Comparative genomic analysis of 5Mg chromosome of Aegilops geniculata and 5Uu chromosome of Aegilops umbellulata reveal genic diversity in the tertiary gene pool

. 2023 ; 14 () : 1144000. [epub] 20230713

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37521926

Wheat is one of the most important cereal crops for the global food security. Due to its narrow genetic base, modern bread wheat cultivars face challenges from increasing abiotic and biotic stresses. Since genetic improvement is the most sustainable approach, finding novel genes and alleles is critical for enhancing the genetic diversity of wheat. The tertiary gene pool of wheat is considered a gold mine for genetic diversity as novel genes and alleles can be identified and transferred to wheat cultivars. Aegilops geniculata and Ae. umbellulata are the key members of the tertiary gene pool of wheat and harbor important genes against abiotic and biotic stresses. Homoeologous-group five chromosomes (5Uu and 5Mg) have been extensively studied from Ae. geniculata and Ae. umbellulata as they harbor several important genes including Lr57, Lr76, Yr40, Yr70, Sr53 and chromosomal pairing loci. In the present study, using chromosome DNA sequencing and RNAseq datasets, we performed comparative analysis to study homoeologous gene evolution in 5Mg, 5Uu, and group 5 wheat chromosomes. Our findings highlight the diversity of transcription factors and resistance genes, resulting from the differential expansion of the gene families. Both the chromosomes were found to be enriched with the "response to stimulus" category of genes providing resistance against biotic and abiotic stress. Phylogenetic study positioned the M genome closer to the D genome, with higher proximity to the A genome than the B genome. Over 4000 genes were impacted by SNPs on 5D, with 4-5% of those genes displaying non-disruptive variations that affect gene function.

Zobrazit více v PubMed

Akhunov E., Nicolet C., Dvorak J. (2009). Single nucleotide polymorphism genotyping in polyploid wheat with the illumina GoldenGate assay. Theor. Appl. Genet. 119, 507–517. doi: 10.1007/s00122-009-1059-5 PubMed DOI PMC

Alonge M., Soyk S., Ramakrishnan S., Wang X., Goodwin S., Sedlazeck F. J., et al. . (2019). RaGOO: fast and accurate reference-guided scaffolding of draft genomes. Genome Biol. 20, 224. doi: 10.1186/s13059-019-1829-6 PubMed DOI PMC

Andrews S. (2010) FastQC: a quality control tool for high throughput sequence data. Available at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc.

Arrigo N., Felber F., Parisod C., Buerki S., Alvarez N., David J., et al. . (2010). Origin and expansion of the allotetraploid aegilops geniculata, a wild relative of wheat. New Phytol. 187, 1170–1180. doi: 10.1111/j.1469-8137.2010.03328.x PubMed DOI

Arrigo N., Guadagnuolo R., Lappe S., Pasche S., Parisod C., Felber F. (2011). Gene flow between wheat and wild relatives: empirical evidence from aegilops geniculata, ae. neglecta and ae. triuncialis. Evol. Appl. 4, 685–695. doi: 10.1111/j.1752-4571.2011.00191.x PubMed DOI PMC

Bálint A. F., Kovács G., Erdei L., Sutka J. (2001). Comparison of the Cu, zn, fe, Ca and mg contents of the grains of wild, ancient and cultivated wheat species. Cereal Res. Commun. 29, 375–382. doi: 10.1007/BF03543684 DOI

Bansal M., Adamski N. M., Toor P. I., Kaur S., Molnár I., Holušová K., et al. . (2020). Aegilops umbellulata introgression carrying leaf rust and stripe rust resistance genes Lr76 and Yr70 located to 9.47-Mb region on 5DS telomeric end through a combination of chromosome sorting and sequencing. Theor. Appl. Genet. 133, 903–915. doi: 10.1007/s00122-019-03514-x PubMed DOI

Bansal M., Kaur S., Dhaliwal H. S., Bains N. S., Bariana H. S., Chhuneja P., et al. . (2017). Mapping of aegilops umbellulata-derived leaf rust and stripe rust resistance loci in wheat. Plant Pathol. 66, 38–44. doi: 10.1111/ppa.12549 DOI

Bao W., Kojima K. K., Kohany O. (2015). Repbase update, a database of repetitive elements in eukaryotic genomes. Mob DNA 6, 4–9. doi: 10.1186/s13100-015-0041-9 PubMed DOI PMC

Bolger A. M., Lohse M., Usadel B. (2014). Genome analysis Trimmomatic : a flexible trimmer for illumina sequence data. Bioinformatics 30, 2114–2120. doi: 10.1093/bioinformatics/btu170 PubMed DOI PMC

Buchfink B., Reuter K., Drost H. G. (2021). Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat. Methods 18, 366–368. doi: 10.1038/s41592-021-01101-x PubMed DOI PMC

Bushnell B. (2014). BBMap: A Fast, Accurate, Splice-Aware Aligner. in 9th Annual Genomics of Energy & Environment Meeting, Walnut Creek, CA, March 17-20, 2014, ed. B. C. No. LBNL-7065E . Ernest Orlando Lawrence Berkeley National Laboratory.

Camacho C., Coulouris G., Avagyan V., Ma N., Papadopoulos J., Bealer K., et al. . (2009). BLAST plus: architecture and applications. BMC Bioinf. 10, 1. doi: 10.1186/1471-2105-10-421 PubMed DOI PMC

Chaudhary H. K., Kaila V., Rather S. A., Badiyal A., Hussain W., Jamwal N. S., et al. . (2014). Wheat. In: Pratap A., Kumar J. (eds) Alien Gene Transfer in Crop Plants, Volume 2. (New York, NY: Springer; ). doi: 10.1007/978-1-4614-9572-7_1 DOI

Cingolani P., Platts A., Wang L. L., Coon M., Nguyen T., Wang L., et al. . (2012). A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin) 6, 80–92. doi: 10.4161/fly.19695 PubMed DOI PMC

Conesa A., Götz S. (2008). Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int. J. Plant Genomics 2008, 619832. doi: 10.1155/2008/619832 PubMed DOI PMC

Conway J. R., Lex A., Gehlenborg N. (2017). UpSetR: an r package for the visualization of intersecting sets and their properties. Bioinformatics 33, 2938–2940. doi: 10.1093/bioinformatics/btx364 PubMed DOI PMC

Criscuolo A. (2019). A fast alignment-free bioinformatics procedure to infer accurate distance-based phylogenetic trees from genome assemblies. Res. Ideas Outcomes 5, e36178. doi: 10.3897/rio.5.e36178 DOI

Danecek P., Bonfield J. K., Liddle J., Marshall J., Ohan V., Pollard M. O., et al. . (2021). Twelve years of SAMtools and BCFtools. Gigascience 10, giab008. doi: 10.1093/gigascience/giab008 PubMed DOI PMC

De Bie T., Cristianini N., Demuth J. P., Hahn M. W. (2006). CAFE: a computational tool for the study of gene family evolution. Bioinformatics 22, 1269–1271. doi: 10.1093/bioinformatics/btl097 PubMed DOI

Doležel J., Vrána J., Šafář J., Bartoš J., Kubaláková M., Šimková H. (2012). Chromosomes in the flow to simplify genome analysis. Funct. Integr. Genomics 12, 397–416. doi: 10.1007/s10142-012-0293-0 PubMed DOI PMC

Du X., Jia Z., Yu Y., Wang S., Che B., Ni F., et al. . (2019). A wheat-aegilops umbellulata addition line improves wheat agronomic traits and processing quality. Breed Sci. 69, 503–507. doi: 10.1270/jsbbs.18200 PubMed DOI PMC

Emms D. M., Kelly S. (2019). OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 1–14. doi: 10.1186/s13059-019-1832-y PubMed DOI PMC

Enghiad A., Ufer D., Countryman A. M., Thilmany D. D. (2017). An overview of global wheat market fundamentals in an era of climate concerns. Int. J. Agron. 2017, 1–15. doi: 10.1155/2017/3931897 DOI

Enright A. J., Van Dongen S., Ouzounis C. A. (2002). An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res. 30, 1575–1584. doi: 10.1093/nar/30.7.1575 PubMed DOI PMC

Farré M., Kim J., Proskuryakova A. A., Zhang Y., Kulemzina A. I., Li Q., et al. . (2019). Evolution of gene regulation in ruminants differs between evolutionary breakpoint regions and homologous synteny blocks. Genome Res. 29, 576–589. doi: 10.1101/gr.239863.118 PubMed DOI PMC

Fernandez-Calvin B., Orellana J. (1992). Relationship between pairing frequencies and genome affinity estimations in Aegiops ovata x Triticum aestivum hybrid plants. Heredity 68, 165–172. doi: 10.1038/hdy.1992.25 PubMed DOI

Feuillet C., Langridge P., Waugh R. (2008). Cereal breeding takes a walk on the wild side. Trends Genet. 24, 24–32. doi: 10.1016/j.tig.2007.11.001 PubMed DOI

Flynn J. M., Hubley R., Goubert C., Rosen J., Clark A. G., Feschotte C., et al. . (2020). RepeatModeler2 for automated genomic discovery of transposable element families. Proc. Natl. Acad. Sci. 117, 9451–9457. doi: 10.1073/pnas.1921046117 PubMed DOI PMC

Garg M., Tsujimoto H., Gupta R. K., Kumar A., Kaur N., Kumar R., et al. . (2016). Chromosome specific substitution lines of aegilops geniculata alter parameters of bread making quality of wheat. PloS One 11, e0162350. doi: 10.1371/journal.pone.0162350 PubMed DOI PMC

Han G., Lu C., Guo J., Qiao Z., Sui N., Qiu N., et al. . (2020). C2H2 zinc finger proteins: master regulators of abiotic stress responses in plants. Front. Plant Sci. 11. doi: 10.3389/fpls.2020.00115 PubMed DOI PMC

He F., Pasam R., Shi F., Kant S., Keeble-gagnere G., Kay P., et al. . (2019). Exome sequencing highlights the role of wild-relative introgression in shaping the adaptive landscape of the wheat genome. Nat. Genet. 51, 896–904. doi: 10.1038/s41588-019-0382-2 PubMed DOI

Hoff K. J., Stanke M. (2019). Predicting genes in single genomes with AUGUSTUS. Curr. Protoc. Bioinf. 65, e57. doi: 10.1002/cpbi.57 PubMed DOI

Huynen M. A., Bork P. (1998). Measuring genome evolution. Proc. Natl. Acad. Sci. USA 95, 5849–5856. doi: 10.1073/pnas.95.11.584 PubMed DOI PMC

Jin J., Tian F., Yang D. C., Meng Y. Q., Kong L., Luo J., et al. . (2017). PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res. 45, D1040–D1045. doi: 10.1093/nar/gkw982 PubMed DOI PMC

Katiyar A., Smita S., Lenka S. K., Rajwanshi R., Chinnusamy V., Bansal K. C. (2012). Genome-wide classification and expression analysis of MYB transcription factor families in rice and arabidopsis. BMC Genomics 13, 544. doi: 10.1186/1471-2164-13-544 PubMed DOI PMC

Kim D., Paggi J. M., Park C., Bennett C., Salzberg S. L. (2019). Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat. Biotechnol. 37, 907–915. doi: 10.1038/s41587-019-0201-4 PubMed DOI PMC

Koressaar T., Remm M. (2007). Enhancements and modifications of primer design program Primer3. Bioinformatics 23, 1289–1291. doi: 10.1093/bioinformatics/btm091 PubMed DOI

Kuraparthy V., Chhuneja P., Dhaliwal H. S., Kaur S., Bowden R. L., Gill B. S. (2007). Characterization and mapping of cryptic alien introgression from aegilops geniculata with new leaf rust and stripe rust resistance genes Lr57 and Yr40 in wheat. Theor. Appl. Genet. 114, 1379–1389. doi: 10.1007/s00122-007-0524-2 PubMed DOI

Li H., Durbin R. (2010). Fast and accurate long-read alignment with burrows-wheeler transform. Bioinformatics 26, 589–595. doi: 10.1093/bioinformatics/btp698 PubMed DOI PMC

Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., et al. . (2009). The sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079. doi: 10.1093/bioinformatics/btp352 PubMed DOI PMC

Li L.-F., Liu B., Olsen K. M., Wendel J. F. (2015). A re-evaluation of the homoploid hybrid origin of aegilops tauschii, the donor of the wheat d-subgenome. New Phytol. 208, 4–8. doi: 10.1111/nph.13294 PubMed DOI

Liao Y., Smyth G. K., Shi W. (2014). FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930. doi: 10.1093/bioinformatics/btt656 PubMed DOI

Liu W., Rouse M., Friebe B., Jin Y., Gill B., Pumphrey M. O. (2011). Discovery and molecular mapping of a new gene conferring resistance to stem rust, Sr53, derived from aegilops geniculata and characterization of spontaneous translocation stocks with reduced alien chromatin. Chromosome Res. 19, 669–682. doi: 10.1007/s10577-011-9226-3 PubMed DOI

Loureiro I., Escorial M. C., García-Baudín J. M., Chueca M. C. (2006). Evidence of natural hybridization between aegilops geniculata and wheat under field conditions in central Spain. Environ. Biosafety Res. 5, 105–109. doi: 10.1051/ebr:2006020 PubMed DOI

Luo M.-C., Gu Y. Q., Puiu D., Wang H., Twardziok S. O., Deal K. R., et al. . (2017). Genome sequence of the progenitor of the wheat d genome aegilops tauschii. Nature 551, 498–502. doi: 10.1038/nature24486 PubMed DOI PMC

Luo R., Liu B., Xie Y., Li Z., Huang W., Yuan J., et al. . (2012). SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1, 18. doi: 10.1186/2047-217X-1-18 PubMed DOI PMC

Marcussen T., Sandve S. R., Heier L., Pfeifer M., Kugler K. G., Zhan B., et al. . (2014). A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345, 1250092. doi: 10.1126/science.1251788 PubMed DOI

McCarthy D. J., Chen Y., Smyth G. K. (2012). Differential expression analysis of multifactor RNA-seq experiments with respect to biological variation. Nucleic Acids Res. 40, 4288–4297. doi: 10.1093/nar/gks042 PubMed DOI PMC

Meimberg H., Rice K. J., Milan N. F., Njoku C. C., McKay J. K. (2009). Multiple origins promote the ecological amplitude of allopolyploid Aegilops (Poaceae). Am. J. Bot. 96, 1262–1273. doi: 10.3732/ajb.0800345 PubMed DOI

Mena M., Orellana J., Lopez-Brafia I., Gareia-Olmedo E., Delibes A. (1993). Characterization of wheat/Aegilops ventricosa introgression and addition lines with respect to the Mv genome. Theor. Appl. Genet. 86, 197–204. PubMed

Middleton C. P., Senerchia N., Stein N., Akhunov E. D., Keller B., Wicker T., et al. . (2014). Sequencing of chloroplast genomes from wheat, barley, rye and their relatives provides a detailed insight into the evolution of the triticeae tribe. PloS One 9, e85761. doi: 10.1371/journal.pone.0085761 PubMed DOI PMC

Mistry J., Bateman A., Finn R. D. (2007). Predicting active site residue annotations in the pfam database. BMC Bioinf. 8, 298. doi: 10.1186/1471-2105-8-298 PubMed DOI PMC

Molnár I., Kubaláková M., Šimková H., Cseh A., Molnár-Láng M., Doležel J. (2011). Chromosome isolation by flow sorting in aegilops umbellulata and ae. comosa and their allotetraploid hybrids ae. biuncialis and ae. geniculata. PloS One 6, e27708. doi: 10.1371/journal.pone.0027708 PubMed DOI PMC

Molnár I., Kubaláková M., Šimková H., Farkas A., Cseh A., Megyeri M., et al. . (2014). Flow cytometric chromosome sorting from diploid progenitors of bread wheat, t. urartu, ae. speltoides and ae. tauschii. Theor. Appl. Genet. 127, 1091–1104. doi: 10.1007/s00122-014-2282-2 PubMed DOI

Nakano T., Suzuki K., Fujimura T., Shinshi H. (2006). Genome-wide analysis of the ERF gene family in arabidopsis and rice. Plant Physiol. 140, 411–432. doi: 10.1104/pp.105.073783 PubMed DOI PMC

Natsidis P., Kapli P., Schiffer P. H., Telford M. J. (2021). Systematic errors in orthology inference and their effects on evolutionary analyses. iScience 24, 102110. doi: 10.1016/j.isci.2021.102110 PubMed DOI PMC

Okada M., Ikeda T. M., Yoshida K., Takumi S. (2018. a). Effect of the U genome on grain hardness in nascent synthetic hexaploids derived from interspecific hybrids between durum wheat and aegilops umbellulata. J. Cereal Sci. 83, 153–161. doi: 10.1016/j.jcs.2018.08.011 DOI

Okada M., Michikawa A., Yoshida K., Nagaki K., Ikeda T. M., Takumi S. (2020). Phenotypic effects of the U-genome variation in nascent synthetic hexaploids derived from interspecific crosses between durum wheat and its diploid relative aegilops umbellulata. PloS One 15, e0231129. doi: 10.1371/journal.pone.0231129 PubMed DOI PMC

Okada M., Yoshida K., Nishijima R., Michikawa A., Motoi Y., Sato K., et al. . (2018. b). RNA-Seq analysis reveals considerable genetic diversity and provides genetic markers saturating all chromosomes in the diploid wild wheat relative aegilops umbellulata. BMC Plant Biol. 18, 271. doi: 10.1186/s12870-018-1498-8 PubMed DOI PMC

Rakszegi M., Molnár I., Lovegrove A., Darkó É., Farkas A., Láng L., et al. . (2017). Addition of aegilops U and m chromosomes affects protein and dietary fiber content of wholemeal wheat flour. Front. Plant Sci. 8. doi: 10.3389/fpls.2017.01529 PubMed DOI PMC

Ramírez-González R. H., Borrill P., Lang D., Harrington S. A., Brinton J., Venturini L., et al. . (2018). The transcriptional landscape of polyploid wheat. Science 361, eaar6089. doi: 10.1126/science.aar6089 PubMed DOI

Ramirez-Gonzalez R. H., Uauy C., Caccamo M. (2015). PolyMarker: a fast polyploid primer design pipeline. Bioinformatics 31, 2038–2039. doi: 10.1093/bioinformatics/btv069 PubMed DOI PMC

Said M., Holušová K., Farkas A., Ivanizs L., Gaál E., Cápal P., et al. . (2021). Development of DNA markers from physically mapped loci in aegilops comosa and aegilops umbellulata using single-gene FISH and chromosome sequences. Front. Plant Sci. 12. doi: 10.3389/fpls.2021.689031 PubMed DOI PMC

Schwacke R., Ponce-Soto G. Y., Krause K., Bolger A. M., Arsova B., Hallab A., et al. . (2019). MapMan4: a refined protein classification and annotation framework applicable to multi-omics data analysis. Mol. Plant 12, 879–892. doi: 10.1016/j.molp.2019.01.003 PubMed DOI

Sears E. R. (1956) The transfer of leaf-rust resistance from aegilops umbellulata to wheat. Available at: https://www.cabdirect.org/cabdirect/abstract/19581600184.

Sela N., Kim E., Ast G. (2010). The role of transposable elements in the evolution of non-mammalian vertebrates and invertebrates. Genome Biol. 11, R59. doi: 10.1186/gb-2010-11-6-r59 PubMed DOI PMC

Sharma A., Srivastava P., Mavi G. S., Kaur S., Kaur J., Bala R., et al. . (2021). Resurrection of wheat cultivar PBW343 using marker-assisted gene pyramiding for rust resistance. Front. Plant Sci. 12. doi: 10.3389/fpls.2021.570408 PubMed DOI PMC

Simão F. A., Waterhouse R. M., Ioannidis P., Kriventseva E. V., Zdobnov E. M. (2015). BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212. doi: 10.1093/bioinformatics/btv351 PubMed DOI

Slater G. S. C., Birney E. (2005). Automated generation of heuristics for biological sequence comparison. BMC Bioinf. 6, 31. doi: 10.1186/1471-2105-6-31 PubMed DOI PMC

Steadham J., Schulden T., Kalia B., Koo D. H., Gill B. S., Bowden R., et al. . (2021). An approach for high-resolution genetic mapping of distant wild relatives of bread wheat: example of fine mapping of Lr57 and Yr40 genes. Theor. Appl. Genet. 134, 2671–2686. doi: 10.1007/s00122-021-03851-w PubMed DOI

Stoilova T., Spetsov P. (2006). Chromosome 6U from aegilops geniculata Roth carrying powdery mildew resistance in bread wheat. Breed Sci. 56, 351–357. doi: 10.1270/jsbbs.56.351 DOI

Sun X., Wang Y., Sui N. (2018). Transcriptional regulation of bHLH during plant response to stress. Biochem. Biophys. Res. Commun. 503, 397–401. doi: 10.1016/j.bbrc.2018.07.123 PubMed DOI

Tang H., Lyons E., Pedersen B., Schnable J. C., Paterson A. H., Freeling M. (2011). Screening synteny blocks in pairwise genome comparisons through integer programming. BMC Bioinf. 12, 102. doi: 10.1186/1471-2105-12-102 PubMed DOI PMC

Tarailo-Graovac M., Chen N. (2009). Using RepeatMasker to identify repetitive elements in genomic sequences. Curr. Protoc. Bioinf. 4.10.1-4.10.14. doi: 10.1002/0471250953.bi0410s25 PubMed DOI

Theißen G., Melzer R., Ruümpler F. (2016). MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution. Dev. (Cambridge) 143, 3259–3271. doi: 10.1242/dev.134080 PubMed DOI

The International Wheat Genome Sequencing Consortium (IWGSC) et al. . (2018). Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361, 661. doi: 10.1126/science.aar7191 PubMed DOI

The SRA Toolkit Development Team . Available at: https://trace.ncbi.nlm.nih.gov/Traces/sra/sra.cgi?view=software.

Thiel T., Michalek W., Varshney R. K., Graner A. (2003). Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare l.). Theor. Appl. Genet. 106, 411–422. doi: 10.1007/s00122-002-1031-0 PubMed DOI

Tiwari V. K., Wang S., Danilova T., Koo D. H., Vrána J., Kubaláková M., et al. . (2015). Exploring the tertiary gene pool of bread wheat: sequence assembly and analysis of chromosome 5Mg of aegilops geniculata. Plant J. 84, 733–746. doi: 10.1111/tpj.13036 PubMed DOI

Tiwari V. K., Wang S., Sehgal S., Vrána J., Friebe B., Kubaláková M., et al. . (2014). SNP discovery for mapping alien introgressions in wheat. BMC Genomics 15, 273. doi: 10.1186/1471-2164-15-273 PubMed DOI PMC

van Poecke R. M. P., Maccaferri M., Tang J., Truong H. T., Janssen A., van Orsouw N. J., et al. . (2013). Sequence-based SNP genotyping in durum wheat. Plant Biotechnol. J. 11, 809–817. doi: 10.1111/pbi.12072 PubMed DOI

Walkowiak S., Gao L., Monat C., Haberer G., Delorean E., Thambugala D., et al. . (2020). Multiple wheat genomes reveal global variation in modern breeding. Nature 588, 277–283. doi: 10.1038/s41586-020-2961-x PubMed DOI PMC

Wang Y., Zhang Y., Zhou R., Dossa K., Yu J., Li D., et al. . (2018). Identification and characterization of the bZIP transcription factor family and its expression in response to abiotic stresses in sesame. PloS One 13, e0200850. doi: 10.1371/journal.pone.0200850 PubMed DOI PMC

Wickham H. (2016). ggplot2: elegant graphics for data analysis (Verlag New York: Springer; ). Available at: https://ggplot2.tidyverse.org.

Winfield M. O., Allen A. M., Burridge A. J., Barker G. L. A., Benbow H. R., Wilkinson P. A., et al. . (2016). High-density SNP genotyping array for hexaploid wheat and its secondary and tertiary gene pool. Plant Biotechnol. J. 14, 1195–1206. doi: 10.1111/pbi.12485 PubMed DOI PMC

Yadav I. S., Sharma A., Kaur S., Nahar N., Bhardwaj S. C., Sharma T. R., et al. . (2016). Comparative temporal transcriptome profiling of wheat near isogenic line carrying Lr57 under compatible and incompatible interactions. Front. Plant Sci. 7. doi: 10.3389/fpls.2016.01943 PubMed DOI PMC

Yang X., Xu M., Wang Y., Cheng X., Huang C., Zhang H., et al. . (2022). Development and molecular cytogenetic identification of two wheat-aegilops geniculata Roth 7Mg chromosome substitution lines with resistance to fusarium head blight, powdery mildew and stripe rust. Int. J. Mol. Sci. 23, 7056. doi: 10.3390/ijms23137056 PubMed DOI PMC

Ye J., Zhang Y., Cui H., Liu J., Wu Y., Cheng Y., et al. . (2018). WEGO 2.0: a web tool for analyzing and plotting GO annotations 2018 update. Nucleic Acids Res. 46, W71–W75. doi: 10.1093/nar/gky400 PubMed DOI PMC

Young M. D., Wakefield M. J., Smyth G. K., Oshlack A. (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Available at: http://genomebiology.com/2010/11/2/R14. PubMed PMC

Zeller F. J., Kong L., Hartl L., Mohler V., Hsam S. L. K. (2002). Chromosomal location of genes for resistance to powdery mildew in common wheat (Triticum aestivum l. em thell.) 7. gene Pm29 in line pova. Euphytica 123, 187–194. doi: 10.1023/A:1014944619304 DOI

Zhang X.-Y., Wang R.-C., Dong Y.-S. (1996). RAPD polymorphisms in aegilops geniculata Roth (Ae. ovata auct. non l.). Genet. Resour. Crop Evol. 43, 429. doi: 10.1007/BF00123733 DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...