Haplotype Analysis of the Pre-harvest Sprouting Resistance Locus Phs-A1 Reveals a Causal Role of TaMKK3-A in Global Germplasm
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
Grantová podpora
BBS/E/J/000C0628
Biotechnology and Biological Sciences Research Council - United Kingdom
PubMed
28955352
PubMed Central
PMC5602128
DOI
10.3389/fpls.2017.01555
Knihovny.cz E-zdroje
- Klíčová slova
- PM19, TaMKK3-A, Triticum aestivum, dormancy, haplotype, pre-harvest sprouting, seed,
- Publikační typ
- časopisecké články MeSH
Pre-harvest sprouting (PHS) is an important cause of quality loss in many cereal crops and is particularly prevalent and damaging in wheat. Resistance to PHS is therefore a valuable target trait in many breeding programs. The Phs-A1 locus on wheat chromosome arm 4AL has been consistently shown to account for a significant proportion of natural variation to PHS in diverse mapping populations. However, the deployment of sprouting resistance is confounded by the fact that different candidate genes, including the tandem duplicated Plasma Membrane 19 (PM19) genes and the mitogen-activated protein kinase kinase 3 (TaMKK3-A) gene, have been proposed to underlie Phs-A1. To further define the Phs-A1 locus, we constructed a physical map across this interval in hexaploid and tetraploid wheat. We established close proximity of the proposed candidate genes which are located within a 1.2 Mb interval. Genetic characterization of diverse germplasm used in previous genetic mapping studies suggests that TaMKK3-A, and not PM19, is the major gene underlying the Phs-A1 effect in European, North American, Australian and Asian germplasm. We identified the non-dormant TaMKK3-A allele at low frequencies within the A-genome diploid progenitor Triticum urartu genepool, and show an increase in the allele frequency in modern varieties. In United Kingdom varieties, the frequency of the dormant TaMKK3-A allele was significantly higher in bread-making quality varieties compared to feed and biscuit-making cultivars. Analysis of exome capture data from 58 diverse hexaploid wheat accessions identified fourteen haplotypes across the extended Phs-A1 locus and four haplotypes for TaMKK3-A. Analysis of these haplotypes in a collection of United Kingdom and Australian cultivars revealed distinct major dormant and non-dormant Phs-A1 haplotypes in each country, which were either rare or absent in the opposing germplasm set. The diagnostic markers and haplotype information reported in the study will help inform the choice of germplasm and breeding strategies for the deployment of Phs-A1 resistance into breeding germplasm.
HOKUREN Agricultural Research InstituteNaganuma Japan
John Innes CentreNorwich United Kingdom
The Institute for Cereal Crop Improvement Tel Aviv UniversityTel Aviv Israel
Zobrazit více v PubMed
Albrecht T., Oberforster M., Kempf H., Ramgraber L., Schacht J., Kazman E., et al. (2015). Genome-wide association mapping of preharvest sprouting resistance in a diversity panel of European winter wheats. J. Appl. Genet. 56 277–285. 10.1007/s13353-015-0286-5 PubMed DOI
Avni R., Nave M., Barad O., Baruch K., Twardziok S. O., Gundlach H., et al. (2017). Wild emmer genome architecture and diversity elucidate wheat evolution and domestication. Science 357 93–97. 10.1126/science.aan0032 PubMed DOI
Balcárková B., Frenkel Z., Škopová M., Abrouk M., Kumar A., Chao S., et al. (2016). A high resolution radiation hybrid map of wheat chromosome 4A. Front. Plant Sci. 7:2063 10.3389/fpls.2016.02063 PubMed DOI PMC
Barnard A., Smith M. F. (2009). The effect of rainfall and temperature on the preharvest sprouting tolerance of winter wheat in the dryland production areas of the Free State Province. Field Crops Res. 112 158–164. 10.1016/j.fcr.2009.02.011 DOI
Barrero J. M., Cavanagh C., Verbyla K. L., Tibbits J. F., Verbyla A. P., Huang B. E., et al. (2015). Transcriptomic analysis of wheat near-isogenic lines identifies PM19-A1 and A2 as candidates for a major dormancy QTL. Genome Biol. 16 93 10.1186/s13059-015-0665-6 PubMed DOI PMC
Barrero J. M., Jacobsen J., Gubler F. (2010). “Seed dormancy: approaches for finding new genes in cereals,” in Plant Developmental Biology - Biotechnological Perspectives Vol. 1 eds Pua E. C., Davey M. R. (Berlin: Springer; ) 361–381. 10.1007/978-3-642-02301-9_18 DOI
Borrill P., Adamski N., Uauy C. (2015). Genomics as the key to unlocking the polyploid potential of wheat. New Phytol. 208 1008–1022. 10.1111/nph.13533 PubMed DOI
Brennan J. P., Fox P. N. (1998). Impact of CIMMYT varieties on the genetic diversity of wheat in Australia, 1973-1993. Aust. J. Agric. Res. 49 175–178. 10.1071/A97065 DOI
Cabral A. L., Jordan M. C., Mccartney C. A., You F. M., Humphreys D. G., Maclachlan R., et al. (2014). Identification of candidate genes, regions and markers for pre-harvest sprouting resistance in wheat (Triticum aestivum L.). BMC Plant Biol. 14:340 10.1186/s12870-014-0340-1 PubMed DOI PMC
Chen C. X., Cai S. B., Bai G. H. (2008). A major QTL controlling seed dormancy and pre-harvest sprouting resistance on chromosome 4A in a Chinese wheat landrace. Mol. Breed. 21 351–358. 10.1007/s11032-007-9135-5 DOI
Clavijo B. J., Venturini L., Schudoma C., Accinelli G. G., Kaithakottil G., Wright J., et al. (2017). An improved assembly and annotation of the allohexaploid wheat genome identifies complete families of agronomic genes and provides genomic evidence for chromosomal translocations. Genome Res. 27 885–896. 10.1101/gr.217117.116 PubMed DOI PMC
Corbineau F., Xia Q., Bailly C., El-Maarouf-Bouteau H. (2014). Ethylene, a key factor in the regulation of seed dormancy. Front. Plant Sci. 5:539 10.3389/fpls.2014.00539 PubMed DOI PMC
Cvikova K., Cattonaro F., Alaux M., Stein N., Mayer K. F., Dolezel J., et al. (2015). High-throughput physical map anchoring via BAC-pool sequencing. BMC Plant Biol. 15:99 10.1186/s12870-015-0429-1 PubMed DOI PMC
Eagles H. A., Cane K., Vallance N. (2009). The flow of alleles of important photoperiod and vernalisation genes through Australian wheat. Crop Pasture Sci. 60 646–657. 10.1071/CP09014 DOI
Fang J., Chu C. (2008). Abscisic acid and the pre-harvest sprouting in cereals. Plant Signal. Behav. 3 1046–1048. 10.4161/psb.3.12.6606 PubMed DOI PMC
Flintham J. (2000). Different genetic components control coat-imposed and embryo-imposeddormancy in wheat. Seed Sci. Res. 10 43–50. 10.1017/S0960258500000052 DOI
Flintham J., Adlam R., Bassoi M., Holdsworth M., Gale M. D. (2002). Mapping genes for resistance to sprouting damage in wheat. Euphytica 126 39–45. 10.1023/A:1019632008244 DOI
Frenkel Z., Paux E., Mester D., Feuillet C., Korol A. (2010). LTC: a novel algorithm to improve the efficiency of contig assembly for physical mapping in complex genomes. BMC Bioinformatics 11:584 10.1186/1471-2105-11-584 PubMed DOI PMC
Gao X., Hu C. H., Li H. Z., Yao Y. J., Meng M., Dong L., et al. (2013). Factors affecting pre-harvest sprouting resistance in wheat (Triticum aestivum l.): a review. J. Anim. Plant Sci. 23 556–565.
Gatford K. T., Eastwood R. F., Halloran G. M. (2002). Germination inhibitors in bracts surrounding the grain of Triticum tauschii. Funct. Plant Biol. 29 881–890. 10.1071/PP01011 PubMed DOI
Hen-Avivi S., Savin O., Racovita R. C., Lee W. S., Adamski N. M., Malitsky S., et al. (2016). A metabolic gene cluster in the wheat W1 and the barley cer-cqu loci determines beta-diketone biosynthesis and glaucousness. Plant Cell 28 1440–1460. 10.1105/tpc.16.00197 PubMed DOI PMC
Hickey L. T., Dieters M. J., Delacy I. H., Kravchuk O. Y., Mares D. J., Banks P. M. (2009). Grain dormancy in fixed lines of white-grained wheat (Triticum aestivum L.) grown under controlled environmental conditions. Euphytica 168 303–310. 10.1007/s10681-009-9929-0 DOI
Himi E., Maekawa M., Miura H., Noda K. (2011). Development of PCR markers for Tamyb10 related to R-1, red grain color gene in wheat. Theor. Appl. Genet. 122 1561–1576. 10.1007/s00122-011-1555-2 PubMed DOI
Himi E., Noda K. (2005). Red grain colour gene (R) of wheat is a Myb-type transcription factor. Euphytica 143 239–242. 10.1007/s10681-005-7854-4 DOI
Jordan K. W., Wang S., Lun Y., Gardiner L. J., Maclachlan R., Hucl P., et al. (2015). A haplotype map of allohexaploid wheat reveals distinct patterns of selection on homoeologous genomes. Genome Biol. 16 48 10.1186/s13059-015-0606-4 PubMed DOI PMC
Knox R. E., Clarke F. R., Clarke J. M., Fox S. L., Depauw R. M., Singh A. K. (2012). Enhancing the identification of genetic loci and transgressive segregants for preharvest sprouting resistance in a durum wheat population. Euphytica 186 193–206. 10.1007/s10681-011-0557-0 DOI
Konieczny A., Ausubel F. M. (1993). A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J. 4 403–410. 10.1046/j.1365-313X.1993.04020403.x PubMed DOI
Kottearachchi N. S., Uchino N., Kato K., Miura H. (2006). Increased grain dormancy in white-grained wheat by introgression of preharvest sprouting tolerance QTLs. Euphytica 152 421–428. 10.1007/s10681-006-9231-3 DOI
Krasileva K., Buffalo V., Bailey P., Pearce S., Ayling S., Tabbita F., et al. (2013). Separating homeologs by phasing in the tetraploid wheat transcriptome. Genome Biol. 14:R66 10.1186/gb-2013-14-6-r66 PubMed DOI PMC
Krasileva K. V., Vasquez-Gross H. A., Howell T., Bailey P., Paraiso F., Clissold L., et al. (2017). Uncovering hidden variation in polyploid wheat. Proc. Natl. Acad. Sci. U.S.A. 114 E913–E921. 10.1073/pnas.1619268114 PubMed DOI PMC
Kulwal P., Ishikawa G., Benscher D., Feng Z., Yu L.-X., Jadhav A., et al. (2012). Association mapping for pre-harvest sprouting resistance in white winter wheat. Theor. Appl. Genet. 125 793–805. 10.1007/s00122-012-1872-0 PubMed DOI
Kulwal P. L., Kumar N., Gaur A., Khurana P., Khurana J. P., Tyagi A. K., et al. (2005). Mapping of a major QTL for pre-harvest sprouting tolerance on chromosome 3A in bread wheat. Theor. Appl. Genet. 111 1052–1059. 10.1007/s00122-005-0021-4 PubMed DOI
Kumar S., Knox R., Clarke F., Pozniak C., Depauw R., Cuthbert R., et al. (2015). Maximizing the identification of QTL for pre-harvest sprouting resistance using seed dormancy measures in a white-grained hexaploid wheat population. Euphytica 205 287–309. 10.1007/s10681-015-1460-x DOI
Lan X. J., Wei Y. M., Liu D. C., Yan Z. H., Zheng Y. L. (2005). Inheritance of seed dormancy in Tibetan semi-wild wheat accession Q1028. J. Appl. Genet. 46 133–138. PubMed
Li C., Ni P., Francki M., Hunter A., Zhang Y., Schibeci D., et al. (2004). Genes controlling seed dormancy and pre-harvest sprouting in a rice-wheat-barley comparison. Funct. Integr. Genomics 4 84–93. 10.1007/s10142-004-0104-3 PubMed DOI
Linkies A., Leubner-Metzger G. (2012). Beyond gibberellins and abscisic acid: how ethylene and jasmonates control seed germination. Plant Cell Rep. 31 253–270. 10.1007/s00299-011-1180-1 PubMed DOI
Liu S., Cai S., Graybosch R., Chen C., Bai G. (2008). Quantitative trait loci for resistance to pre-harvest sprouting in US hard white winter wheat Rio Blanco. Theor. Appl. Genet. 117 691–699. 10.1007/s00122-008-0810-7 PubMed DOI
Liu S., Sehgal S. K., Li J., Lin M., Trick H. N., Yu J., et al. (2013). Cloning and characterization of a critical regulator for preharvest sprouting in wheat. Genetics 195 263–273. 10.1534/genetics.113.152330 PubMed DOI PMC
Liu S., Sehgal S. K., Lin M., Li J., Trick H. N., Gill B. S., et al. (2015). Independent mis-splicing mutations in TaPHS1 causing loss of preharvest sprouting (PHS) resistance during wheat domestication. New Phytol. 208 928–935. 10.1111/nph.13489 PubMed DOI
Lohwasser U., Rehman Arif M. A., Börner A. (2013). Discovery of loci determining pre-harvest sprouting and dormancy in wheat and barley applying segregation and association mapping. Biol. Plant. 57 663–674. 10.1007/s10535-013-0332-2 DOI
Mares D., Mrva K. (2014). Wheat grain preharvest sprouting and late maturity alpha-amylase. Planta 240 1167–1178. 10.1007/s00425-014-2172-5 PubMed DOI
Mares D., Mrva K., Cheong J., Williams K., Watson B., Storlie E., et al. (2005). A QTL located on chromosome 4A associated with dormancy in white- and red-grained wheats of diverse origin. Theor. Appl. Genet. 111 1357–1364. 10.1007/s00122-005-0065-5 PubMed DOI
Matilla A. J., Matilla-Vázquez M. A. (2008). Involvement of ethylene in seed physiology. Plant Sci. 175 87–97. 10.1016/j.plantsci.2008.01.014 DOI
Mohan A., Kulwal P., Singh R., Kumar V., Mir R., Kumar J., et al. (2009). Genome-wide QTL analysis for pre-harvest sprouting tolerance in bread wheat. Euphytica 168 319–329. 10.1007/s10681-009-9935-2 DOI
Mori M., Uchino N., Chono M., Kato K., Miura H. (2005). Mapping QTLs for grain dormancy on wheat chromosome 3A and the group 4 chromosomes, and their combined effect. Theor. Appl. Genet. 110 1315–1323. 10.1007/s00122-005-1972-1 PubMed DOI
Munkvold J., Tanaka J., Benscher D., Sorrells M. (2009). Mapping quantitative trait loci for preharvest sprouting resistance in white wheat. Theor. Appl. Genet. 119 1223–1235. 10.1007/s00122-009-1123-1 PubMed DOI
nabim (2014). Wheat Varieties. Available at: http://www.nabim.org.uk/wheat/wheat-varieties [accessed April 19 2017].
Nakamura S., Abe F., Kawahigashi H., Nakazono K., Tagiri A., Matsumoto T., et al. (2011). A wheat homolog of MOTHER OF FT AND TFL1 acts in the regulation of germination. Plant Cell 23 3215–3229. 10.1105/tpc.111.088492 PubMed DOI PMC
Nakamura S., Pourkheirandish M., Morishige H., Kubo Y., Nakamura M., Ichimura K., et al. (2016). Mitogen-activated protein kinase kinase 3 regulates seed dormancy in barley. Curr. Biol. 26 775–781. 10.1016/j.cub.2016.01.024 PubMed DOI
Nave M., Avni R., Ben-Zvi B., Hale I., Distelfeld A. (2016). QTLs for uniform grain dimensions and germination selected during wheat domestication are co-located on chromosome 4B. Theor. Appl. Genet. 129 1303–1315. 10.1007/s00122-016-2704-4 PubMed DOI
Ogbonnaya F. C., Imtiaz M., Depauw R. M. (2007). Haplotype diversity of preharvest sprouting QTLs in wheat. Genome 50 107–118. 10.1139/g06-142 PubMed DOI
Ramirez-Gonzalez R. H., Segovia V., Bird N., Fenwick P., Holdgate S., Berry S., et al. (2015). RNA-Seq bulked segregant analysis enables the identification of high-resolution genetic markers for breeding in hexaploid wheat. Plant Biotechnol. J. 13 613–624. 10.1111/pbi.12281 PubMed DOI
Reeves J., Chiapparino E., Donini P., Ganal M., Guiard J., Hamrit S., et al. (2004). “Changes over time in the genetic diversity of four major European crops: a report from the GEDIFLUX Framework 5 Project,” in Proceedings of the 17th EUCARPIA General Congress, Tulln, Austria, 8–11 September 2004 eds Vollmann J., Grausgruber H., Ruckenbauer P. (Vienna: University of Natural Resources and Applied Life Sciences; ) 3–7.
Shaw P. D., Graham M., Kennedy J., Milne I., Marshall D. F. (2014). Helium: visualization of large scale plant pedigrees. BMC Bioinformatics 15:259 10.1186/1471-2105-15-259 PubMed DOI PMC
Shorinola O., Bird N., Simmonds J., Berry S., Henriksson T., Jack P., et al. (2016). The wheat Phs-A1 pre-harvest sprouting resistance locus delays the rate of seed dormancy loss and maps 0.3 cM distal to the PM19 genes in UK germplasm. J. Exp. Bot. 67 4169–4178. 10.1093/jxb/erw194 PubMed DOI PMC
Simsek S., Ohm J.-B., Lu H., Rugg M., Berzonsky W., Alamri M. S., et al. (2014). Effect of pre-harvest sprouting on physicochemical properties of starch in wheat. Foods 3 194–207. 10.3390/foods3020194 PubMed DOI PMC
Smith S. M., Maughan P. J. (2015). SNP genotyping using KASPar assays. Methods Mol. Biol. 1245 243–256. 10.1007/978-1-4939-1966-6_18 PubMed DOI
Solovyev V., Kosarev P., Seledsov I., Vorobyev D. (2006). Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biol. 7(Suppl. 1):S10 10.1186/gb-2006-7-s1-s10 PubMed DOI PMC
Torada A., Ikeguchi S., Koike M. (2005). Mapping and validation of PCR-based markers associated with a major QTL for seed dormancy in wheat. Euphytica 143 251–255. 10.1007/s10681-005-7872-2 DOI
Torada A., Koike M., Ikeguchi S., Tsutsui I. (2008). Mapping of a major locus controlling seed dormancy using backcrossed progenies in wheat (Triticum aestivum L.). Genome 51 426–432. 10.1139/G08-007 PubMed DOI
Torada A., Koike M., Ogawa T., Takenouchi Y., Tadamura K., Wu J., et al. (2016). A causal gene for seed dormancy on wheat chromosome 4A encodes a MAP kinase kinase. Curr. Biol. 26 782–787. 10.1016/j.cub.2016.01.063 PubMed DOI
Uauy C. (2017). Wheat genomics comes of age. Curr. Opin. Plant Biol. 36 142–148. 10.1016/j.pbi.2017.01.007 PubMed DOI
Voss-Fels K. P., Qian L., Parra-Londono S., Uptmoor R., Frisch M., Keeble-Gagnère G., et al. (2017). Linkage drag constrains the roots of modern wheat. Plant Cell Environ. 40 717–725. 10.1111/pce.12888 PubMed DOI
Wicker T., Matthews D. E., Keller B. (2000). TREP: a database for Triticeae repetitive elements. Trends Plant Sci. 7 561–562. 10.1016/S1360-1385(02)02372-5 DOI
Wingen L. U., Orford S., Goram R., Leverington-Waite M., Bilham L., Patsiou T. S., et al. (2014). Establishing the A. E. Watkins landrace cultivar collection as a resource for systematic gene discovery in bread wheat. Theor. Appl. Genet. 127 1831–1842. 10.1007/s00122-014-2344-5 PubMed DOI PMC
Xiao-bo R., Xiu-Jin L., Deng-Cai L., Jia-Li W., You-Liang Z. (2008). Mapping QTLs for pre-harvest sprouting tolerance on chromosome 2D in a synthetic hexaploid wheat × common wheat cross. J. Appl. Genet. 49 333–341. 10.1007/BF03195631 PubMed DOI
Zhang X. Q., Li C., Tay A., Lance R., Mares D., Cheong J., et al. (2008). A new PCR-based marker on chromosome 4AL for resistance to pre-harvest sprouting in wheat (Triticum aestivum L.). Mol. Breed. 22 227–236. 10.1007/s11032-008-9169-3 DOI
Zong Y., Wang Y., Li C., Zhang R., Chen K., Ran Y., et al. (2017). Precise base editing in rice, wheat and maize with a Cas9- cytidine deaminase fusion. Nat. Biotechnol. 35 438–440. 10.1038/nbt.3811 PubMed DOI