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United States Department of Agriculture

Agricultural Research Service

Research Project: IMPROVEMENT OF HARD RED SPRING AND DURUM WHEAT FOR DISEASE RESISTANCE AND QUALITY USING GENETICS AND GENOMICS Title: Ploidy-Dependent Unreductional Meiotic Cell Division in Polyploid Wheat

Authors
item Cai, Xiwen -
item Xu, Steven
item Zhu, Xianwen -

Submitted to: Chromosoma
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: January 6, 2010
Publication Date: February 2, 2010
Citation: Cai, X., Xu, S.S., Zhu, X. 2010. Ploidy-Dependent Unreductional Meiotic Cell Division in Polyploid Wheat. Chromosoma. 119:275-285

Interpretive Summary: Meiosis is a specialized cell division to generate gametes (i.e. eggs and sperms) involved in sexual reproduction. Meiosis includes two successive nuclear divisions, i.e. first meiotic division (meiosis I) and second meiotic division (meiosis II). The first meiotic division involves pairing and segregation of homologous (identical) chromosomes and reduces the number of chromosomes in half. The second meiotic division involves separation of two daughter strands of chromosomes and formation of four daughter cells which subsequently develop to gametes. Thereby, meiosis I is reductional and meiosis II equational. Meiosis ensures genome stability and any deviations from normal meiosis lead to various genetic consequences, including aneuploidy (individuals having extra copies or missing copies of specific chromosomes) and polyploidy (individual having one or more extra sets of chromosomes). Unreductional meiotic cell division (UMCD), also known as meiotic restitution, is a variant meiotic division that gives rise to unreduced gametes due to the failure of chromosome segregation and leads to the formation of polyploidy. It has been considered a significant driving force for origin of polyploidy in nature. The mechanisms underlying UMCD, however, are still obscure. Because orientation of sister centromeres (the most condensed region of a chromosome) of paired chromosomes steers chromosome segregation in cell division, we attempted to elucidate the mechanisms of UMCD by investigating orientation of sister centromeres in UMCD and regular cell division. From this study, we found that sister centromeres co-oriented to the same pole at meiosis I in wheat ‘Langdon’ (LDN), but bi-oriented toward two opposite poles under haploid condition even though co-oriented chromosomes were also observed. It was also found that chromosomal cohesion persisted in the centromeric region until late stage of meiosis II in both LDN and its haploid. The cells with all chromosomes bi-oriented underwent UMCD and generated unreduced gametes under haploid condition of LDN. We concluded that the tension created by bi-orientation of sister centromeres prevented chromosomes from migrating toward either of poles and the persistence of centromeric cohesion prevented sister chromatids from separating at meiosis I, which contributed to the onset of this haploid-dependent UMCD. In addition, we found that sister centromeres always co-oriented in the paired chromosomes, whereas sister centromeres in unpaired chromosomes either bi-oriented or co-oriented in LDN haploid. Thus, chromosome pairing was probably another factor involved in the coordination of centromeres orientation in meiosis.

Technical Abstract: Meiosis includes one round of DNA replication and two successive nuclear divisions, i.e. meiosis I (reductional) and meiosis II (equational). This specialized cell division reduces chromosomes in half and generates haploid gametes in sexual reproduction of eukaryotes. It ensures faithful transmission of genetic materials over sexual generations through fertilization and generates genetic variability through chromosome recombination and segregation. Unreductional meiotic cell division (UMCD), also known as meiotic restitution, is a variant meiotic cell division that gives rise to unreduced gametes due to the failure of chromosome segregation and leads to the formation of polyploidy. It has been considered a significant driving force behind polyploidization in nature. The mechanisms underlying UMCD, however, are still largely obscure. Because kinetochore orientation steers chromosome segregation in cell division, we attempted to elucidate the mechanisms of UMCD by investigating kinetochore orientation in UMCD and regular cell division. Here we found that sister kinetochores co-oriented at meiosis I under disomic condition in the tetraploid wheat ‘Langdon’ (LDN), but bi-oriented under haploid condition even though co-oriented chromosomes were also observed. It was also found that chromosomal cohesion persisted in the centromeric region until anaphase II in both disomic and haploid LDN. Meiocytes with all chromosomes bi-oriented underwent UMCD and generated unreduced gametes under haploid condition in LDN. Thereby, we concluded that the tension created by bi-orientation of sister kinetochores prevented chromosomes from migrating toward either of poles and the persistence of centromeric cohesion prevented sister chromatids from separating at meiosis I, which contributed to the onset of this haploid-dependent UMCD in LDN. Most likely the gene(s) responsible for kinetochore orientation at meiosis I was ploidy-regulated in the disomic and haploid LDN. In addition, we found that sister kinetochores always co-oriented in the synapsed chromosomes, whereas sister kinetochores in asynapsed chromosomes (univalents) either bi-oriented or co-oriented in LDN. Thus, synapsis was probably another factor involved in the coordination of kinetochore orientation in meiosis.

Last Modified: 10/22/2014
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