Wild emmer wheat, the progenitor of modern bread wheat, exhibits great diversity in the VERNALIZATION1 gene
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic-ecollection
Document type Journal Article
PubMed
36684759
PubMed Central
PMC9853909
DOI
10.3389/fpls.2022.1106164
Knihovny.cz E-resources
- Keywords
- GWAS, VERNALIZATION1, heading time, next generation sequencing, wild emmer wheat,
- Publication type
- Journal Article MeSH
Wild emmer wheat is an excellent reservoir of genetic variability that can be utilized to improve cultivated wheat to address the challenges of the expanding world population and climate change. Bearing this in mind, we have collected a panel of 263 wild emmer wheat (WEW) genotypes across the Fertile Crescent. The genotypes were grown in different locations and phenotyped for heading date. Genome-wide association mapping (GWAS) was carried out, and 16 SNPs were associated with the heading date. As the flowering time is controlled by photoperiod and vernalization, we sequenced the VRN1 gene, the most important of the vernalization response genes, to discover new alleles. Unlike most earlier attempts, which characterized known VRN1 alleles according to a partial promoter or intron sequences, we obtained full-length sequences of VRN-A1 and VRN-B1 genes in a panel of 95 wild emmer wheat from the Fertile Crescent and uncovered a significant sequence variation. Phylogenetic analysis of VRN-A1 and VRN-B1 haplotypes revealed their evolutionary relationships and geographic distribution in the Fertile Crescent region. The newly described alleles represent an attractive resource for durum and bread wheat improvement programs.
Department of Field Crops Faculty of Agriculture University of Çukurova Adana Turkey
Department of Geoinformatics Faculty of Science Palacký University Olomouc Olomouc Czechia
See more in PubMed
Abdul Kayum M., Nath U., Park J.-I., Biswas M., Choi E., Song J.-Y., et al. (2018). Genome-wide identification, characterization, and expression profiling of glutathione s-transferase (GST) family in pumpkin reveals likely role in cold-stress tolerance. Genes (Basel). 9, 84. doi: 10.3390/genes9020084 PubMed DOI PMC
Alonso-Peral M. M., Oliver S. N., Casao M. C., Greenup A. A., Trevaskis B. (2011). The promoter of the cereal PubMed DOI PMC
Badaeva E. D., Konovalov F. A., Knüpffer H., Fricano A., Ruban A. S., Kehel Z., et al. (2022). Genetic diversity, distribution and domestication history of the neglected GGAtAt genepool of wheat. Theor. Appl. Genet. 135, 755–776. doi: 10.1007/s00122-021-03912-0 PubMed DOI PMC
Balfourier F., Bouchet S., Robert S., DeOliveira R., Rimbert H., Kitt J., et al. (2019). Worldwide phylogeography and history of wheat genetic diversity. Sci. Adv. 5, eaav0536. doi: 10.1126/sciadv.aav0536 PubMed DOI PMC
Balla M. Y., Gorafi Y. S. A., Kamal N. M., Abdalla M. G. A., Tahir I. S. A., Tsujimoto H. (2022. a). Exploiting wild emmer wheat diversity to improve wheat a and b genomes in breeding for heat stress adaptation. Front. Plant Sci. 13. doi: 10.3389/fpls.2022.895742 PubMed DOI PMC
Balla M. Y., Gorafi Y. S. A., Kamal N. M., Abdalla M. G. A., Tahir I. S. A., Tsujimoto H. (2022. b). Harnessing the diversity of wild emmer wheat for genetic improvement of durum wheat. Theor. Appl. Genet. 135, 1671–1684. doi: 10.1007/s00122-022-04062-7 PubMed DOI PMC
Bankevich A., Nurk S., Antipov D., Gurevich A. A., Dvorkin M., Kulikov A. S., et al. (2012). SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477. doi: 10.1089/cmb.2012.0021 PubMed DOI PMC
Beales J., Turner A., Griffiths S., Snape J. W., Laurie D. A. (2007). A pseudo-response regulator is misexpressed in the photoperiod insensitive PubMed DOI
Becker A., Theißen G. (2003). The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol. Phylogenet. Evol. 29, 464–489. doi: 10.1016/S1055-7903(03)00207-0 PubMed DOI
Bolger A. M., Lohse M., Usadel B. (2014). Trimmomatic: A flexible trimmer for illumina sequence data. Bioinformatics 30, 2114–2120. doi: 10.1093/bioinformatics/btu170 PubMed DOI PMC
Cagirici H. B., Sen T. Z. (2020). Genome-wide discovery of G-quadruplexes in wheat: Distribution and putative functional roles. G3 Genes Genomes Genet. 10, 2021–2032. doi: 10.1534/g3.120.401288 PubMed DOI PMC
Carles C. C., Choffnes-Inada D., Reville K., Lertpiriyapong K., Fletcher J. C. (2005). PubMed DOI
Carles C. C., Fletcher J. C. (2009). The SAND domain protein ULTRAPETALA1 acts as a trithorax group factor to regulate cell fate in plants. Genes Dev. 23, 2723–2728. doi: 10.1101/gad.1812609 PubMed DOI PMC
Chee P. W., Elias E. M., Anderson J. A., Kianian S. F. (2001). Evaluation of a high grain protein QTL from DOI
Chen L., Bernhardt A., Lee J., Hellmann H. (2015). Identification of PubMed DOI
Chen A., Dubcovsky J. (2012). Wheat TILLING mutants show that the vernalization gene PubMed DOI PMC
Chen L., Lee J. H., Weber H., Tohge T., Witt S., Roje S., et al. (2013). PubMed DOI PMC
Chhuneja P., Arora J. K., Kaur P., Kaur S., Singh K. (2015). Characterization of wild emmer wheat DOI
Civáň P., Ivaničová Z., Brown T. A. (2013). Reticulated origin of domesticated emmer wheat supports a dynamic model for the emergence of agriculture in the fertile crescent. PloS One 8, e81955. doi: 10.1371/journal.pone.0081955 PubMed DOI PMC
Debernardi J. M., Woods D. P., Li K., Li C., Dubcovsky J. (2022). PubMed DOI PMC
Díaz A., Zikhali M., Turner A. S., Isaac P., Laurie D. A. (2012). Copy number variation affecting the PubMed DOI PMC
Dubcovsky J., Dvorak J. (2007). Genome plasticity a key factor in the success of polyploid wheat under domestication. Science 316, 1862–1866. doi: 10.1126/science.1143986 PubMed DOI PMC
Egea-Cortines M., Saedler H., Sommer H. (1999). Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in PubMed DOI PMC
Fadida-Myers A., Fuerst D., Tzuberi A., Yadav S., Nashef K., Roychowdhury R., et al. (2022). Emmer wheat eco-geographic and genomic congruence shapes phenotypic performance under Mediterranean climate. Plants 11, 1460. doi: 10.3390/plants11111460 PubMed DOI PMC
Feng Y., Tao S., Zhang P., Sperti F. R., Liu G., Cheng X., et al. (2022). Epigenomic features of DNA G-quadruplexes and their roles in regulating rice gene transcription. Plant Physiol. 188, 1632–1648. doi: 10.1093/plphys/kiab566 PubMed DOI PMC
Foreign Agricultural Service/USDA (2022). World agricultural production. Circ. Ser., 1–43. doi: 10.32317/2221-1055.201907059 DOI
Frischmeyer P. A., Dietz H. C. (1999). Nonsense-mediated mRNA decay in health and disease. Hum. Mol. Genet. 8, 1893–1900. doi: 10.1093/hmg/8.10.1893 PubMed DOI
Fu D., Szucs P., Yan L., Helguera M., Skinner J. S., Von Zitzewitz J., et al. (2005). Large Deletions within the first intron in PubMed DOI
Gao Y., An K., Guo W., Chen Y., Zhang R., Zhang X., et al. (2021). The endosperm-specific transcription factor TaNAC019 regulates glutenin and starch accumulation and its elite allele improves wheat grain quality. Plant Cell 33, 603–622. doi: 10.1093/plcell/koaa040 PubMed DOI PMC
Garg R., Aggarwal J., Thakkar B. (2016). Genome-wide discovery of G-quadruplex forming sequences and their functional relevance in plants. Sci. Rep. 6, 31–35. doi: 10.1038/srep28211 PubMed DOI PMC
Golovnina K. A., Kondratenko E. Y., Blinov A. G., Goncharov N. P. (2010). Molecular characterization of vernalization loci PubMed DOI PMC
Hao Y., Xu S., Lyu Z., Wang H., Kong L., Sun S. (2021). Comparative analysis of the glutathione s-transferase gene family of four PubMed DOI PMC
Harlan J. R., Wet J. M. J. (1971). Toward a rational classification of cultivated plants. Taxon 20, 509–517. doi: 10.2307/1218252 DOI
Hentze M. W., Kulozik A. E. (1999). A perfect message: RNA surveillance and nonsense-mediated decay. Cell 96, 307–310. doi: 10.1016/S0092-8674(00)80542-5 PubMed DOI
Hori K., Ogiso-Tanaka E., Matsubara K., Yamanouchi U., Ebana K., Yano M. (2013). PubMed DOI PMC
Huang M., Liu X., Zhou Y., Summers R. M., Zhang Z. (2019). BLINK: a package for the next level of genome-wide association studies with both individuals and markers in the millions. Gigascience 8, 1–12. doi: 10.1093/gigascience/giy154 PubMed DOI PMC
Huppert J. L., Balasubramanian S. (2007). G-Quadruplexes in promoters throughout the human genome. Nucleic Acids Res. 35, 406–413. doi: 10.1093/nar/gkl1057 PubMed DOI PMC
Islam S., Sajib S., Jui Z. S., Arabia S., Islam T., Ghosh A. (2019). Genome-wide identification of glutathione s-transferase gene family in pepper, its classification, and expression profiling under different anatomical and environmental conditions. Sci. Rep. 9, 9101. doi: 10.1038/s41598-019-45320-x PubMed DOI PMC
Itoh T., Kamiya A., Kimura M., Murai K. (2021). Heterogeneous expression and purification of the wheat VRN1 K-box domain suggest the formation of a tetramer of the VRN1 protein. Am. J. Plant Sci. 12, 1002–1010. doi: 10.4236/ajps.2021.127068 DOI
Ivaničová Z., Jakobson I., Reis D., Šafář J., Milec Z., Abrouk M., et al. (2016). Characterization of new allele influencing flowering time in bread wheat introgressed from PubMed DOI
Ivaničová Z., Valárik M., Pánková K., Trávníčková M., Doležel J., Šafář J., et al. (2017). Heritable heading time variation in wheat lines with the same number of PubMed DOI PMC
Jin F. F., Wei L. (2016). The expression patterns of three DOI
Katoh K., Misawa K., Kuma K., Miyata T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066. doi: 10.1093/nar/gkf436 PubMed DOI PMC
Katoh K., Standley D. M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 30, 772–780. doi: 10.1093/molbev/mst010 PubMed DOI PMC
Keidar D., Doron C., Kashkush K. (2018). Genome-wide analysis of a recently active retrotransposon, au SINE, in wheat: content, distribution within subgenomes and chromosomes, and gene associations. Plant Cell Rep. 37, 193–208. doi: 10.1007/s00299-017-2213-1 PubMed DOI PMC
Kippes N., Guedira M., Lin L., Alvarez M. A., Brown-Guedira G. L., Dubcovsky J. (2018). Single nucleotide polymorphisms in a regulatory site of PubMed DOI PMC
Konopatskaia I., Vavilova V., Kondratenko E. Y., Blinov A., Goncharov N. P. (2016). PubMed DOI PMC
Kwon C.-T., Kim S.-H., Kim D., Paek N.-C. (2015). The rice floral repressor PubMed DOI PMC
Lago S., Nadai M., Cernilogar F. M., Kazerani M., Domíniguez Moreno H., Schotta G., et al. (2021). Promoter G-quadruplexes and transcription factors cooperate to shape the cell type-specific transcriptome. Nat. Commun. 12, 3885. doi: 10.1038/s41467-021-24198-2 PubMed DOI PMC
Lai X., Vega-Léon R., Hugouvieux V., Blanc-Mathieu R., van der Wal F., Lucas J., et al. (2021). The intervening domain is required for DNA-binding and functional identity of plant MADS transcription factors. Nat. Commun. 12, 4760. doi: 10.1038/s41467-021-24978-w PubMed DOI PMC
Leigh F. J., Wright T. I. C., Horsnell R. A., Dyer S., Bentley A. R. (2022). Progenitor species hold untapped diversity for potential climate-responsive traits for use in wheat breeding and crop improvement. Heredity (Edinb). 128, 291–303. doi: 10.1038/s41437-022-00527-z PubMed DOI PMC
Li H. (2013). Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv: Genomics. doi: 10.48550/arXiv.1303.3997 DOI
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
Liu G., Gao Y., Wang H., Wang Y., Chen J., Zhang P., et al. (2022). Premature termination codon of PubMed DOI PMC
Liu X., Huang M., Fan B., Buckler E. S., Zhang Z. (2016). Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PloS Genet. 12, e1005767. doi: 10.1371/journal.pgen.1005767 PubMed DOI PMC
Liu Z., Jia Y., Ding Y., Shi Y., Li Z., Guo Y., et al. (2017). Plasma membrane CRPK1-mediated phosphorylation of 14-3-3 proteins induces their nuclear import to fine-tune CBF signaling during cold response. Mol. Cell 66, 117–128.e5. doi: 10.1016/j.molcel.2017.02.016 PubMed DOI
Li G., Yu M., Fang T., Cao S., Carver B. F., Yan L. (2013). Vernalization requirement duration in winter wheat is controlled by PubMed DOI PMC
Lu F., Chen M., Zhao Y., Wu S., Yasir M., Zhang H., et al. (2022). Genetic mapping and candidate gene prediction of a QTL related to early heading on wild emmer chromosome 7BS in the genetic background of common wheat. Agronomy 12, 1089. doi: 10.3390/agronomy12051089 DOI
Maccaferri M., Harris N. S., Twardziok S. O., Pasam R. K., Gundlach H., Spannagl M., et al. (2019). Durum wheat genome highlights past domestication signatures and future improvement targets. Nat. Genet. 51, 885–895. doi: 10.1038/s41588-019-0381-3 PubMed DOI
Maizels N., Gray L. T. (2013). The G4 genome. PloS Genet. 9, e1003468. doi: 10.1371/journal.pgen.1003468 PubMed DOI PMC
Makhoul M., Chawla H. S., Wittkop B., Stahl A., Voss-Fels K. P., Zetzsche H., et al. (2022). Long-amplicon single-molecule sequencing reveals novel, trait-associated variants of PubMed DOI PMC
Maquat L. E. (1995). When cells stop making sense: effects of nonsense codons on RNA metabolism in vertebrate cells. RNA 1, 453–465. PubMed PMC
Ma H., Yanofsky M. F., Meyerowitz E. M. (1991). PubMed DOI
Mayer K. F. X., Rogers J., Doležel J., Pozniak C., Eversole K., Feuillet C., et al. (2014). A chromosome-based draft sequence of the hexaploid bread wheat ( PubMed DOI
Merchuk-Ovnat L., Barak V., Fahima T., Ordon F., Lidzbarsky G. A., Krugman T., et al. (2016). Ancestral QTL alleles from wild emmer wheat improve drought resistance and productivity in modern wheat cultivars. Front. Plant Sci. 7. doi: 10.3389/fpls.2016.00452 PubMed DOI PMC
Mulder N. J., Apweiler R., Attwood T. K., Bairoch A., Bateman A., Binns D., et al. (2007). New developments in the InterPro database. Nucleic Acids Res. 35, 224–228. doi: 10.1093/nar/gkl841 PubMed DOI PMC
Muterko A., Kalendar R., Salina E. (2016). Novel alleles of the PubMed DOI PMC
Nevo E., Fu Y.-B., Pavlicek T., Khalifa S., Tavasi M., Beiles A. (2012). Evolution of wild cereals during 28 years of global warming in Israel. Proc. Natl. Acad. Sci. 109, 3412–3415. doi: 10.1073/pnas.1121411109 PubMed DOI PMC
Nuttonson M. Y. (1955). Wheat-Climate Relationships and the Use of Phenology in Ascertaining the Thermal and Photo-Thermal Requirements of Wheat. Washington, DC: American Institute of Crop Ecology, 388pp.
Peng J. H., Fahima T., Röder M. S., Huang Q. Y., Dahan A., Li Y. C., et al. (2000). High-density molecular map of chromosome region harboring stripe-rust resistance genes PubMed DOI
Peng J., Ronin Y., Fahima T., Röder M. S., Li Y., Nevo E., et al. (2003). Domestication quantitative trait loci in PubMed DOI PMC
Piepho H. P., Möhring J., Melchinger A. E., Büchse A. (2008). BLUP for phenotypic selection in plant breeding and variety testing. Euphytica 161, 209–228. doi: 10.1007/s10681-007-9449-8 DOI
Pu L., Liu M., Kim S. Y., Chen L. F. O., Fletcher J. C., Renee Sung Z. (2013). EMBRYONIC FLOWER1 and ULTRAPETALA1 act antagonistically on arabidopsis development and stress response. Plant Physiol. 162, 812–830. doi: 10.1104/pp.112.213223 PubMed DOI PMC
Putterill J., Robson F., Lee K., Simon R., Coupland G. (1995). The PubMed DOI
Reader S. M., Miller T. E. (1991). The introduction into bread wheat of a major gene for resistance to powdery mildew from wild emmer wheat. Euphytica 53, 57–60. doi: 10.1007/BF00032033 DOI
Rezaei M. K., Shobbar Z. S., Shahbazi M., Abedini R., Zare S. (2013). Glutathione s-transferase (GST) family in barley: Identification of members, enzyme activity, and gene expression pattern. J. Plant Physiol. 170, 1277–1284. doi: 10.1016/j.jplph.2013.04.005 PubMed DOI
Rice P., Longden L., Bleasby A. (2000). EMBOSS: The European molecular biology open software suite. Trends Genet. 16, 276–277. doi: 10.1016/S0168-9525(00)02024-2 PubMed DOI
Robinson J. T., Thorvaldsdóttir H., Wenger A. M., Zehir A., Mesirov J. P. (2017). Variant review with the integrative genomics viewer. Cancer Res. 77, e31–e34. doi: 10.1158/0008-5472.CAN-17-0337 PubMed DOI PMC
Roncallo P. F., Akkiraju P. C., Cervigni G. L., Echenique V. C. (2017). QTL mapping and analysis of epistatic interactions for grain yield and yield-related traits in DOI
Rong J. K., Millet E., Manisterski J., Feldman M. (2000). A new powdery mildew resistance gene: Introgression from wild emmer into common wheat and RFLP-based mapping. Euphytica 115, 121–126. doi: 10.1023/A:1003950431049 DOI
Royo C., Soriano J. M., Alvaro F. (2017). “Wheat: A crop in the bottom of the Mediterranean diet pyramid,” in DOI
Saedler H., Becker A., Winter K. U., Kirchner C., Theißen G. (2001). MADS-box genes are involved in floral development and evolution. Acta Biochim. Pol. 48, 351–358. doi: 10.18388/abp.2001_3920 PubMed DOI
Saitou N., Nei M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425. doi: 10.1093/oxfordjournals.molbev.a040454 PubMed DOI
Shcherban A. B., Schichkina A. A., Salina E. A. (2016). The occurrence of spring forms in tetraploid PubMed DOI PMC
Shcherban A. B., Strygina K. V., Salina E. A. (2015). PubMed DOI PMC
Spiegel J., Cuesta S. M., Adhikari S., Hänsel-Hertsch R., Tannahill D., Balasubramanian S. (2021). G-Quadruplexes are transcription factor binding hubs in human chromatin. Genome Biol. 22, 117. doi: 10.1186/s13059-021-02324-z PubMed DOI PMC
Stelmakh A. F. (1998). Genetic systems regulating flowering response in wheat. Euphytica 100, 359–369. doi: 10.1023/a:1018374116006 DOI
Strejčková B., Milec Z., Holušová K., Cápal P., Vojtková T., Čegan R., et al. (2021). In-depth sequence analysis of bread wheat PubMed DOI PMC
Tamura K., Nei M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10, 512–526. doi: 10.1093/oxfordjournals.molbev.a040023 PubMed DOI
Tanaka C., Itoh T., Iwasaki Y., Mizuno N., Nasuda S., Murai K. (2018). Direct interaction between VRN1 protein and the promoter region of the wheat PubMed DOI
Trevaskis B., Bagnall D. J., Ellis M. H., Peacock W. J., Dennis E. S. (2003). MADS box genes control vernalization-induced flowering in cereals. Proc. Natl. Acad. Sci. 100, 13099–13104. doi: 10.1073/pnas.1635053100 PubMed DOI PMC
Valton A. L., Hassan-Zadeh V., Lema I., Boggetto N., Alberti P., Saintomé C., et al. (2014). G4 motifs affect origin positioning and efficiency in two vertebrate replicators. EMBO J. 33, 732–746. doi: 10.1002/embj.201387506 PubMed DOI PMC
Volná A., Bartas M., Nezval J., Špunda V., Pečinka P., Červeň J. (2021). Searching for G-Quadruplex-Binding proteins in plants: New insight into possible G-quadruplex regulation. BioTech 10, 20. doi: 10.3390/biotech10040020 PubMed DOI PMC
Wang R., Ma J., Zhang Q., Wu C., Zhao H., Wu Y., et al. (2019). Genome-wide identification and expression profiling of glutathione transferase gene family under multiple stresses and hormone treatments in wheat ( PubMed DOI PMC
Xiao J., Xu S., Li C., Xu Y., Xing L., Niu Y., et al. (2014). PubMed DOI PMC
Xing L., Li J., Xu Y., Xu Z., Chong K. (2009). Phosphorylation modification of wheat lectin VER2 is associated with vernalization-induced PubMed DOI PMC
Yang X., Cheema J., Zhang Y., Deng H., Duncan S., Umar M. I., et al. (2020). RNA G-Quadruplex structures exist and function PubMed DOI PMC
Yang Y., Fanning L., Jack T. (2003). The K domain mediates heterodimerization of the PubMed DOI
Yan L., Helguera M., Kato K., Fukuyama S., Sherman J., Dubcovsky J. (2004). Allelic variation at the PubMed DOI
Yan L., Loukoianov A., Tranquilli G., Helguera M., Fahima T., Dubcovsky J. (2003). Positional cloning of the wheat vernalization gene PubMed DOI PMC
Yoo S. Y., Kim Y., Kim S. Y., Lee J. S., Ahn J. H. (2007). Control of flowering time and cold response by a NAC-domain protein in PubMed DOI PMC
Zhu M., Gao J., Lin X. J., Gong Y. Y., Qi Y. C., Ma Y. L., et al. (2021). Novel roles of an intragenic G-quadruplex in controlling microRNA expression and cardiac function. Nucleic Acids Res. 49, 2522–2536. doi: 10.1093/nar/gkab055 PubMed DOI PMC