterman MS (1988) Genomic mapping by fingerprinting random clones: a mathematical analysis. Genomics 2:231–239. doi:10.1016/0888-7543(88)90007-9
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760. doi:10.1093/bioinformatics/btp324
Ma L-J et al (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:367–373. doi:10.1038/nature08850
McDonald MC, Oliver RP, Friesen TL, Brunner PC, McDonald BA (2013) Global diversity and distribution of three necrotrophic effectors in Phaeosphaeria nodorum and related species. New Phytol 199:241–251. doi:10.1111/nph.12257
Mills RE et al (2011) Mapping copy number variation by population-scale genome sequencing. Nature 470:59–65. doi:10.1038/nature09708
Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A (2005) Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet 37:997–1002
Oliver KR, Greene WK (2009) Transposable elements: powerful facilitators of evolution. BioEssays 31:703–714. doi:10.1002/bies.200800219
Oliver R (2012) Genomic tillage and the harvest of fungal phytopathogens. New Phytol 196:1015–1023. doi:10.1111/j.1469-8137.2012.04330.x
Park J et al (2008) Fungal Cytochrome P450 Database. BMC Genomics 9:402. doi:10.1186/1471-2164-9-402
Parker IM, Gilbert GS (2004) The evolutionary ecology of novel plant-pathogen interactions. Annu Rev Ecol Evol Syst 35:675–700. doi:10.1146/annurev.ecolsys.34.011802.132339
Raffaele S, Kamoun S (2012) Genome evolution in filamentous plant pathogens: why bigger can be better. Nat Rev Micro 10:417–430
Raman R et al (2012) Molecular mapping of qualitative and quantitative loci for resistance to Leptosphaeria maculans causing blackleg disease in canola (Brassica napus L.). Theor Appl Genet 125:405–418. doi:10.1007/s00122-012-1842-6
Richards TA (2011) Genome evolution: horizontal movements in the fungi. Curr Biol 21:R166–R168. doi:10.1016/j.cub.2011.01.028
Rojas MC, Hedden P, Gaskin P, Tudzynski B (2001) The P450-1 gene of Gibberella fujikuroi encodes a multifunctional enzyme in gibberellin biosynthesis. Proc Natl Acad Sci 98:5838–5843. doi:10.1073/pnas.091096298
Rouxel T et al (2011) Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat-induced point mutations. Nat Commun 2:202. doi:10.1038/ncomms1189
Rudrabhatla P, Reddy MM, Rajasekharan R (2006) Genome-wide analysis and experimentation of plant serine/ threonine/tyrosine-specific protein kinases. Plant Mol Biol 60:293–319. doi:10.1007/s11103-005-4109-7
Sutherland JB (1992) Detoxification of polycyclic aromatic hydrocarbons by fungi. J Ind Microbiol 9:53–61. doi:10.1007/BF01576368
Syme RA, Hane JK, Friesen TL, Oliver RP (2013) Resequencing and comparative genomics of Stagonospora nodorum: sectional gene absence and effector discovery. G3: Genes|Genomes|Genetics 3:959–969
Tan S, Zhong Y, Hou H, Yang S, Tian D (2012) Variation of presence/absence genes among Arabidopsis populations. BMC Evol Biol 12:86. doi:10.1186/1471-2148-12-86
Tautz D, Domazet-Lošo T (2011) The evolutionary origin of orphan genes. Nat Rev Genet 12:692–702
Umate P, Tuteja N, Tuteja R (2011) Genome-wide comprehensive analysis of human helicases. Commun Integr Biol 4:118–137. doi:10.4161/cib.4.1.13844
URGI Unite Recherche Genomique Info (2010) Plant and fungi data integration. URGI. http://urgi.versailles.inra.fr/Species/Leptosphaeria/Sequences-Databases/Download. 2014
Van de Wouw AP, Cozijnsen AJ, Hane JK, Brunner PC, McDonald BA, Oliver RP, Howlett BJ (2010) Evolution of linked avirulence effectors in Leptosphaeria maculans is affected by genomic environment and exposure to resistance genes in host plants. PLoS Pathog 6:e1001180. doi:10.1371/journal.ppat.1001180
Venn L (1979) The genetic control of sexual compatibility in Leptosphaeria maculans. Australas Plant Pathol 8:5–6. doi:10.1071/APP9790005
Wickham H (2009) ggplot2: elegant graphics for data analysis. New York
Wu Y (2012) Unwinding and rewinding: double faces of helicase? J Nucleic Acids 2012:140601. doi:10.1155/2012/140601
Yin T, Cook D, Lawrence M (2012) ggbio: an R package for extending the grammar of graphics for genomic data. Genome Biol 13:R77. doi:10.1186/gb-2012-13-8-r77
Zander M et al (2013) Identifying genetic diversity of avirulence genes in Leptosphaeria maculans using whole genome sequencing. Funct Integr Genomics 13:295–308. doi:10.1007/s10142-013-0324-5
Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829
Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18:292–298. doi:10.1016/S0169-5347(03)00033-8
Zhang L-M, Luo H, Liu Z-Q, Zhao Y, Luo J-C, Hao D-Y, Jing H-C (2014) Genome-wide patterns of large-size presence/absence variants in sorghum. J Integr Plant Biol 56:24–37. doi:10.1111/jipb.12121
Zheng D et al (2007) Pseudogenes in the ENCODE regions: consensus annotation, analysis of transcription, and evolution. Genome Res 17:839–851. doi:10.1101/gr.5586307
Zheng L-Y et al (2011) Genome-wide patterns of genetic variation in sweet and grain sorghum (Sorghum bicolor). Genome Biol 12:R114. doi:10.1186/gb-2011-12-11-r114
Acknowledgments
The authors would like to acknowledge the funding support from the Australian Research Council (Projects LP0882095, LP0883462, LP0989200, LP110100200 and DP0985953).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Golicz, A.A., Martinez, P.A., Zander, M. et al. Gene loss in the fungal canola pathogen Leptosphaeria maculans . Funct Integr Genomics 15, 189–196 (2015). https://doi.org/10.1007/s10142-014-0412-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-014-0412-1