Ph2 encodes the mismatch repair protein MSH7-3D that inhibits wheat homoeologous recombination
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
33547285
PubMed Central
PMC7865012
DOI
10.1038/s41467-021-21127-1
PII: 10.1038/s41467-021-21127-1
Knihovny.cz E-zdroje
- MeSH
- alely MeSH
- chiméra MeSH
- chromozomy rostlin chemie MeSH
- DNA rostlinná genetika metabolismus MeSH
- fyzikální mapování chromozomů MeSH
- homologní rekombinace * MeSH
- meióza MeSH
- mutace MeSH
- oprava chybného párování bází DNA MeSH
- ploidie MeSH
- pšenice genetika metabolismus MeSH
- regulace genové exprese u rostlin * MeSH
- rostlinné proteiny genetika metabolismus MeSH
- šlechtění rostlin metody MeSH
- žito genetika metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- DNA rostlinná MeSH
- rostlinné proteiny MeSH
Meiotic recombination is a critical process for plant breeding, as it creates novel allele combinations that can be exploited for crop improvement. In wheat, a complex allohexaploid that has a diploid-like behaviour, meiotic recombination between homoeologous or alien chromosomes is suppressed through the action of several loci. Here, we report positional cloning of Pairing homoeologous 2 (Ph2) and functional validation of the wheat DNA mismatch repair protein MSH7-3D as a key inhibitor of homoeologous recombination, thus solving a half-century-old question. Similar to ph2 mutant phenotype, we show that mutating MSH7-3D induces a substantial increase in homoeologous recombination (up to 5.5 fold) in wheat-wild relative hybrids, which is also associated with a reduction in homologous recombination. These data reveal a role for MSH7-3D in meiotic stabilisation of allopolyploidy and provides an opportunity to improve wheat's genetic diversity through alien gene introgression, a major bottleneck facing crop improvement.
Zobrazit více v PubMed
Hajjar R, Hodgkin T. The use of wild relatives in crop improvement: a survey of developments over the last 20 years. Euphytica. 2007;156:1–13. doi: 10.1007/s10681-007-9363-0. DOI
Mercier R, Mézard C, Jenczewski E, Macaisne N, Grelon M. The molecular biology of meiosis in plants. Annu. Rev. Plant Biol. 2015;66:297–327. doi: 10.1146/annurev-arplant-050213-035923. PubMed DOI
Wood TE, et al. The frequency of polyploid speciation in vascular plants. Proc. Natl Acad. Sci. 2009;106:13875–13879. doi: 10.1073/pnas.0811575106. PubMed DOI PMC
Blake NK, Lehfeldt BR, Lavin M, Talbert LE. Phylogenetic reconstruction based on low copy DNA sequence data in an allopolyploid: the B genome of wheat. Genome. 1999;42:351–360. doi: 10.1139/g98-136. PubMed DOI
Huang S, et al. Genes encoding plastid acetyl-CoA carboxylase and 3-phosphoglycerate kinase of the Triticum/Aegilops complex and the evolutionary history of polyploid wheat. Proc. Natl Acad. Sci. 2002;99:8133–8138. doi: 10.1073/pnas.072223799. PubMed DOI PMC
Riley R, Chapman V. Genetic control of the cytologically diploid behaviour of hexaploid wheat. Nature. 1958;182:713–715. doi: 10.1038/182713a0. DOI
Sears ER. Intergenomic chromosome relationships in hexaploid wheat. Proc. Int. Congr. Genet. 1958;2:258–259.
Mello-Sampayo T, Lorente R. The role of chromosome 3D in the regulation of meiotic pairing in hexaploid wheat. EWAC Newsl. 1968;2:16–24.
Mello-Sampayo T. Genetic regulation of meiotic chromosome pairing by chromosome 3D of Triticum aestivum. Nat. N. Biol. 1971;230:22–23. doi: 10.1038/newbio230022a0. PubMed DOI
Giorgi, B. & Barbera, F. Use of mutants that affect homoeologous pairing for introducing alien variation in both durum and common wheat. (International Atomic Energy Agency, 1981).
Giorgi B, Barbera F. Increase of homoeologous pairing in hybrids between a ph mutant of T. turgidum L. var. durum and two tetraploid species of Aegilops: Aegilops kotschyi and Ae. cylindrica. Cereal Res. Commun. 1981;9:205–2.
Sears ER. An induced mutant with homoeologous pairing in wheat. Can. J. Genet. Cytol. 1977;19:585–593. doi: 10.1139/g77-063. DOI
Gill KS, Gill BS. A DNA fragment mapped within the submicroscopic deletion of Ph1, a chromosome pairing regulator gene in polyploid wheat. Genetics. 1991;129:257–259. doi: 10.1093/genetics/129.1.257. PubMed DOI PMC
Gill KS, Gill BS, Endo TR, Mukai Y. Fine physical mapping of Ph1, a chromosome pairing regulator gene in polyploid wheat. Genetics. 1993;134:1231–1236. doi: 10.1093/genetics/134.4.1231. PubMed DOI PMC
Griffiths S, et al. Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat. Nature. 2006;439:749–752. doi: 10.1038/nature04434. PubMed DOI
Al-Kaff N, et al. Detailed dissection of the chromosomal region containing the Ph1 locus in wheat Triticum aestivum: with deletion mutants and expression profiling. Ann. Bot. 2008;101:863–872. doi: 10.1093/aob/mcm252. PubMed DOI PMC
Martín AC, Rey M-D, Shaw P, Moore G. Dual effect of the wheat Ph1 locus on chromosome synapsis and crossover. Chromosoma. 2017;126:669–680. doi: 10.1007/s00412-017-0630-0. PubMed DOI PMC
Sidhu GK, Rustgi S, Shafqat MN, von Wettstein D, Gill KS. Fine structure mapping of a gene-rich region of wheat carrying Ph1, a suppressor of crossing over between homoeologous chromosomes. Proc. Natl Acad. Sci. 2008;105:5815–5820. doi: 10.1073/pnas.0800931105. PubMed DOI PMC
De Muyt A, et al. A meiotic XPF–ERCC1-like complex recognizes joint molecule recombination intermediates to promote crossover formation. Genes Dev. 2018;32:283–296. doi: 10.1101/gad.308510.117. PubMed DOI PMC
Rey M-D, et al. Exploiting the ZIP4 homologue within the wheat Ph1 locus has identified two lines exhibiting homoeologous crossover in wheat-wild relative hybrids. Mol. Breed. 2017;37:95. doi: 10.1007/s11032-017-0700-2. PubMed DOI PMC
Rey MD, et al. Magnesium increases homoeologous crossover frequency during meiosis in ZIP4 (Ph1 gene) mutant wheat-wild relative hybrids. Front. Plant Sci. 2018;9:1–12. doi: 10.3389/fpls.2018.00509. PubMed DOI PMC
Sutton T, et al. The Ph2 pairing homoeologous locus of wheat (Triticum aestivum): identification of candidate meiotic genes using a comparative genetics approach. Plant J. 2003;36:443–456. doi: 10.1046/j.1365-313X.2003.01891.x. PubMed DOI
Svačina R, et al. Development of deletion lines for chromosome 3D of bread wheat. Front. Plant Sci. 2020;10:1–6. doi: 10.3389/fpls.2019.01756. PubMed DOI PMC
Ji L-H, Langridge P. An early meiosis cDNA clone from wheat. Mol. Gen. Genet. 1994;243:17–23. doi: 10.1007/BF00283871. PubMed DOI
Whitford, R. From Intimate Chromosome Associations to Wild Sex in Wheat (Triticum aestivum). (University of Adelaide, Australia, 2002).
Letarte, J. Identification and Characterisation of Early Meiotic Genes in Wheat. (University of Adelaide, Australia, 1996).
Dong C, et al. WM5: isolation and characterisation of a gene expressed during early meiosis and shoot meristem development in wheat. Funct. Plant Biol. 2005;32:249. doi: 10.1071/FP04198. PubMed DOI
Dong C, Whitford R, Langridge P. A DNA mismatch repair gene links to the Ph2 locus in wheat. Genome. 2002;45:116–124. doi: 10.1139/g01-126. PubMed DOI
Lloyd AH, Milligan AS, Langridge P, Able JA. TaMSH7: a cereal mismatch repair gene that affects fertility in transgenic barley (Hordeum vulgare L.) BMC Plant Biol. 2007;7:1–9. doi: 10.1186/1471-2229-7-67. PubMed DOI PMC
Wall AM, Riley R, Chapman V. Wheat mutants permitting homoeologous meiotic chromosome pairing. Genet. Res. 1971;18:311–328. doi: 10.1017/S0016672300012714. DOI
Sears ER. A wheat mutation conditioning an intermediate level of homoeologous chromosome pairing. Can. J. Genet. Cytol. 1982;24:715–719. doi: 10.1139/g82-076. DOI
Martinez M, Cuñado N, Carcelén N, Romero C. The Ph1 and Ph2 loci play different roles in the synaptic behaviour of hexaploid wheat Triticum aestivum. Theor. Appl. Genet. 2001;103:398–405. doi: 10.1007/s00122-001-0543-3. DOI
Ceoloni C, Donini P. Combining mutations for the two homoeologous pairing suppressor genes Ph1 and Ph2 in common wheat and in hybrids with alien Triticeae. Genome. 1993;36:377–386. doi: 10.1139/g93-052. PubMed DOI
Appels R, et al. Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science. 2018;361:6403. PubMed
Mello-Sampayo, T. & Canas, P. Suppressors of meiotic chromosome pairing in common wheat. Proc 4th Wheat Genet. Symp. Columbia, Missouri, USA 709–713 (1973).
King R, et al. Mutation scanning in wheat by exon capture and next-generation sequencing. PLoS One. 2015;10:e0137549. doi: 10.1371/journal.pone.0137549. PubMed DOI PMC
Krasileva KV, et al. Uncovering hidden variation in polyploid wheat. Proc. Natl Acad. Sci. 2017;114:913–921. doi: 10.1073/pnas.1619268114. PubMed DOI PMC
Tam SM, Hays JB, Chetelat RT. Effects of suppressing the DNA mismatch repair system on homeologous recombination in tomato. Theor. Appl. Genet. 2011;123:1445–1458. doi: 10.1007/s00122-011-1679-4. PubMed DOI
Chirinos-arias MC, Spampinato CP. Plant physiology and biochemistry growth and development of AtMSH7 mutants in Arabidopsis thaliana. Plant Physiol. Biochem. 2020;146:329–336. doi: 10.1016/j.plaphy.2019.11.035. PubMed DOI
Alabdullah AK, et al. A co-expression network in hexaploid wheat reveals mostly balanced expression and lack of significant gene loss of homeologous meiotic genes upon polyploidization. Front. Plant Sci. 2019;10:1325. doi: 10.3389/fpls.2019.01325. PubMed DOI PMC
Martín AC, et al. Genome-wide transcription during early wheat meiosis is independent of synapsis, ploidy level, and the Ph1 locus. Front. Plant Sci. 2018;9:1–19. doi: 10.3389/fpls.2018.01791. PubMed DOI PMC
Watson-Haigh NS, Suchecki R, Kalashyan E, Garcia M, Baumann U. DAWN: a resource for yielding insights into the diversity among wheat genomes. BMC Genom. 2018;19:1–20. doi: 10.1186/s12864-018-5228-2. PubMed DOI PMC
Sears ER. Homoeologous chromosomes in Triticum aestivum. Genetics. 1952;37:624.
Sears ER. Genetic control of chromosome pairing in wheat. Annu. Rev. Genet. 1976;10:31–51. doi: 10.1146/annurev.ge.10.120176.000335. PubMed DOI
Reyes, G. X. et al. New insights into the mechanism of DNA mismatch repair. Chromosoma124, 443–462 (2016). PubMed PMC
Culligan KM, Hays JB. Arabidopsis MutS homologs - AtMSH2, AtMSH3, AtMSH6, and a Novel AtMSH7 - form three distinct protein heterodimers with different specificities for mismatched DNA. Plant Cell. 2000;12:991–1002. PubMed PMC
Wu SY, Culligan K, Lamers M, Hays J. Dissimilar mispair-recognition spectra of Arabidopsis DNA-mismatch-repair proteins MSH2·MSH6 (MutSα) and MSH2·MSH7 (MutSγ) Nucleic Acids Res. 2003;31:6027–6034. doi: 10.1093/nar/gkg780. PubMed DOI PMC
Gómez R, Spampinato CP. Mismatch recognition function of Arabidopsis thaliana MutSγ. DNA Repair. 2013;12:257–264. doi: 10.1016/j.dnarep.2013.01.002. PubMed DOI
McCulloch SD, Gu L, Li GM. Bi-directional processing of DNA loops by mismatch repair-dependent and -independent pathways in human cells. J. Biol. Chem. 2003;278:3891–3896. doi: 10.1074/jbc.M210687200. PubMed DOI
Tian L, Gu L, Li GM. Distinct nucleotide binding/hydrolysis properties and molar ratio of MutSα and MutSβ determine their differential mismatch binding activities. J. Biol. Chem. 2009;284:11557–11562. doi: 10.1074/jbc.M900908200. PubMed DOI PMC
Culligan KM. Evolutionary origin, diversification and specialization of eukaryotic MutS homolog mismatch repair proteins. Nucleic Acids Res. 2000;28:463–471. doi: 10.1093/nar/28.2.463. PubMed DOI PMC
Lario LD, Botta P, Casati P, Spampinato CP. Role of AtMSH7 in UV-B-induced DNA damage recognition and recombination. J. Exp. Bot. 2015;66:3019–3026. doi: 10.1093/jxb/eru464. PubMed DOI
Chakraborty U, Alani E. Understanding how mismatch repair proteins participate in the repair/anti-recombination decision. FEMS Yeast Res. 2016;16:1–12. doi: 10.1093/femsyr/fow071. PubMed DOI PMC
Hu Q, et al. Meiotic chromosome association 1 interacts with TOP3α and regulates meiotic recombination in rice. Plant Cell. 2017;29:1697–1708. doi: 10.1105/tpc.17.00241. PubMed DOI PMC
Fernandes JB, et al. FIGL1 and its novel partner FLIP form a conserved complex that regulates homologous recombination. PLoS Genet. 2018;14:e1007317. doi: 10.1371/journal.pgen.1007317. PubMed DOI PMC
Martín AC, Shaw P, Phillips D, Reader S, Moore G. Licensing MLH1 sites for crossover during meiosis. Nat. Commun. 2014;5:4580. doi: 10.1038/ncomms5580. PubMed DOI PMC
Driscoll CJ. Genetic suppression of homoeologous chromosome pairing in hexaploid wheat. Can. J. Genet. Cytol. 1972;14:39–42. doi: 10.1139/g72-004. DOI
Miller TE, Reader SM, Gale MD. The effect of homoeologous group 3 chromosomes on chromosome pairing and crossability in Triticum aestivum. Can. J. Genet. Cytol. 1983;25:634–641. doi: 10.1139/g83-094. DOI
Lloyd AH, et al. Meiotic gene evolution: can you teach a new dog new tricks? Mol. Biol. Evol. 2014;31:1724–1727. doi: 10.1093/molbev/msu119. PubMed DOI
Andrews, S. FastQC: a quality control tool for high throughput sequence data. Babraham Bioinforma. (2016). https://www.bioinformatics.babraham.ac.uk/projects/fastqc/.
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC
Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat. Methods. 2012;9:357–359. doi: 10.1038/nmeth.1923. PubMed DOI PMC
Li H, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078–2079. doi: 10.1093/bioinformatics/btp352. PubMed DOI PMC
Cingolani P, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff. Fly. 2012;6:80–92. doi: 10.4161/fly.19695. PubMed DOI PMC
Tucker EJ, et al. Molecular identification of the wheat male fertility gene Ms1 and its prospects for hybrid breeding. Nat. Commun. 2017;8:869. doi: 10.1038/s41467-017-00945-2. PubMed DOI PMC
Chen S, Zhou Y, Chen Y, Gu J. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34:i884–i890. doi: 10.1093/bioinformatics/bty560. PubMed DOI PMC
Dobin A, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29:15–21. doi: 10.1093/bioinformatics/bts635. PubMed DOI PMC
Guindon S, et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 2010;59:307–321. doi: 10.1093/sysbio/syq010. PubMed DOI
Zadoks JC, Chang TT, Konzak CF. A decimal code for the growth stages of cereals. Weed Res. 1974;14:415–421. doi: 10.1111/j.1365-3180.1974.tb01084.x. DOI
Pingault L, et al. Deep transcriptome sequencing provides new insights into the structural and functional organization of the wheat genome. Genome Biol. 2015;16:1–15. doi: 10.1186/s13059-015-0601-9. PubMed DOI PMC
Gametocidal genes: from a discovery to the application in wheat breeding
Meiotic Recognition of Evolutionarily Diverged Homologs: Chromosomal Hybrid Sterility Revisited