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Mechanism of haploidy-dependent unreductional meiotic cell division in polyploid wheat

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Abstract

Unreductional meiotic cell division (UMCD) generates unreduced gametes and leads to polyploidy. The tetraploid wheat “Langdon” (LDN) undergoes normal meiosis, but its polyhaploid undergoes UMCD. Here, we found that sister kinetochores oriented syntelically at meiosis I in LDN, but amphitelically in LDN polyhaploid and the interspecific hybrid of LDN with Aegilops tauschii. We also observed that sister centromere cohesion persisted until anaphase II in LDN, LDN polyhaploid, and the interspecific hybrid. Meiocytes with all chromosomes oriented amphitelically underwent UMCD in LDN polyhaploid, and the interspecific hybrid, suggesting the tension created by the amphitelic orientation of sister kinetochores and persistence of centromeric cohesion between sister chromatids at meiosis I contribute to the onset of UMCD. Most likely, some ploidy-regulated genes were responsible for kinetochore orientation at meiosis I in LDN and LDN-derived polyhaploids. In addition, we found sister kinetochores of synapsed chromosomes oriented syntelically, whereas asynapsed chromosomes oriented either amphitelically or syntelically. Thus, synapsis probably is another factor for the coordination of kinetochore orientation in LDN.

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References

  • Adams KL, Wendel JF (2005) Polyploidy and genome evolution in plants. Curr Opin Plant Biol 8:135–141

    Article  CAS  PubMed  Google Scholar 

  • Adams KL, Cronn R, Percifield R, Wendel JF (2003) Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc Natl Acad Sci USA 100:4649–4654

    Article  CAS  PubMed  Google Scholar 

  • Bai X, Peirson BN, Dong F, Xue C, Makaroff CA (1999) Isolation and characterization of SYN1, a RAD21-like gene essential for meiosis in Arabidopsis. Plant Cell 11:417–430

    Article  CAS  PubMed  Google Scholar 

  • Bannister LA, Reinholdt LG, Munroe RJ, Schimenti JC (2004) Positional cloning and characterization of mouse mei8, a disrupted allelle of the meiotic cohesin Rec8. Genesis 40:184–194

    Article  CAS  PubMed  Google Scholar 

  • Bastiaanssen HJM, Ramanna MS, Huigen DJ, Jacobsen E (1998) Selection of diploid tuberous Solanum hybrids for 2n-egg formation using 2x.4x-crosses. Euphytica 101:325–339

    Article  Google Scholar 

  • Blake NK, Lehfeldt BR, Lavin M, Talbert LE (1999) Phylogenetic reconstruction based on low copy DNA sequence data in an allopolyploid, the B genome of wheat. Genome 42:351–360

    Article  CAS  PubMed  Google Scholar 

  • Bretagnolle F, Thompson JD (1995) Tansley Review No. 78. Gametes with the stomatic chromosome number, mechanisms of their formation and role in the evolution of autopolypoid plants. New Phytol 129:1–22

    Article  Google Scholar 

  • Buonomo SB, Clyne RK, Fuchs J, Loidl J, Uhlmann F, Nasmyth K (2000) Disjunction of homologous chromosomes in meiosis I depends on proteolytic cleavage of the meiotic cohesin Rec8 by separin. Cell 103:387–398

    Article  CAS  PubMed  Google Scholar 

  • Cai X (1994) Chromosome translocations in the common wheat variety “Amigo”. Hereditas 121:199–202

    Article  Google Scholar 

  • Cai X, Xu SS (2007) Meiosis-driven genome variation in plants. Current Genomics 8:151–161

    Article  CAS  PubMed  Google Scholar 

  • Cai X, Dong F, Edelmann RE, Makaroff CA (2003) The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing. J Cell Sci 116:2999–3007

    Article  CAS  PubMed  Google Scholar 

  • Chan A, Cande WZ (1998) Maize meiotic spindles assemble around chromatin and do not require paired chromosomes. J Cell Sci 111:3507–3515

    CAS  PubMed  Google Scholar 

  • Chelysheva L, Diallo S, Vezon D, Gendrot G, Vrielynck N, Belcram K, Rocques N, Marquez-Lema A, Bhatt AM, Horlow C, Mercier R, Mezard C, Grelon M (2005) AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J Cell Sci 118:4621–4632

    Article  CAS  PubMed  Google Scholar 

  • Clyne RK, Katis VL, Jessop L, Benjamin KR, Herskowitz I, Lichten M, Nasmyth K (2003) Polo-like kinase Cdc5 promotes chiasmata formation and cosegregation of sister centromeres at meiosis I. Nat Cell Biol 5:480–485

    Article  CAS  PubMed  Google Scholar 

  • Dvorak J, Diterlizzi P, Zhang HB, Resta P (1993) The evolution of polyploid wheats—identification of the A-genome donor species. Genome 36:21–31

    Article  CAS  PubMed  Google Scholar 

  • Fukuda K, Sakamoto S (1992a) Cytological studies on unreduced male gamete formation in hybrids between tetraploid emmer wheats and Aegilops squarrosa L. Jap J Breed 42:255–266

    Google Scholar 

  • Fukuda K, Sakamoto S (1992b) Studies on the factors controlling the formation of unreduced gametes in hybrids between tetraploid emmer wheats and Aegilops squarrosa L. Jap J Breed 42:747–760

    Google Scholar 

  • Galitski T, Saldanha AJ, Styles CA, Lander ES, Fink GR (1999) Ploidy regulation of gene expression. Science 285:251–254

    Article  CAS  PubMed  Google Scholar 

  • Golubovskaya IN, Hamant O, Timofejeva L, Wang CJ, Braun D, Meeley R, Cande WZ (2006) Alleles of afd1 dissect REC8 functions during meiotic prophase I. J Cell Sci 119:3306–3315

    Article  CAS  PubMed  Google Scholar 

  • Hauf S, Biswas A, Langegger M, Kawashima SA, Tsukahara T, Watanabe Y (2007) Aurora controls sister kinetochore mono-orientation and homolog bi-orientation in meiosis-I. EMBO J 26:4475–4486

    Article  CAS  PubMed  Google Scholar 

  • He P, Friebe BR, Gill BS, Zhou JM (2003) Allopolyploidy alters gene expression in the highly stable hexaploid wheat. Plant Mol Biol 52:401–414

    Article  CAS  PubMed  Google Scholar 

  • Huang S, Sirikhachornkit A, Su XJ, Faris J, Gill B, Haselkorn R, Gornicki P (2002) 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 USA 99:8133–8138

    Article  CAS  PubMed  Google Scholar 

  • Jauhar PP (2007) Meiotic restitution in wheat polyhaploids (amphihaploids), a potent evolutionary force. J Hered 98:188–193

    Article  CAS  PubMed  Google Scholar 

  • Jauhar PP, Dogramaci-Altuntepe M, Peterson TS, Almouslem AB (2000) Seedset on synthetic haploids of durum wheat, cytological and molecular investigations. Crop Sci 40:1742–1749

    Article  Google Scholar 

  • Kantama L, Sharbel TF, Schranz ME, Mitchell-Olds T, de Vries S, de Jong H (2007) Diploid apomicts of the Boechera holboellii complex display large-scale chromosome substitutions and aberrant chromosomes. Proc Natl Acad Sci USA 104:14026–14031

    Article  CAS  PubMed  Google Scholar 

  • Kashkush K, Feldman M, Levy AA (2002) Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics 160:1651–1659

    CAS  PubMed  Google Scholar 

  • Kihara H (1944) Discovery of the DD-analyser, one of the ancestors of vulgare wheat. Ag Hort (Tokyo) 19:889–890

    Google Scholar 

  • Kleckner N (1996) Meiosis, how could it work? Proc Natl Acad Sci U S A 93:8167–8174

    Article  CAS  PubMed  Google Scholar 

  • Klein F, Mahr P, Galova M, Buonomo SBC, Michaelis C, Nairz K, Nasmyth K (1999) A central role for cohesions in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98:91–103

    Article  CAS  PubMed  Google Scholar 

  • Laurie DA, Bennet MD (1986) Wheat x maize hybridization. Can J Genet Cytol 28:313–316

    Google Scholar 

  • Lee B, Amon A (2001) Meiosis, how to create a specialized cell cycle. Curr Opin Cell Biol 13:770–777

    Article  CAS  PubMed  Google Scholar 

  • Lee BH, Amon A (2003) Role of Polo-like kinase CDC5 in programming meiosis I chromosome segregation. Science 300:482–486

    Article  CAS  PubMed  Google Scholar 

  • Lee HS, Chen ZJ (2001) Protein-coding genes are epigenetically regulated in Arabidopsis polyploids. Proc Natl Acad Sci USA 98:6753–6758

    Article  CAS  PubMed  Google Scholar 

  • Lee BH, Amon A, Prinz S (2002) Spo13 regulates cohesin cleavage. Genes Dev 16:1672–1681

    Article  CAS  PubMed  Google Scholar 

  • Lyrene PM, Vorsa N, Ballington JR (2003) Polyploidy and sexual polyploidization in the genus Vaccinium. Euphytica 133:27–36

    Article  Google Scholar 

  • Madlung A, Tyagi PA, Watson B, Jiang H, Kagochi T, Doerge RW, Martienssen R, Comai L (2005) Genomic changes in synthetic Arabidopsis polyploids. Plant J 41:221–230

    Article  CAS  PubMed  Google Scholar 

  • McFadden ES, Sears ER (1946) The origin of Triticum speltoides and its free-threshing hexaploid relatives. J Hered 37:81–89

    Google Scholar 

  • McKim KS, Hawley RS (1995) Chromosomal control of meiotic cell division. Science 270:1595–1601

    Article  CAS  PubMed  Google Scholar 

  • Monje-Casas F, Prabhu VR, Lee BH, Boselli M, Amon A (2007) Kinetochore orientation during meiosis is controlled by Aurora B and the monopolin complex. Cell 128:477–490

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco culture. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Ozkan H, Levy AA, Feldman M (2001) Allopolyploidy-induced rapid genome evolution in the wheat (Aegilops–Triticum) group. Plant Cell 13:1735–1747

    Article  CAS  PubMed  Google Scholar 

  • Paliulis LV, Nicklas RB (2000) The reduction of chromosome number in meiosis is determined by properties built into the chromosomes. J Cell Biol 150:1223–1232

    Article  CAS  PubMed  Google Scholar 

  • Parisi S, McKay MJ, Molnar M, Thompson MA, van der Spek PJ, van Drunen-Schoenmaker E, Kanaar R, Lehmann E, Hoeijmakers JH, Kohli J (1999) Rec8p, a meiotic recombination and sister chromatid cohesion phosphoprotein of the Rad21p family conserved from fission yeast to humans. Mol Cell Biol 19:3515–3528

    CAS  PubMed  Google Scholar 

  • Parra MT, Viera A, Gomez R, Page J, Benavente R, Santos JL, Rufas JS, Suja JA (2004) Involvement of the cohesin Rad21 and SCP3 in monopolar attachment of sister kinetochores during mouse meiosis I. J Cell Sci 117:1221–1234

    Article  CAS  PubMed  Google Scholar 

  • Pasierbek P, Jantsch M, Melcher M, Schleiffer A, Schweizer D, Loidl J (2001) A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes Dev 15:1349–1360

    Article  CAS  PubMed  Google Scholar 

  • Peloquin SJ (1982) Meiotic mutants in potato breeding. Stadler Symp 14:99–109

    Google Scholar 

  • Petronczki M, Matos J, Mori S, Gregan J, Bogdanova A, Schwickart M, Mechtler K, Shirahige K, Zachariae W, Nasmyth K (2006) Monopolar attachment of sister kinetochores at meiosis I requires casein kinase 1. Cell 126:1049–1064

    Article  CAS  PubMed  Google Scholar 

  • Ramanna MS, Jacobsen E (2003) Relevance of sexual polyploidization for crop improvement—a review. Euphytica 133:3–18

    Article  Google Scholar 

  • Riley R, Unrau J, Chapman V (1958) Evidence on the origin of the B genome of wheat. J Hered 49:91–98

    Google Scholar 

  • Shaked H, Kashkush K, Ozkan H, Feldman M, Levy AA (2001) Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. Plant Cell 13:1749–1759

    Article  CAS  PubMed  Google Scholar 

  • Shonn MA, McCarroll R, Murray AW (2002) Spo13 protects meiotic cohesin at centromeres in meiosis I. Genes Dev 16:1659–1671

    Article  CAS  PubMed  Google Scholar 

  • Stefani A (1986) Unreduced gametes in the F1 hybrid of Triticum durum Desf. X Haynaldia villosa Schur. Z Pflanzenzucht 96:8–14

    Google Scholar 

  • Takumi S, Nasuda S, Liu YG, Tsunewaki K (1993) Wheat phylogeny determined by RFLP analysis of nuclear-DNA.1. Einkorn wheat. Jap J Genet 68:73–79

    Article  Google Scholar 

  • Toth A, Rabitsch KP, Galova M, Schleiffer A, Buonomo SB, Nasmyth K (2000) Functional genomics identifies monopolin, a kinetochore protein required for segregation of homologs during meiosis I. Cell 103:1155–1168

    Article  CAS  PubMed  Google Scholar 

  • Uhlmann F, Nasmyth K (1998) Cohesion between sister chromatids must be established during DNA replication. Curr Biol 8:1095–1101

    Article  CAS  PubMed  Google Scholar 

  • Wagenaar EB (1968a) Meiotic restitution and the origin of polyploidy. I. Influence of genotype on polyploid seedset in a Triticum crassum × T. turgidum hybrid. Can J Genet Cytol 10:836–843

    Google Scholar 

  • Wagenaar EB (1968b) Meiotic restitution and the origin of polyploidy. II. Prolonged duration of metaphase I as causal factor of restitution induction. Can J Genet Cytol 10:844–852

    Google Scholar 

  • Wang J, Tian L, Lee HS, Wei NE, Jiang H, Watson B, Madlung A, Osborn TC, Doerge RW, Comai L, Chen ZJ (2006) Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172:507–517

    Article  CAS  PubMed  Google Scholar 

  • Watanabe Y (2004) Modifying sister chromatid cohesion for meiosis. J Cell Sci 117:4017–4023

    Article  CAS  PubMed  Google Scholar 

  • Watanabe Y, Nurse P (1999) Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400:461–464

    Article  CAS  PubMed  Google Scholar 

  • Watanabe Y, Yokobayashi S, Yamamoto M, Nurse P (2001) Pre-meiotic S phase is linked toreductional chromosome segregation and recombination. Nature 409:359–363

    Article  CAS  PubMed  Google Scholar 

  • Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249

    Article  CAS  PubMed  Google Scholar 

  • Xu S, Dong Y (1992) Fertility and meiotic mechanisms of hybrids between chromosome autoduplication tetraploid wheats and Aegilops species. Genome 35:379–384

    Google Scholar 

  • Xu SJ, Joppa LR (1995) Mechanisms and inheritance of first division restitution in hybrids of wheat, rye, and Aegilops squarrosa. Genome 38:607–615

    CAS  PubMed  Google Scholar 

  • Xu SJ, Joppa LR (2000a) Hexaploid triticales from hybrids of “Langdon” durum D-genome substitutions with “Gazelle” rye. Plant Breed 119:223–226

    Article  Google Scholar 

  • Xu SJ, Joppa LR (2000b) First-division restitution in hybrids of Langdon durum disomic substitution lines with rye and Aegilops squarrosa. Plant Breed 119:233–241

    Article  Google Scholar 

  • Yokobayashi S, Watanabe Y (2005) The kinetochore protein Moa1 enables cohesion-mediated monopolar attachment at meiosis I. Cell 123:803–817

    Article  CAS  PubMed  Google Scholar 

  • Yokobayashi S, Yamamoto M, Watanabe Y (2003) Cohesins determine the attachment manner of kinetochores to spindle microtubules at meiosis I in fission yeast. Mol Cell Biol 23:3965–3973

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Tao J, Wang S, Chong K, Wang T (2006) The rice OsRad21-4, an orthologue of yeast Rec8 protein, is required for efficient meiosis. Plant Mol Biol 60:533–554

    Article  CAS  PubMed  Google Scholar 

  • Zohary D, Feldman M (1962) Hybridization between amphiploids and the evolution of polyploids in the wheat (Aegilops–Triticum) group. Evolution 16:44–61

    Article  Google Scholar 

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Acknowledgements

We thank members of the Cai and Xu laboratories for their help in this research and Drs. Mike Christoffers and Lili Qi for critical review of this manuscript. This research was supported by the National Science Foundation under Grant No. 0457356.

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Authors and Affiliations

  1. Department of Plant Sciences, NDSU Dept. 7076, North Dakota State University, Fargo, ND, 58108-6050, USA

    Xiwen Cai & Xianwen Zhu

  2. USDA-ARS, Northern Crop Sciences Laboratory, Fargo, ND, 58108-6050, USA

    Steven S. Xu

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  1. Xiwen Cai
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Correspondence to Xiwen Cai.

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Communicated by I. Schubert

Xiwen Cai and Steven S. Xu contributed equally to this work.

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Cai, X., Xu, S.S. & Zhu, X. Mechanism of haploidy-dependent unreductional meiotic cell division in polyploid wheat. Chromosoma 119, 275–285 (2010). https://doi.org/10.1007/s00412-010-0256-y

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