Transposable element genomic fissuring in Pyrenophora teres is associated with genome expansion and dynamics of host-pathogen genetic interactions

Article


Syme, Robert A., Martin, Anke, Wyatt, Nathan A., Lawrence, Julie A., Muria-Gonzalez, Mariano J., Friesen, Timothy L. and Ellwood, Simon R.. 2018. "Transposable element genomic fissuring in Pyrenophora teres is associated with genome expansion and dynamics of host-pathogen genetic interactions." Frontiers in Genetics. 9, pp. 1-15. https://doi.org/10.3389/fgene.2018.00130
Article Title

Transposable element genomic fissuring in Pyrenophora teres is associated with genome expansion and dynamics of host-pathogen genetic interactions

ERA Journal ID210481
Article CategoryArticle
AuthorsSyme, Robert A. (Author), Martin, Anke (Author), Wyatt, Nathan A. (Author), Lawrence, Julie A. (Author), Muria-Gonzalez, Mariano J. (Author), Friesen, Timothy L. (Author) and Ellwood, Simon R. (Author)
Journal TitleFrontiers in Genetics
Journal Citation9, pp. 1-15
Article Number130
Number of Pages15
Year2018
Place of PublicationSwitzerland
ISSN1664-8021
Digital Object Identifier (DOI)https://doi.org/10.3389/fgene.2018.00130
Web Address (URL)https://www.frontiersin.org/articles/10.3389/fgene.2018.00130/full
Abstract

Pyrenophora teres, P. teres f. teres (PTT) and P. teres f. maculate (PTM) cause significant diseases in barley, but little is known about the large-scale genomic differences that may distinguish the two forms. Comprehensive genome assemblies were constructed from long DNA reads, optical and genetic maps. As repeat masking in fungal genomes influences the final gene annotations, an accurate and reproducible pipeline was developed to ensure comparability between isolates. The genomes of the two forms are highly collinear, each composed of 12 chromosomes. Genome evolution in P teres is characterized by genome fissuring through the insertion and expansion of transposable elements (TEs), a process that isolates blocks of genic sequence. The phenomenon is particularly pronounced in PTT, which has a larger, more repetitive genome than PTM and more recent transposon activity measured by the frequency and size of genome fissures. PTT has a longer cultivated host association and, notably, a greater range of host-pathogen genetic interactions compared to other Pyrenophora spp., a property which associates better with genome size than pathogen lifestyle. The two forms possess similar complements of TE families with Tc1/Mariner and LINE-like Tad-1 elements more abundant in PTT. Tad-1 was only detectable as vestigial fragments in PTM and, within the forms, differences in genome sizes and the presence and absence of several TE families indicated recent lineage invasions. Gene differences between P. teres forms are mainly associated with gene-sparse regions near or within TE-rich regions, with many genes possessing characteristics of fungal effectors. Instances of gene interruption by transposons resulting in pseudogenization were detected in PTT. In addition, both forms have a large complement of secondary metabolite gene clusters indicating significant capacity to produce an array of different molecules. This study provides genomic resources for functional genetics to help dissect factors underlying the host-pathogen interactions.

Keywordsbarley net blotch, Hordeum vulgare, single molecule sequencing DNA, optical mapping, synteny, transposable element, repeat annotation
ANZSRC Field of Research 2020300409. Crop and pasture protection (incl. pests, diseases and weeds)
Byline AffiliationsCurtin University
Centre for Crop Health
North Dakota State University, United States
Institution of OriginUniversity of Southern Queensland
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Lehmensiek, A., Campbell, A. W., Williamson, P. M., Michalowitz, M., Sutherland, M. W. and Daggard, G. E.. 2004. "QTLs for black-point resistance in wheat and the identification of potential markers for use in breeding programmes." Plant Breeding. 123 (5), pp. 410-416. https://doi.org/10.1111/j.1439-0523.2004.01013.x
Resistance gene analogues of wheat: molecular genetic analysis of ESTs
McFadden, H. G., Lehmensiek, A. and Lagudah, E. S.. 2006. "Resistance gene analogues of wheat: molecular genetic analysis of ESTs." Theoretical and Applied Genetics: international journal of plant breeding research. 113 (6), pp. 987-1002. https://doi.org/10.1007/s00122-006-0358-3
Diversity arrays technology (DArT) for high-throughput profiling of the hexaploid wheat genome
Akbari, Mona, Wenzl, Peter, Caig, Vanessa, Carling, Jason, Xia, Ling, Yang, Shiying, Uszynski, Grzegorz, Mohler, Volker, Lehmensiek, Anke, Kuchel, Haydn, Hayden, Mathew J., Howes, Neil, Sharp, Peter, Vaughan, Peter, Rathmell, Bill, Huttner, Eric and Kilian, Andrzej. 2006. "Diversity arrays technology (DArT) for high-throughput profiling of the hexaploid wheat genome." Theoretical and Applied Genetics: international journal of plant breeding research. 113 (8), pp. 1409-1420. https://doi.org/10.1007/s00122-006-0365-4
Flour yield QTLs in three Australian doubled haploid wheat populations
Lehmensiek, A., Eckermann, P. J., Verbyla, A. P., Appels, R., Sutherland, M. W., Martin, D. and Daggard, G. E.. 2006. "Flour yield QTLs in three Australian doubled haploid wheat populations." Australian Journal of Agricultural Research. 57 (10), pp. 1115-1122. https://doi.org/10.1071/AR05375
Development of molecular markers for crown rot resistance in wheat: mapping of QTLs for seedling resistance in a '2-49' x 'Janz' population
Collard, B. C. Y., Grams, R. A., Bovill, W. D., Percy, C. D., Jolley, R., Lehmensiek, A., Wildermuth, G. B. and Sutherland, M. W.. 2005. "Development of molecular markers for crown rot resistance in wheat: mapping of QTLs for seedling resistance in a '2-49' x 'Janz' population." Plant Breeding. 124 (6), pp. 532-537. https://doi.org/10.1111/j.1439-0523.2005.01163.x
Molecular characterization of a Triticum timopheevii introgression in a Wentworth/Lang population
Lehmensiek, A., Bovill, W. D., Banks, P. M. and Sutherland, M. W.. 2008. "Molecular characterization of a Triticum timopheevii introgression in a Wentworth/Lang population." Appels, Rudi (ed.) 11th International Wheat Genetics Symposium 2008 (IWGS 2008). Brisbane, Australia 24 - 29 Aug 2008 Sydney, Australia.
Infection of wheat tissues by fusarium pseudograminearum
Knight, N. L., Percy, C., Lehmensiek, A., Herde, D. J. and Sutherland, M. W.. 2008. "Infection of wheat tissues by fusarium pseudograminearum." Appels, Rudi (ed.) 11th International Wheat Genetics Symposium 2008 (IWGS 2008). Brisbane, Australia 24 - 29 Aug 2008 Sydney, Australia.
Validation of black point QTL in wheat
Tah, P. R., Lehmensiek, A., Williamson, P. M., Michalowitz, M., Done, A. and Daggard, G. E.. 2008. "Validation of black point QTL in wheat." Appels, Rudi, Eastwood, Russell, Lagudah, Peter, Mackay, Michael, McIntyre, Lynne and Sharp, Peter J. (ed.) 11th International Wheat Genetics Symposium 2008 (IWGS 2008). Brisbane, Australia 24 - 29 Aug 2008 Sydney, Australia.
Identification of genetic regions associated with black point in barley
Tah, Priya R., Lehmensiek, A., Fox, Glen P., Mace, Emma, Sulman, Maria, Bloustein, Gary and Daggard, Grant E.. 2010. "Identification of genetic regions associated with black point in barley." Field Crops Research. 115 (1), pp. 61-66. https://doi.org/10.1016/j.fcr.2009.10.003
Molecular mapping of adult plant stripe rust resistance in wheat and identification of pyramided QTL genotypes
Bariana, H. S., Bansal, U. K., Schmidt, A., Lehmensiek, A., Kaur, J., Miah, H., Howes, N. and McIntyre, C. L.. 2010. "Molecular mapping of adult plant stripe rust resistance in wheat and identification of pyramided QTL genotypes." Euphytica: international journal on plant breeding. 176 (2), pp. 251-260. https://doi.org/10.1007/s10681-010-0240-x
Mapping spot blotch resistance genes in four barley populations
Bovill, Jessica, Lehmensiek, Anke, Sutherland, Mark W., Platz, Greg. J., Usher, Terry, Franckowiak, Jerome and Mace, Emma. 2010. "Mapping spot blotch resistance genes in four barley populations." Molecular Breeding: new strategies in plant improvement. 26 (4), pp. 653-666. https://doi.org/10.1007/s11032-010-9401-9
Chromosome composition of an F2 Triticum aestivum × T. turgidum spp. durum cross analysed by DArT markers and MCFISH
Eberhard, Friederike S., Zhang, Peng, Lehmensiek, Anke, Hare, Ray A., Simpfendorfer, Steven and Sutherland, Mark W.. 2010. "Chromosome composition of an F2 Triticum aestivum × T. turgidum spp. durum cross analysed by DArT markers and MCFISH." Crop and Pasture Science. 61 (8), pp. 619-624. https://doi.org/10.1071/CP10131
An investigation of genetic variation among Australian isolates of Bipolaris sorokiniana from different cereal tissues and comparison of their abilities to cause spot blotch on barley
Knight, N. L., Platz, G. J., Lehmensiek, A. and Sutherland, M. W.. 2010. "An investigation of genetic variation among Australian isolates of Bipolaris sorokiniana from different cereal tissues and comparison of their abilities to cause spot blotch on barley." Australasian Plant Pathology. 39 (3), pp. 207-216. https://doi.org/10.1071/AP09082
Genomic regions associated with common root rot resistance in the barley variety Delta
Lehmensiek, A., Bovill, J., Sutherland, M. W. and McNamara, R. B.. 2010. "Genomic regions associated with common root rot resistance in the barley variety Delta." Australasian Plant Pathology. 39 (3), pp. 241-246. https://doi.org/10.1071/AP09089
Population structure of South African and Australian Pyrenophora teres isolates
Lehmensiek, A., Bester-van der Merwe, A. E., Sutherland, M. W., Platz, G., Kriel, W. M., Potgieter, G. F. and Prins, R.. 2010. "Population structure of South African and Australian Pyrenophora teres isolates." Plant Pathology. 59 (3), pp. 504-515. https://doi.org/10.1111/j.1365-3059.2009.02231.x
Genetic mapping in the Triticeae
Lehmensiek, Anke, Bovill, William, Wenzl, Peter, Langridge, Peter and Appels, Rudi. 2009. "Genetic mapping in the Triticeae." Feuillet, Catherine and Muehlbauer, Gary (ed.) Genetics and genomics of the Triticeae. New York, NY. United States. Springer. pp. 201-235
QTL mapping of stripe, leaf and stem rust resistance genes in a Kariega x Avocet S doubled haploid wheat population
Prins, R., Pretorius, Z. A., Bender, C. M. and Lehmensiek, A.. 2011. "QTL mapping of stripe, leaf and stem rust resistance genes in a Kariega x Avocet S doubled haploid wheat population." Molecular Breeding: new strategies in plant improvement. 27 (2), pp. 259-270. https://doi.org/10.1007/s11032-010-9428-y
Bipolaris sorokiniana resistance loci identified on chromosomes 3HS and 7HS in three related barley
Sutherland, M. W., Lehmensiek, A., Leist, C., Platz, G. and Usher, T. R.. 2009. "Bipolaris sorokiniana resistance loci identified on chromosomes 3HS and 7HS in three related barley." Poulsen, David (ed.) ABTS 2009: Barley - The Grain for Gain. Sunshine Coast, Australia 13 - 16 Sep 2009 Indooroopilly, Australia.
Chromosome composition in an F2 hexaploid x durum cross analysed by DArT markers and MCFISH
Eberhard, F. S., Zhang, P., Lehmensiek, A., Sutherland, M. W., Hare, R. and Simpfendorfer, S.. 2008. "Chromosome composition in an F2 hexaploid x durum cross analysed by DArT markers and MCFISH." Appels, Rudi, Eastwood, Russell, Lagudah, Evans, Mackay, Michael, McIntyre, Lynne, Sharp, Peter and Langridge, Peter (ed.) 11th International Wheat Genetics Sympoium (IWGS 2008). Brisbane, Australia 24 - 29 Aug 2008 Sydney, Australia.
The application of molecular markers for partial resistance against fusarium crown rot in hexaploid and tetraploid wheats
Sutherland, Mark, Bovill, W. D., Horne, M., Lehmensiek, A., Eberhard, F., Percy, C., Wildermuth, G. B., Simpfendorfer, S. and Hare, R.. 2008. "The application of molecular markers for partial resistance against fusarium crown rot in hexaploid and tetraploid wheats." 10th International Fusarium and Fusarium Genomics Workshop 2008. Sardinia, Italy 30 Aug - 02 Sep 2008 Sardinia,Italy.
Mapping markers for priority traits in the northern grains region of Australia
Mace, E., Sutherland, Mark, Lehmensiek, Anke, Bovill, Bill, Bovill, Jessica, Collard, Bert, Daggard, Grant and Christopher, M. J.. 2006. "Mapping markers for priority traits in the northern grains region of Australia." ITMI Workshop and ACPFG Genomics Symposium (2006). Victor Harbour, Australia 27 - 31 Aug 2006
Strategies for fine mapping QTLs for crown rot resistance in wheats
Bovill, W. D., Collard, B. C. Y., Lehmensiek, Anke, Wildermuth, G. B. and Sutherland, Mark W.. 2005. "Strategies for fine mapping QTLs for crown rot resistance in wheats." Cahill, David (ed.) 15th Biennial Australasian Plant Pathology Society Conference. Geelong, Australia 26 - 29 Sep 2005 Geelong.
Molecular mapping of durable rust resistance in wheat and its implication in breeding
Bariana, H. S., Miah, H., Brown, G. N., Willey, N. and Lehmensiek, A.. 2007. "Molecular mapping of durable rust resistance in wheat and its implication in breeding." 7th International Wheat Conference (IWC 2005). Argentina 27 Nov - 02 Dec 2005 https://doi.org/10.1007/1-4020-5497-1_88
Genetic mapping of gray leaf spot (GLS) resistance genes in maize
Lehmensiek, A., Esterhuizen, A. M., Van Staden, D., Nelson, S. W. and Retief, A. E.. 2001. "Genetic mapping of gray leaf spot (GLS) resistance genes in maize ." Theoretical and Applied Genetics: international journal of plant breeding research. 103 (5), pp. 797-803. https://doi.org/10.1007/s001220100599