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.
Similar content being viewed by others
References
Adams KL, Wendel JF (2005) Polyploidy and genome evolution in plants. Curr Opin Plant Biol 8:135–141
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
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
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
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
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
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
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
Cai X (1994) Chromosome translocations in the common wheat variety “Amigo”. Hereditas 121:199–202
Cai X, Xu SS (2007) Meiosis-driven genome variation in plants. Current Genomics 8:151–161
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
Chan A, Cande WZ (1998) Maize meiotic spindles assemble around chromatin and do not require paired chromosomes. J Cell Sci 111:3507–3515
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
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
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
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
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
Galitski T, Saldanha AJ, Styles CA, Lander ES, Fink GR (1999) Ploidy regulation of gene expression. Science 285:251–254
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
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
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
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
Jauhar PP (2007) Meiotic restitution in wheat polyhaploids (amphihaploids), a potent evolutionary force. J Hered 98:188–193
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
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
Kashkush K, Feldman M, Levy AA (2002) Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics 160:1651–1659
Kihara H (1944) Discovery of the DD-analyser, one of the ancestors of vulgare wheat. Ag Hort (Tokyo) 19:889–890
Kleckner N (1996) Meiosis, how could it work? Proc Natl Acad Sci U S A 93:8167–8174
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
Laurie DA, Bennet MD (1986) Wheat x maize hybridization. Can J Genet Cytol 28:313–316
Lee B, Amon A (2001) Meiosis, how to create a specialized cell cycle. Curr Opin Cell Biol 13:770–777
Lee BH, Amon A (2003) Role of Polo-like kinase CDC5 in programming meiosis I chromosome segregation. Science 300:482–486
Lee HS, Chen ZJ (2001) Protein-coding genes are epigenetically regulated in Arabidopsis polyploids. Proc Natl Acad Sci USA 98:6753–6758
Lee BH, Amon A, Prinz S (2002) Spo13 regulates cohesin cleavage. Genes Dev 16:1672–1681
Lyrene PM, Vorsa N, Ballington JR (2003) Polyploidy and sexual polyploidization in the genus Vaccinium. Euphytica 133:27–36
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
McFadden ES, Sears ER (1946) The origin of Triticum speltoides and its free-threshing hexaploid relatives. J Hered 37:81–89
McKim KS, Hawley RS (1995) Chromosomal control of meiotic cell division. Science 270:1595–1601
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
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco culture. Physiol Plant 15:473–497
Ozkan H, Levy AA, Feldman M (2001) Allopolyploidy-induced rapid genome evolution in the wheat (Aegilops–Triticum) group. Plant Cell 13:1735–1747
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
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
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
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
Peloquin SJ (1982) Meiotic mutants in potato breeding. Stadler Symp 14:99–109
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
Ramanna MS, Jacobsen E (2003) Relevance of sexual polyploidization for crop improvement—a review. Euphytica 133:3–18
Riley R, Unrau J, Chapman V (1958) Evidence on the origin of the B genome of wheat. J Hered 49:91–98
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
Shonn MA, McCarroll R, Murray AW (2002) Spo13 protects meiotic cohesin at centromeres in meiosis I. Genes Dev 16:1659–1671
Stefani A (1986) Unreduced gametes in the F1 hybrid of Triticum durum Desf. X Haynaldia villosa Schur. Z Pflanzenzucht 96:8–14
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
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
Uhlmann F, Nasmyth K (1998) Cohesion between sister chromatids must be established during DNA replication. Curr Biol 8:1095–1101
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
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
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
Watanabe Y (2004) Modifying sister chromatid cohesion for meiosis. J Cell Sci 117:4017–4023
Watanabe Y, Nurse P (1999) Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400:461–464
Watanabe Y, Yokobayashi S, Yamamoto M, Nurse P (2001) Pre-meiotic S phase is linked toreductional chromosome segregation and recombination. Nature 409:359–363
Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249
Xu S, Dong Y (1992) Fertility and meiotic mechanisms of hybrids between chromosome autoduplication tetraploid wheats and Aegilops species. Genome 35:379–384
Xu SJ, Joppa LR (1995) Mechanisms and inheritance of first division restitution in hybrids of wheat, rye, and Aegilops squarrosa. Genome 38:607–615
Xu SJ, Joppa LR (2000a) Hexaploid triticales from hybrids of “Langdon” durum D-genome substitutions with “Gazelle” rye. Plant Breed 119:223–226
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
Yokobayashi S, Watanabe Y (2005) The kinetochore protein Moa1 enables cohesion-mediated monopolar attachment at meiosis I. Cell 123:803–817
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
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
Zohary D, Feldman M (1962) Hybridization between amphiploids and the evolution of polyploids in the wheat (Aegilops–Triticum) group. Evolution 16:44–61
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by I. Schubert
Xiwen Cai and Steven S. Xu contributed equally to this work.
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00412-010-0256-y