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Homoeologous Shuffling and Chromosome Compensation

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Homoeologous Shuffling and Chromosome Compensation Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus Zhiyong Xiong, Robert T. Gaeta, and J. Chris Pires1 Division of Biological Sciences, University of Missouri, Columbia, MO 65211 Edited by Susan R. Wessler, University of Georgia, Athens, GA, and approved March 31, 2011 (received for review September 22, 2010) Polyploidy has contributed to the evolution of eukaryotes, partic- B. napus affords an excellent opportunity for conducting cy- ularly flowering plants. The genomic consequences of polyploidy togenetic investigations of evolution in a resynthesized allo- have been extensively studied, but the mechanisms for chromo- polyploid. Natural B. napus (AACC; 2n = 38) is thought to have some stability and diploidization in polyploids remain largely un- formed 5,000 to 10,000 y ago by the hybridization of ancestors of known. By using new cytogenetic tools to identify all of the Brassica rapa (AA; 2n = 20) and Brassica oleracea (CC; 2n = 18) homoeologous chromosomes, we conducted a cytological investi- (28, 29, 30). B. rapa and B. oleracea are also ancient polyploids, gation of 50 resynthesized Brassica napus allopolyploids across gen- and large-scale chromosome rearrangements occurred in the A erations S0:1 to S5:6 and in the S10:11 generation. Changes in copy and C genomes following divergence from a common ancestor number of individual chromosomes were detected in the S0:1 gen- (31). Several studies have demonstrated that genetic changes eration and increased in subsequent generations, despite the fact caused by homoeologous chromosome rearrangement are com- that the mean chromosome number among lines was approxi- mon in newly resynthesized B. napus allotetraploids (12, 14); mately 38. The chromosome complement of individual plants (seg- however, little is known about karyotype stability in resynthe- regants) ranged from 36 to 42, with a bias toward the accumulation sized lineages. This is in part because of difficulties in dis- of extra chromosomes. Karyotype analysis of the S10:11 generation tinguishing among the 38 small chromosomes of B. napus, and detected aneuploidy and inter- and intragenomic rearrangements, because of a lack of cytological markers. Mapping studies and chromosome breakage and fusion, rDNA changes, and loss of repeat BAC resources now permit rigorous evolutionary studies of sequences. Chromosome sets with extensive homoeology showed homoeologous chromosomes in B. napus. the greatest instability. Dosage balance requirements maintained In this study, we conducted a cytological investigation of 50 chromosome numbers at or near the tetraploid level, and the loss resynthesized B. napus allopolyploids across generations S0:1 to and gain of chromosomes frequently involved homoeologous chro- S5:6 and in the S10:11 generation. Previous studies of this pop- mosome replacement and compensation. These data indicate that ulation used mapped, genome-wide molecular markers and early generations of resynthesized B. napus involved aneuploidy detected genome-wide homoeologous chromosome rearrange- and gross chromosomal rearrangements, and that dosage balance ments and changes in homoeologous gene expression (14). As mechanisms enforced chromosome number stability. Seed yield and eight or more progenies of each line were pooled for analysis, pollen viability were inversely correlated with increasing aneu- these previous studies were only capable of detecting genetic ploidy, and the greatest fertility was observed in two lines that were changes that were fixed in each line. Furthermore, these studies additive for parental chromosomes. These data on resynthesized did not include a cytological characterization of individual plants B. napus and the correlation of fertility with additive karyotypes or their chromosome complement. By using a newly developed cast light on the origins and establishment of natural B. napus. cytogenetic method to distinguish all 38 chromosomes present in B. napus (32), we report evidence for homoeolog pairing and olyploidy (i.e., whole genomic duplication) has played a sig- chromosome rearrangements, aneuploidy, and homoeologous Pnificant role in the evolutionary history of all eukaryotes (1), chromosome compensation. and particularly in flowering plants (2). It is estimated that most flowering plants are polyploid, including most agricultural crops Results (3–7). Although all angiosperms have experienced at least one Karyotyping Resynthesized B. napus Using FISH with Repetitive DNA round of whole-genome duplication during their evolution, they Sequences and BAC Clones. Previously we performed a cytogenetic have undergone diploidization (8–10). The structural evolution of analysis of natural B. napus, B. rapa, and B. oleracea by using genomes in ancient polyploids included reductions in chromo- 45S, 5S, CentBr1, CentBr2, and BAC clones containing repetitive some number, chromosome fusions, and various types of chro- sequences (32) (Fig. S1). In this study, we made a standardized mosomal rearrangements (8, 11). Studies on newly resynthesized karyotype of resynthesized allopolyploids of B. napus capable of Brassica napus and recently formed polyploids of Tragopogon distinguishing all parental chromosomes. Two BACs from each suggest that genomic changes occur rapidly following allopoly- – of the 10 chromosomes of B. rapa were used to identify the ploidization in some plant species (12 14). Allopolyploidization homoeologous chromosomes in the A and C genomes (Fig. S1). can result in chromosomal rearrangements, DNA methylation Chromosomes C1 and C5 were similar, but distinguishable by changes, chromatin remodeling, changes in gene expression, and activation of transposable elements (13–22). Cytogenetic studies differences in centromere organization and the signal intensity using FISH have reported chromosomal changes, including of KBrB072L17. changes at ribosomal DNA loci, intergenomic translocations, an- euploidy, and loss of repeats (23–25). In Arabidopsis, synthetic allotetraploids are meiotically stable (26, 27), and the frequencies Author contributions: Z.X. and J.C.P. designed research; Z.X. performed research; Z.X. and of aneuploidy and chromosome abnormalities are relatively low R.T.G. analyzed data; and Z.X., R.T.G., and J.C.P. wrote the paper. (27). Many previous studies have lacked the chromosome-specific The authors declare no conflict of interest. markers necessary to identify all homoeologous chromosomes. This article is a PNAS Direct Submission. Little is known about the stability of homoeologous chromosomes 1To whom correspondence should be addressed. E-mail: [email protected]. and the mechanisms for chromosome change in large populations This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. of resynthesized allopolyploids. 1073/pnas.1014138108/-/DCSupplemental. 7908–7913 | PNAS | May 10, 2011 | vol. 108 | no. 19 www.pnas.org/cgi/doi/10.1073/pnas.1014138108 Downloaded by guest on September 26, 2021 Aneuploidy in Resynthesized B. napus. Thirty-eight chromosomes The C genome did not show a significant bias in the loss or gain are expected in resynthesized B. napus. This includes 13 pairs of of chromosomes (38 lost and 55 gained; P = 0.0971). chromosomes containing CentBr1 and six pairs of chromosomes with CentBr2 signals. However, the chromosome constitution of Chromosomal Dosage Balance Among S10:11 Resynthesized B. napus. segregants within every line was variable across generations In the S10:11 generation, no chromosome exceeded four copies, (range, 2n =36–42; Table 1 and Fig. S2). The frequency of extra or and the total number of chromosomes in each homoeologous set missing chromosomes (i.e., aneuploidy) among the five lineages (e.g., A1 + C1) was usually four. Lost chromosomes were often analyzed increased from 24.1% in the S0:1 to 71.4% in S5:6 gen- compensated by the gain of homoeologous chromosome, partic- eration. The mean chromosome number remained approximately ularly for homoeologous chromosome sets A1/C1 and A2/C2 38, and variation increased over successive generations (Table 1). (Table 2, Fig. 1, and Fig. S3). The gain of two extra chromosomes Among the 50 S5:6 lines analyzed, only one line (EL550) contained usually occurred with the loss of one or both homoeologous 38 chromosomes (26 CentBr1 and 12 CentBr2) in all segregants chromosomes. Thirty-one of 38 S10:11 lines (81.6%) were aneu- analyzed. The mean chromosome number among S5:6 lines was ploid for chromosomes within homoeologous sets A1/C1 or A2/ 38.37, which was significantly different from 38 (one-sample t test, C2, or in both homoeologous sets. Between 84.2% and 86.8% of P < 0.002); however, the distribution of chromosome numbers was these lines contained four chromosomes in homoeologous sets A1/ not normal, and was skewed toward the accumulation of more C1 and A2/C2, respectively, and thus demonstrated compensating chromosomes (Shapiro–Wilk test, W = 0.947; P < 0.05; Fig. S2; aneuploidy (total number of chromosome was four, but did not skewness of 0.64). Sixty-five percent of S10:11 plants were aneuploid contain two copies of each homoeolog). A few lines contained three based on centromere signals and total chromosome numbers or five total chromosomes in these homoeologous sets (Table 2). (Table 1). The average number of chromosomes per line was No line had more than five chromosomes in a homoeologous set, 38.58, which was significantly greater than 38 (one-sample t test, and one line (EL7400) had two A2 chromosomes and
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