Abstract
The B-chromosome of maize contains an A-chromosome centromere-specific satellite CentC repeat in its centromere region (CENB) and at multiple locations in its distal heterochromatic regions (BDHs). Because CentC is highly repetitive, it is a challenge to study CentC sequences within individual centromeres or chromosome regions. The combined structure of CentC and a BDH-specific CL-repeat has allowed us to isolate CentC sequences from BDHs. In the study described herein, we have used a PCR method to amplify 13 CL-CentC variant products that were specifically mapped to A-centromeres (CENAs), the CENB, and BDHs via the tertiary trisomes and hypoploids of five B-10L translocations. Cloning and sequence analyses of these CL-CentC products have revealed a local CentC homogenization within the three CentC-containing regions. Phylogenetic analysis has indicated that the CentC sequences of BDHs are more closely related to those of CENAs in comparison to that of the CENB. Furthermore, the CentC monomers that are within the CENB are more diverse than those within BDHs and CENAs. These results shed light on the evolution of CentC repeats on the B-chromosome and provide a better understanding of B-chromosome evolution.
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Abbreviations
- CENB:
-
B-chromosome centromere
- CENAs:
-
A-chromosome centromeres
- BDHs:
-
Distal heterochromatic regions of the B-chromosome
- BS:
-
B short arm
- CK:
-
Centromeric knob
- PE:
-
Proximal euchromatic region
- DH:
-
Distal heterochromatic region
- DE:
-
Distal euchromatic tip
- FISH:
-
Fluorescence in situ hybridization
- TT:
-
Tertiary trisome
- HO:
-
Hypoploid
References
Alfentio MR, Birchler JA (1993) Molecular characterization of a maize B chromosome centric sequence. Genetics 135:589–597
Ananiev EV, Phillips RL, Rines HW (1998) Chromosome-specific molecular organization of maize (Zea mays L.) centromeric regions. Proc Natl Acad Sci USA 95:13073–13078
Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580
Carlson WR (1969) Factors affecting preferential fertilization in maize. Genetics 62:543–554
Cheng YM (2010) Evolution of the heterochromatic regions on maize B long arm based on the sequence structure of CL-repeat variants. Chromosome Res 18:605–619
Cheng YM, Lin BY (2003) Cloning and characterization of maize B chromosome sequences derived from microdissection. Genetics 164:299–310
Cheng YM, Lin BY (2004) Molecular organization of large fragments of maize B chromosome: indication of a novel repeat. Genetics 166:1947–1961
Chilton MD, McCarthy BJ (1973) DNA from maize with and without B chromosomes: a comparative study. Genetics 74:605–614
Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190
Hall SE, Luo S, Hall AE, Preuss D (2005) Differential rates of local and global homogenization in centromere satellites from Arabidopsis relatives. Genetics 170:1913–1927
Jin W, Melo JR, Nagali K, Talbert PB, Henikoff S, Dawe RK, Jiang J (2004) Maize centromeres: organization and functional adaptation in the genetic background of oat. Plant Cell 16:571–581
Jin W, Lamb JC, Vega JM, Dawe RK, Birchler JA, Jiang J (2005) Molecular and functional dissection of the maize B centromere. Plant Cell 17:1412–1423
Jones RN, Viegas W, Houben A (2008) A century of B chromosomes in plants: so what? Ann Bot 101:767–775
Kuwada Y (1915) Ueber die Chromosomenzahl von Zea mays L. Bot Mag Tokyo 29:83–89
Lamb JC, Kato A, Birchler JA (2005) Sequences associated with A chromosome centromeres are present throughout the maize B chromosome. Chromosoma 113:337–349
Lamb JC, Riddle NC, Cheng YM, Theuri J, Birchler JA (2007) Localization and transcription of a retrotransposon-derived element on the maize B chromosome. Chromosome Res 15:383–398
Lee HR, Neumann P, Macas J, Jiang J (2006) Transcription and evolutionary dynamics of the centromeric satellite repeat CentO in rice. Mol Biol Evol 23:2505–2520
Lin BY (1972) Synthesis of a set of B-A translocations involving a given segment of chromosome 10. Maize Genet Coop News Lett 46:193–194
Lin BY (1974) TB-10 breakpoints and marker genes on the long arm of chromosome 10. Maize Genet Coop News Lett 48:182–184
Lin BY (1978) Regional control of nondisjunction of the B-chromosome in maize. Genetics 90:613–627
Lo KL, Lin YP, Chen LJ, Lin BY (2009) Isolation and characterization of new maize B sequences from a microdissected library. Plant Mol Biol Rep 27:350–354
Longley AE (1927) Supernumerary chromosomes in Zea mays. J Agric Res 35:769–784
Malik HS, Henikoff S (2002) Conflict begets complexity: the evolution of centromeres. Curr Opin Genet Dev 12:711–718
Nagaki K, Song J, Stupar RM, Parokonny AS, Yuan Q, Ouyang S, Liu J, Hsiao J, Jones KM, Dawe RK, Buell CR, Jiang J (2003) Molecular and cytological analyses of large tracks of centromeric DNA reveal the structure and evolutionary dynamics of maize centromeres. Genetics 163:759–770
Page BT, Wanous MK, Birchler JA (2001) Characterization of a maize chromosome 4 centromeric sequence: evidence for an evolutionary relationship with the B chromosome centromere. Genetics 159:291–302
Peng SF, Lin YP, Lin BY (2005) Characterization of AFLP sequences from regions of maize B chromosome defined by 12 B-10L translocations. Genetics 169:375–388
Roman H (1947) Mitotic nondisjunction in the case of interchanges involving the B-type chromosome in maize. Genetics 32:391–409
Roman H (1948) Directed fertilization in maize. Proc Natl Acad Sci USA 34:36–42
Stark EA, Connerton I, Bennet ST, Barnes SR, Parker JS, Forster JW (1996) Molecular analysis of the structure of the maize B-chromosome. Chromosome Res 4:15–23
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Theuri J, Phelps-Durr T, Mathews S, Birchler JA (2005) A comparative study of retrotransposons in the centromeric regions of A and B chromosomes of maize. Cytogenet Genome Res 110:203–208
Zhong CX, Marshall JB, Topp C, Mroczek R, Kato A, Nagaki K, Birchler JA, Jiang JM, Dawe RK (2002) Centromeric retroelements and satellites interact with maize kinetochore protein CENH3. Plant Cell 14:2825–2836
Acknowledgment
This work was supported by the National Sciences Council grant of Taiwan (NSC99-2311-B-005-003-MY3).
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Supplementary Figure 1
Diagram of the pB51-15 sequences showing the PCR primers landing sites. The CL-repeat primer (CL-1) and CentC primer (BCentC-1) were designed from sequences of the B-clone (pB51-15, AY426743; Cheng and Lin 2004). Gray box CL-repeat monomer, red box CentC monomer, arrow primers binding site (GIF 12 kb)
Supplementary Figure 2
Sequence logo analysis of CentC monomers. Logos display the consensus sequences of complete CentC monomers from CC7TT, CC7HO, and CC0B clones (upper panel), and the selected nucleotides significantly different among CentC sequences of the three origins (lower panel) (GIF 471 kb)
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Peng, SF., Cheng, YM. Characterization of satellite CentC repeats from heterochromatic regions on the long arm of maize B-chromosome. Chromosome Res 19, 183–191 (2011). https://doi.org/10.1007/s10577-010-9183-2
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DOI: https://doi.org/10.1007/s10577-010-9183-2