Abstract
To better understand the structure and evolution of the genomes of four plant pathogenic species of Zymoseptoria, we analyzed the occurrence, relative abundance (RA), and density (RD) of simple sequence repeats (SSRs) in their whole genome and transcriptome sequences. In this study, SSRs are defined as repeats of more than 12 bases in length. The genome and transcriptome sequences of Zymoseptoria ardabiliae show the highest RA (201.1 and 129.9) and RD (3229.4 and 1928.2) of SSRs, while those of Zymoseptoria pseudotritici show the lowest RA (167.2 and 118.5) and RD (2482.2 and 1687.0). The majority of SSRs in the genomic and transcriptome sequences of species were trinucleotide SSRs, while dinucleotide SSRs were the least common. The most common trinucleotide motifs in the transcriptomic sequences across all species were those that encoded the amino acid arginine. As per our motif conservation study, Zymoseptoria tritici (12.4%) possessed the most unique motifs, while Z. pseudotritici (3.9%) had the fewest. Overall, only 38.1% of the motifs were found to be conserved among the species. Gene enrichment studies reveal that three of the species, Z. ardabiliae, Zymoseptoria brevis, and Z. pseudotritici, have SSRs in their genes related to cellular metabolism, while the remaining Z. tritici harbors SSRs in genes related to DNA synthesis and gene expression. In an effort to improve the genetic resources for the orphan species of pathogenic Zymoseptoria, a total of 73,134 primers were created. The genomic resources developed in this study could help with analyses of genetic relatedness within the population and the development of species-specific markers.
Similar content being viewed by others
References
Abd-Elsalam K, Bahkali AH, Moslem M, De Wit PJGM, Verreet J-A (2011) Detection of Mycosphaerella graminicola in wheat leaves by a Microsatellite dinucleotide specific-primer. Int J Mol Sci. https://doi.org/10.3390/ijms12010682
Adhikari TB, Wallwork H, Goodwin SB (2004) Microsatellite markers linked to the Stb2 and Stb3 genes for resistance to Septoria tritici blotch in wheat. Crop Sci 44:1403–1411. https://doi.org/10.2135/cropsci2004.1403
Alotaibi NM, Saeed M, Alshammari N, Alabdallah NM, Mahfooz S (2023) Comparative genomics reveals the presence of simple sequence repeats in genes related to virulence in plant pathogenic Pythium ultimum and Pythium vexans. Arch Microbiol 205:256. https://doi.org/10.1007/s00203-023-03595-9
Chedli RBH, Aouini L, M’Barek SB, Bahri BA, Verstappen E, Kema Gerrit HJ, Rezgui S, Yahyaoui A, Chaabane H (2022) Genetic diversity and population structure of Zymoseptoria tritici on bread wheat in Tunisia using SSR markers. Eur J Plant Pathol 163:429–440. https://doi.org/10.1007/s10658-022-02486-x
da Maia LC, Palmieri DA, de Souza VQ, Kopp MM, de Carvalho FIF, Costa de Oliveira A (2008) SSR locator: tool for simple sequence repeat discovery integrated with primer design and PCR simulation. Int J Plant Gen 2008:412696. https://doi.org/10.1155/2008/412696
Eriksen L, Shaw MW, Ostergård H (2001) A model of the effect of pseudothecia on genetic recombination and epidemic development in populations of Mycosphaerella graminicola. Phytopathology 91:240–248. https://doi.org/10.1094/phyto.2001.91.3.240
Feurtey A, Lorrain C, Croll D, Eschenbrenner C, Freitag M, Habig M, Haueisen J, Möller M, Schotanus K, Stukenbrock EH (2020) Genome compartmentalization predates species divergence in the plant pathogen genus Zymoseptoria. BMC Genom 21:588. https://doi.org/10.1186/s12864-020-06871-w
Fones H, Gurr S (2015) The impact of Septoria tritici Blotch disease on wheat: an EU perspective. Fungal Genet Biol 79:3–7. https://doi.org/10.1016/j.fgb.2015.04.004
Garbe E, Vylkova S (2019) Role of amino acid metabolism in the virulence of human pathogenic fungi. Curr Clin Microbiol Rep 6:108–119. https://doi.org/10.1007/s40588-019-00124-5
Gautier A, Marcel TC, Confais J, Crane C, Kema G, Suffert F, Walker AS (2014) Development of a rapid multiplex SSR genotyping method to study populations of the fungal plant pathogen Zymoseptoria tritici. BMC Res Notes 7:373. https://doi.org/10.1186/1756-0500-7-373
Gogoi M, Datey A, Wilson KT, Chakravortty D (2016) Dual role of arginine metabolism in establishing pathogenesis. Curr Opin Microbiol 29:43–48. https://doi.org/10.1016/j.mib.2015.10.005
Goodwin SB, Ben M’Barek S, Dhillon B, Wittenberg AHJ, Crane CF, Hane JK, Foster AJ, Van der Lee TAJ, Grimwood J, Aerts A, Antoniw J, Bailey A, Bluhm B, Bowler J, Bristow J, van der Burgt A, Canto-Canché B, Churchill ACL, Conde-Ferràez L, Cools HJ, Coutinho PM, Csukai M, Dehal P, De Wit P, Donzelli B, van de Geest HC, van Ham RCHJ, Hammond-Kosack KE, Henrissat B, Kilian A, Kobayashi AK, Koopmann E, Kourmpetis Y, Kuzniar A, Lindquist E, Lombard V, Maliepaard C, Martins N, Mehrabi R, Nap JPH, Ponomarenko A, Rudd JJ, Salamov A, Schmutz J, Schouten HJ, Shapiro H, Stergiopoulos I, Torriani SFF, Tu H, de Vries RP, Waalwijk C, Ware SB, Wiebenga A, Zwiers L-H, Oliver RP, Grigoriev IV, Kema GHJ (2011) Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet 7:e1002070. https://doi.org/10.1371/journal.pgen.1002070
Kabbage M, Leslie JF, Hulbert SH, Bockus WW (2009) Comparison of natural populations of Mycosphaerella graminicola from single fields in Kansas and California. Physiol Mol Plant Pathol 74:55–59. https://doi.org/10.1016/j.pmpp.2009.09.002
Kobras CM, Fenton AK, Sheppard SK (2021) Next-generation microbiology: from comparative genomics to gene function. Genome Biol 22:123. https://doi.org/10.1186/s13059-021-02344-9
Li Y-C, Korol AB, Fahima T, Nevo E (2004) Microsatellites within genes: structure, function, and evolution. Mol Biol Evol 21:991–1007. https://doi.org/10.1093/molbev/msh073
Liu S, Wei Y, Zhang S-H (2020) The C3HC type zinc-finger protein (ZFC3) interacting with Lon/MAP1 is important for mitochondrial gene regulation, infection hypha development and longevity of Magnaporthe oryzae. BMC Microbiol 20:23. https://doi.org/10.1186/s12866-020-1711-4
Lund PA, De Biase D, Liran O, Scheler O, Mira NP, Cetecioglu Z, Fernández EN, Bover-Cid S, Hall R, Sauer M, O’Byrne C (2020) Understanding how microorganisms respond to acid ph is central to their control and successful exploitation. Front Microbiol. https://doi.org/10.3389/fmicb.2020.556140
Mahfooz S, Singh SP, Mishra N, Mishra A (2017) A comparison of microsatellites in phyto-pathogenic Aspergillus species in order to develop markers for the assessment of genetic diversity among its isolates. Front Microbiol. https://doi.org/10.3389/fmicb.2017.01774
Mahfooz S, Srivastava A, Srivastava AK, Arora DK (2015) A comparative analysis of distribution and conservation of microsatellites in the transcripts of sequenced Fusarium species and development of genic-SSR markers for polymorphism analysis. FEMS Microbiol Lett. https://doi.org/10.1093/femsle/fnv131
Mahfooz S, Srivastava A, Yadav MC, Tahoor A (2019) Comparative genomics in phytopathogenic prokaryotes reveals the higher relative abundance and density of long-SSRs in the smallest prokaryotic genome. 3 Biotech 9:340. https://doi.org/10.1007/s13205-019-1872-8
Moxon ER, Rainey PB, Nowak MA, Lenski RE (1994) Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr Biol 4:24–33. https://doi.org/10.1016/S0960-9822(00)00005-1
Orton ES, Deller S, Brown JK (2011) Mycosphaerella graminicola: from genomics to disease control. Mol Plant Pathol 12:413–424. https://doi.org/10.1111/j.1364-3703.2010.00688.x
Otzen C, Müller S, Jacobsen ID, Brock M (2013) Phylogenetic and phenotypic characterisation of the 3-ketoacyl-CoA thiolase gene family from the opportunistic human pathogenic fungus Candida albicans. FEMS Yeast Res 13:553–564. https://doi.org/10.1111/1567-1364.12057
Quaedvlieg W, Kema GH, Groenewald JZ, Verkley GJ, Seifbarghi S, Razavi M, Mirzadi Gohari A, Mehrabi R, Crous PW (2011) Zymoseptoria gen. nov.: a new genus to accommodate Septoria-like species occurring on graminicolous hosts. Persoonia 26:57–69. https://doi.org/10.3767/003158511x571841
Raudvere U, Kolberg L, Kuzmin I, Arak T, Adler P, Peterson H, Vilo J (2019) g:Profiler: a web server for functional enrichment analysis and conversions of gene lists (2019 update). Nucl Acids Res 47:W191–W198. https://doi.org/10.1093/nar/gkz369
Razavi M, Hughes GR (2004) Molecular variability of Mycosphaerella graminicola as detected by RAPD markers. J Phytopathol 152:543–548. https://doi.org/10.1111/j.1439-0434.2004.00893.x
Silao FGS, Ljungdahl PO (2021) Amino acid sensing and assimilation by the fungal pathogen Candida albicans in the human host. Pathogens. https://doi.org/10.3390/pathogens11010005
Singh P, Nath R, Venkatesh V (2021) Comparative genome-wide characterization of microsatellites in Candida albicans and Candida dubliniensis leading to the development of species-specific marker. Public Health Genom 24:1–13. https://doi.org/10.1159/000512087
Stukenbrock EH, Banke S, Javan-Nikkhah M, McDonald BA (2007) Origin and domestication of the fungal wheat pathogen Mycosphaerella graminicola via sympatric speciation. Mol Biol Evol 24:398–411. https://doi.org/10.1093/molbev/msl169
Stukenbrock EH, Quaedvlieg W, Javan-Nikhah M, Zala M, Crous PW, McDonald BA (2012) Zymoseptoria ardabiliae and Z. pseudotritici, two progenitor species of the septoria tritici leaf blotch fungus Z. tritici (synonym: Mycosphaerella graminicola). Mycologia 104:1397–1407. https://doi.org/10.3852/11-374
Takahara H, Huser A, O’Connell R (2012) Two arginine biosynthesis genes are essential for pathogenicity of Colletotrichum higginsianum on Arabidopsis. Mycology 3:54–64. https://doi.org/10.1080/21501203.2011.654353
Tan K-C, Oliver RP (2017) Regulation of proteinaceous effector expression in phytopathogenic fungi. PLoS Pathog 13:e1006241. https://doi.org/10.1371/journal.ppat.1006241
Teng JLL, Yeung ML, Chan E, Jia L, Lin CH, Huang Y, Tse H, Wong SSY, Sham PC, Lau SKP, Woo PCY (2017) PacBio but not illumina technology can achieve fast, accurate and complete closure of the high GC, complex Burkholderia pseudomallei two-chromosome genome. Front Microbiol. https://doi.org/10.3389/fmicb.2017.01448
Törönen P, Medlar A, Holm L (2018) PANNZER2: a rapid functional annotation web server. Nucl Acids Res 46:W84-w88. https://doi.org/10.1093/nar/gky350
Tørresen OK, Star B, Mier P, Andrade-Navarro MA, Bateman A, Jarnot P, Gruca A, Grynberg M, Kajava AV, Promponas VJ, Anisimova M, Jakobsen KS, Linke D (2019) Tandem repeats lead to sequence assembly errors and impose multi-level challenges for genome and protein databases. Nucl Acids Res 47:10994–11006. https://doi.org/10.1093/nar/gkz841
Varshney RK, Graner A, Sorrells ME (2005) Genic microsatellite markers in plants: features and applications. Trends Biotechnol 23:48–55. https://doi.org/10.1016/j.tibtech.2004.11.005
Voelz K, May RC (2010) Cryptococcal interactions with the host immune system. Eukaryot Cell 9:835–846. https://doi.org/10.1128/ec.00039-10
Waalwijk C, Mendes O, Verstappen ECP, de Waard MA, Kema GHJ (2002) Isolation and characterization of the mating-type idiomorphs from the wheat septoria leaf blotch fungus Mycosphaerella graminicola. Fungal Genet Biol 35:277–286. https://doi.org/10.1006/fgbi.2001.1322
Wu G, Bazer FW, Davis TA, Kim SW, Li P, Marc Rhoads J, Carey Satterfield M, Smith SB, Spencer TE, Yin Y (2009) Arginine metabolism and nutrition in growth, health and disease. Amino Acids 37:153–168. https://doi.org/10.1007/s00726-008-0210-y
Acknowledgements
This research has been funded by Scientific Research Deanship at the University of Ha’il – Saudi Arabia through project number RG-21 152.
Author information
Authors and Affiliations
Contributions
SM developed the concept and designed the analysis. MAK obtained financial support. JN, PA, PS, RMEA, ABME, AMK, NARKM, and RS conducted bioinformatics analysis. MAK and SM wrote and revised the paper.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Kausar, M.A., Narayan, J., Agarwal, P. et al. Distribution and conservation of simple sequence repeats in plant pathogenic species of Zymoseptoria and development of genomic resources for its orphaned species. Antonie van Leeuwenhoek 117, 11 (2024). https://doi.org/10.1007/s10482-023-01915-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10482-023-01915-z