A novel allele of ASY3 is associated with greater meiotic stability in autotetraploid Arabidopsis lyrata

Autoři: Paul J. Seear aff001;  Martin G. France aff001;  Catherine L. Gregory aff001;  Darren Heavens aff002;  Roswitha Schmickl aff003;  Levi Yant aff005;  James D. Higgins aff001
Působiště autorů: Department of Genetics and Genome Biology, University of Leicester, Leicester, United Kingdom aff001;  Earlham Institute, Norwich Research Park Innovation Centre, Norwich, United Kingdom aff002;  Department of Botany, Faculty of Science, Charles University, Prague, Czech Republic aff003;  Institute of Botany, The Czech Academy of Sciences, Průhonice, Czech Republic aff004;  Future Food Beacon of Excellence and the School of Life Sciences, University of Nottingham, Nottingham, United Kingdom aff005
Vyšlo v časopise: A novel allele of ASY3 is associated with greater meiotic stability in autotetraploid Arabidopsis lyrata. PLoS Genet 16(7): e32767. doi:10.1371/journal.pgen.1008900
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008900


In this study we performed a genotype-phenotype association analysis of meiotic stability in 10 autotetraploid Arabidopsis lyrata and A. lyrata/A. arenosa hybrid populations collected from the Wachau region and East Austrian Forealps. The aim was to determine the effect of eight meiosis genes under extreme selection upon adaptation to whole genome duplication. Individual plants were genotyped by high-throughput sequencing of the eight meiosis genes (ASY1, ASY3, PDS5b, PRD3, REC8, SMC3, ZYP1a/b) implicated in synaptonemal complex formation and phenotyped by assessing meiotic metaphase I chromosome configurations. Our results reveal that meiotic stability varied greatly (20–100%) between individual tetraploid plants and associated with segregation of a novel ASYNAPSIS3 (ASY3) allele derived from A. lyrata. The ASY3 allele that associates with meiotic stability possesses a putative in-frame tandem duplication (TD) of a serine-rich region upstream of the coiled-coil domain that appears to have arisen at sites of DNA microhomology. The frequency of multivalents observed in plants homozygous for the ASY3 TD haplotype was significantly lower than in plants heterozygous for ASY3 TD/ND (non-duplicated) haplotypes. The chiasma distribution was significantly altered in the stable plants compared to the unstable plants with a shift from proximal and interstitial to predominantly distal locations. The number of HEI10 foci at pachytene that mark class I crossovers was significantly reduced in a plant homozygous for ASY3 TD compared to a plant heterozygous for ASY3 ND/TD. Fifty-eight alleles of the 8 meiosis genes were identified from the 10 populations analysed, demonstrating dynamic population variability at these loci. Widespread chimerism between alleles originating from A. lyrata/A. arenosa and diploid/tetraploids indicates that this group of rapidly evolving genes may provide precise adaptive control over meiotic recombination in the tetraploids, the very process that gave rise to them.

Klíčová slova:

Alleles – Haplotypes – Meiosis – Phosphorylation – Polymerase chain reaction – Sequence alignment – Serine – Tetraploidy – Plant genomics – Single nucleotide polymorphisms


1. Alix K, Gerard PR, Schwarzacher T, Heslop-Harrison JSP. Polyploidy and interspecific hybridization: partners for adaptation, speciation and evolution in plants. Ann Bot. 2017;120(2):183–94. doi: 10.1093/aob/mcx079 28854567.

2. Selmecki AM, Maruvka YE, Richmond PA, Guillet M, Shoresh N, Sorenson AL, et al. Polyploidy can drive rapid adaptation in yeast. Nature. 2015;519(7543):349–52. doi: 10.1038/nature14187 25731168.

3. Baduel P, Bray S, Vallejo-Marin M, Kolar F, Yant L. The "Polyploid Hop": Shifting Challenges and Opportunities Over the Evolutionary Lifespan of Genome Duplications. Front Ecol Evol. 2018;6. ARTN 117 doi: 10.3389/fevo.2018.00117

4. Rey MD, Martin AC, Higgins J, Swarbreck D, Uauy C, Shaw P, 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(8):95. doi: 10.1007/s11032-017-0700-2 28781573.

5. Gonzalo A, Lucas MO, Charpentier C, Sandmann G, Lloyd A, Jenczewski E. Reducing MSH4 copy number prevents meiotic crossovers between non-homologous chromosomes in Brassica napus. Nat Commun. 2019;10(1):2354. doi: 10.1038/s41467-019-10010-9 31142748.

6. Jenczewski E, Eber F, Grimaud A, Huet S, Lucas MO, Monod H, et al. PrBn, a major gene controlling homeologous pairing in oilseed rape (Brassica napus) haploids. Genetics. 2003;164(2):645–53. 12807785.

7. Henry IM, Dilkes BP, Tyagi A, Gao J, Christensen B, Comai L. The BOY NAMED SUE quantitative trait locus confers increased meiotic stability to an adapted natural allopolyploid of Arabidopsis. Plant Cell. 2014;26(1):181–94. doi: 10.1105/tpc.113.120626 24464296.

8. Yant L, Hollister JD, Wright KM, Arnold BJ, Higgins JD, Franklin FCH, et al. Meiotic adaptation to genome duplication in Arabidopsis arenosa. Curr Biol. 2013;23(21):2151–6. Epub 2013/10/22. doi: 10.1016/j.cub.2013.08.059 24139735.

9. Page SL, Hawley RS. The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol. 2004;20:525–58. doi: 10.1146/annurev.cellbio.19.111301.155141 15473851.

10. Lam WS, Yang X, Makaroff CA. Characterization of Arabidopsis thaliana SMC1 and SMC3: evidence that AtSMC3 may function beyond chromosome cohesion. J Cell Sci. 2005;118(Pt 14):3037–48. doi: 10.1242/jcs.02443 15972315.

11. Pradillo M, Knoll A, Oliver C, Varas J, Corredor E, Puchta H, et al. Involvement of the Cohesin Cofactor PDS5 (SPO76) During Meiosis and DNA Repair in Arabidopsis thaliana. Front Plant Sci. 2015;6:1034. doi: 10.3389/fpls.2015.01034 26648949.

12. Bhatt AM, Lister C, Page T, Fransz P, Findlay K, Jones GH, et al. The DIF1 gene of Arabidopsis is required for meiotic chromosome segregation and belongs to the REC8/RAD21 cohesin gene family. Plant J. 1999;19(4):463–72. doi: 10.1046/j.1365-313x.1999.00548.x 10504568

13. Cai X, Dong F, Edelmann RE, Makaroff CA. The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing. J Cell Sci. 2003;116(Pt 14):2999–3007. doi: 10.1242/jcs.00601 12783989.

14. Chelysheva L, Diallo S, Vezon D, Gendrot G, Vrielynck N, Belcram K, et al. AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J Cell Sci. 2005;118(Pt 20):4621–32. doi: 10.1242/jcs.02583 16176934.

15. Lambing C, Tock AJ, Topp SD, Choi K, Kuo PC, Zhao X, et al. Interacting genomic landscapes of REC8-cohesin, chromatin and meiotic recombination in Arabidopsis thaliana. Plant Cell. 2020. Epub 2020/02/07. doi: 10.1105/tpc.19.00866 32024691.

16. Tesse S, Bourbon HM, Debuchy R, Budin K, Dubois E, Liangran Z, et al. Asy2/Mer2: an evolutionarily conserved mediator of meiotic recombination, pairing, and global chromosome compaction. Genes Dev. 2017;31(18):1880–93. Epub 2017/10/13. doi: 10.1101/gad.304543.117 29021238.

17. De Muyt A, Pereira L, Vezon D, Chelysheva L, Gendrot G, Chambon A, et al. A high throughput genetic screen identifies new early meiotic recombination functions in Arabidopsis thaliana. Plos Genet. 2009;5(9):e1000654. doi: 10.1371/journal.pgen.1000654 19763177.

18. Armstrong SJ, Caryl AP, Jones GH, Franklin FC. Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci. 2002;115(Pt 18):3645–55. doi: 10.1242/jcs.00048 12186950.

19. Ferdous M, Higgins JD, Osman K, Lambing C, Roitinger E, Mechtler K, et al. Inter-homolog crossing-over and synapsis in Arabidopsis meiosis are dependent on the chromosome axis protein AtASY3. Plos Genet. 2012;8(2):e1002507. doi: 10.1371/journal.pgen.1002507 22319460.

20. Chambon A, West A, Vezon D, Horlow C, De Muyt A, Chelysheva L, et al. Identification of ASYNAPTIC4, a Component of the Meiotic Chromosome Axis. Plant Physiol. 2018;178(1):233–46. doi: 10.1104/pp.17.01725 30002256.

21. Caryl AP, Armstrong SJ, Jones GH, Franklin FC. A homologue of the yeast HOP1 gene is inactivated in the Arabidopsis meiotic mutant asy1. Chromosoma. 2000;109(1–2):62–71. Epub 2000/06/16. doi: 10.1007/s004120050413 10855496.

22. West AMV, Rosenbereg SC, Ur SN, Lehmern MK, Ye QZ, Hagemann G, et al. A conserved filamentous assembly underlies the structure of the meiotic chromosome axis. Elife. 2019;8. ARTN e40372 doi: 10.7554/eLife.40372 30657449

23. Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FC. The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev. 2005;19(20):2488–500. doi: 10.1101/gad.354705 16230536.

24. Schmickl R, Koch MA. Arabidopsis hybrid speciation processes. Proc Natl Acad Sci U S A. 2011;108(34):14192–7. Epub 2011/08/10. doi: 10.1073/pnas.1104212108 21825128.

25. Marburger S, Monnahan P, Seear PJ, Martin SH, Koch J, Paajanen P, et al. Interspecific introgression mediates adaptation to whole genome duplication. Nat Commun. 2019;10(1):5218. Epub 2019/11/20. doi: 10.1038/s41467-019-13159-5 31740675.

26. Hohmann N, Koch MA. An Arabidopsis introgression zone studied at high spatio-temporal resolution: interglacial and multiple genetic contact exemplified using whole nuclear and plastid genomes. BMC Genomics. 2017;18(1):810. Epub 2017/10/24. doi: 10.1186/s12864-017-4220-6 29058582.

27. Arnold B, Kim ST, Bomblies K. Single Geographic Origin of a Widespread Autotetraploid Arabidopsis arenosa Lineage Followed by Interploidy Admixture. Mol Biol Evol. 2015;32(6):1382–95. Epub 2015/04/12. doi: 10.1093/molbev/msv089 25862142.

28. Lafon-Placette C, Köhler C. Endosperm-based postzygotic hybridization barriers: developmental mechanisms and evolutionary drivers. Molecular Ecology. 2016;25(11):2620–9. doi: 10.1111/mec.13552 26818717

29. Morgan C, Zhang H, Henry CE, Franklin FCH, Bomblies K. Derived alleles of two axis proteins affect meiotic traits in autotetraploid Arabidopsis arenosa. Proceedings of the National Academy of Sciences. 2020;117(16):8980–8. doi: 10.1073/pnas.1919459117 32273390

30. Chelysheva L, Vezon D, Chambon A, Gendrot G, Pereira L, Lemhemdi A, et al. The Arabidopsis HEI10 is a new ZMM protein related to Zip3. Plos Genet. 2012;8(7):e1002799. Epub 2012/07/31. doi: 10.1371/journal.pgen.1002799 22844245.

31. Wright KM, Arnold B, Xue K, Surinova M, O'Connell J, Bomblies K. Selection on meiosis genes in diploid and tetraploid Arabidopsis arenosa. Mol Biol Evol. 2015;32(4):944–55. doi: 10.1093/molbev/msu398 25543117.

32. Grishaeva TM, Bogdanov YF. Conservation and variability of synaptonemal complex proteins in phylogenesis of eukaryotes. Int J Evol Biol. 2014;2014:856230. Epub 2014/08/26. doi: 10.1155/2014/856230 25147749.

33. Yang C, Sofroni K, Wijnker E, Hamamura Y, Carstens L, Harashima H, et al. The Arabidopsis Cdk1/Cdk2 homolog CDKA;1 controls chromosome axis assembly during plant meiosis. The EMBO Journal. 2020;39(3):e101625. doi: 10.15252/embj.2019101625 31556459

34. Osman K, Yang J, Roitinger E, Lambing C, Heckmann S, Howell E, et al. Affinity proteomics reveals extensive phosphorylation of the Brassica chromosome axis protein ASY1 and a network of associated proteins at prophase I of meiosis. Plant J. 2018;93(1):17–33. doi: 10.1111/tpj.13752 29078019.

35. Brakenhoff RH, Schoenmakers JG, Lubsen NH. Chimeric cDNA clones: a novel PCR artifact. Nucleic Acids Res. 1991;19(8):1949. Epub 1991/04/25. doi: 10.1093/nar/19.8.1949 2030976.

36. Chen JM, Cooper DN, Chuzhanova N, Ferec C, Patrinos GP. Gene conversion: mechanisms, evolution and human disease. Nat Rev Genet. 2007;8(10):762–75. Epub 2007/09/12. doi: 10.1038/nrg2193 17846636.

37. Hazarika MH, Rees H. Genotypic control of chromosome behaviour in rye X. Chromosome pairing and fertility in autotetraploids. Heredity. 1967;22(3):317–32. doi: 10.1038/hdy.1967.44

38. He W, Rao H, Tang S, Bhagwat N, Kulkarni DS, Ma Y, et al. Regulated Proteolysis of MutSgamma Controls Meiotic Crossing Over. Mol Cell. 2020. Epub 2020/03/05. doi: 10.1016/j.molcel.2020.02.001 32130890.

39. Mergner J, Frejno M, List M, Papacek M, Chen X, Chaudhary A, et al. Mass-spectrometry-based draft of the Arabidopsis proteome. Nature. 2020. doi: 10.1038/s41586-020-2094-2 32188942

40. Sanchez-Moran E, Santos JL, Jones GH, Franklin FC. ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev. 2007;21(17):2220–33. doi: 10.1101/gad.439007 17785529.

41. Jorgensen MH, Ehrich D, Schmickl R, Koch MA, Brysting AK. Interspecific and interploidal gene flow in Central European Arabidopsis (Brassicaceae). BMC Evol Biol. 2011;11:346. doi: 10.1186/1471-2148-11-346 22126410.

42. Bomblies K, Higgins JD, Yant L. Meiosis evolves: adaptation to external and internal environments. The New phytologist. 2015;208(2):306–23. doi: 10.1111/nph.13499 26075313.

43. Giraut L, Falque M, Drouaud J, Pereira L, Martin OC, Mezard C. Genome-Wide Crossover Distribution in Arabidopsis thaliana Meiosis Reveals Sex-Specific Patterns along Chromosomes. Plos Genet. 2011;7(11). ARTN e1002354 doi: 10.1371/journal.pgen.1002354 22072983

44. Otto SP. The evolutionary consequences of polyploidy. Cell. 2007;131(3):452–62. doi: 10.1016/j.cell.2007.10.022 17981114.

45. Monnahan P, Kolar F, Baduel P, Sailer C, Koch J, Horvath R, et al. Pervasive population genomic consequences of genome duplication in Arabidopsis arenosa. Nat Ecol Evol. 2019;3(3):457–68. doi: 10.1038/s41559-019-0807-4 30804518.

46. Hu TT, Pattyn P, Bakker EG, Cao J, Cheng JF, Clark RM, et al. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet. 2011;43(5):476–+. doi: 10.1038/ng.807 21478890

47. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–7. doi: 10.1093/nar/gkh340 15034147.

48. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59(3):307–21. Epub 2010/06/09. doi: 10.1093/sysbio/syq010 20525638.

49. Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17(8):754–5. Epub 2001/08/29. doi: 10.1093/bioinformatics/17.8.754 11524383.

50. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol Biol Evol. 2018;35(6):1547–9. Epub 2018/05/04. doi: 10.1093/molbev/msy096 29722887.

51. Mascher M, Gundlach H, Himmelbach A, Beier S, Twardziok SO, Wicker T, et al. A chromosome conformation capture ordered sequence of the barley genome. Nature. 2017;544(7651):427–33. doi: 10.1038/nature22043 28447635.

52. Higgins JD, Wright KM, Bomblies K, Franklin FC. Cytological techniques to analyze meiosis in Arabidopsis arenosa for investigating adaptation to polyploidy. Front Plant Sci. 2014;4:546. doi: 10.3389/fpls.2013.00546 24427164.

53. Chelysheva L, Grandont L, Vrielynck N, le Guin S, Mercier R, Grelon M. An easy protocol for studying chromatin and recombination protein dynamics during Arabidopsis thaliana meiosis: immunodetection of cohesins, histones and MLH1. Cytogenet Genome Res. 2010;129(1–3):143–53. Epub 2010/07/16. doi: 10.1159/000314096 20628250.

54. Lambing C, Osman K, Nuntasoontorn K, West A, Higgins JD, Copenhaver GP, et al. Arabidopsis PCH2 Mediates Meiotic Chromosome Remodeling and Maturation of Crossovers. Plos Genet. 2015;11(7):e1005372. doi: 10.1371/journal.pgen.1005372 26182244.

55. Wong YH, Lee TY, Liang HK, Huang CM, Wang TY, Yang YH, et al. KinasePhos 2.0: a web server for identifying protein kinase-specific phosphorylation sites based on sequences and coupling patterns. Nucleic Acids Research. 2007;35:W588–W94. doi: 10.1093/nar/gkm322 17517770

56. Blom N, Sicheritz-Ponten T, Gupta R, Gammeltoft S, Brunak S. Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics. 2004;4(6):1633–49. doi: 10.1002/pmic.200300771 15174133.

57. Zhao Q, Xie YB, Zheng YY, Jiang S, Liu WZ, Mu WP, et al. GPS-SUMO: a tool for the prediction of sumoylation sites and SUMO-interaction motifs. Nucleic Acids Research. 2014;42(W1):W325–W30. doi: 10.1093/nar/gku383 24880689

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