Abstract
B chromosomes are dispensable elements that occur in many species, including maize. The maize B chromosome is acrocentric and highly heterochromatic and undergoes nondisjunction during the second pollen mitosis. In this study, we determined the genetic behavior and organization of two naturally occurring B chromosome variants (designated Bta and Btb). The morphology and genetic behavior of the Bta chromosome were similar to those of the typical B chromosome, but the Bta chromosome contained a deletion in the first heterochromatin region and had higher transmission frequencies through both male and female parents. The Btb chromosome was reduced in size, consisted primarily of heterochromatin, and had a lower transmission frequency. The Btb chromosome lacked nondisjunctional behavior, which was restored by the presence of normal B chromosomes in the cell. Furthermore, the Btb chromosome contained two centromeric regions, only one of which was active. The organization of these two naturally occurring B chromosome variants was also determined using fluorescence in situ hybridization with B-associated sequences and by amplification of B-specific molecular markers to create possible evolutionary models.
Similar content being viewed by others
Abbreviations
- BFB:
-
Breakage-fusion-bridge
- CK:
-
Centromeric knob
- DE:
-
Distal euchromatin
- DH:
-
Distal heterochromatin
- FISH:
-
Fluorescence in situ hybridization
- PE:
-
Proximal euchromatin
- SCAR:
-
Sequence-characterized amplified region
References
Alfenito 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
Bakkali M, Cabrero J, Lopez-Leon MD, Perfectti F, Camacho JP (1999) The B chromosome polymorphism of the grasshopper Eyprepocnemis plorans in North Africa. I. B variants and frequency. Heredity 83:428–434
Birchler JA, Han F (2013) Meiotic behavior of small chromosomes in maize. Front Plant Sci 4:505
Camacho JPM (2005) B chromosome. In: Gregory TR (ed) The evolution of the genome. Elsevier, San Diego, pp 223–286
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
Chien YL, Lin CY, Lo KL, Cheng YM (2014) Development and mapping of CL-repeat display markers on the maize B chromosome. Cytogenet Genome Res 144:227–236
Chilton MD, McCarthy BJ (1973) DNA from maize with and without B chromosomes: a comparative study. Genetics 74:605–614
Dhar MK, Friebe B, Koul AK, Gill BS (2002) Origin of an apparent B chromosome by mutation, chromosome fragmentation and specific DNA sequence amplification. Chromosoma 111:332–340
Graham ND, Cody JP, Swyers NC, McCaw ME, Zhao C, Birchler JA (2015) Engineered minichromosomes in plants: structure, function, and applications. Int Rev Cell Mol Biol 318:63–119
Han F, Lamb JC, Birchler JA (2006) High frequency of centromere inactivation resulting in stable dicentric chromosomes of maize. Proc Natl Acad Sci USA 103:3238–3243
Han F, Gao Z, Yu W, Birchler JA (2007) Minichromosome analysis of chromosome pairing, disjunction, and sister chromatid cohesion in maize. Plant Cell 19:3853–3863
Houben A, Thompson N, Ahne R, Leach CR, Verlin D, Timmis JN (1999) A monophyletic origin of the B chromosomes of Brachycome dichromosomatica (Asteraceae). Plant Syst Evol 219:127–135
Houben A, Mette MF, Teo CH, Lermontova I, Schubert I (2013) Engineered plant minichromosomes. Int J Dev Biol 57:651–657
Houben A, Banaei-Moghaddam AM, Klemme S, Timmis JN (2014) Evolution and biology of supernumerary B chromosomes. Cell Mol Life Sci 71:467–478
Jin W, Melo JR, Nagaki K et al (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 chromosome centromere. Plant Cell 17:1412–1423
Johnson SS, Phillips RL, Rines HW (1987) Possible role of heterochromatin in chromosome breakage induced by tissue culture in oats (Avena sativa L.). Genome 29:439–446
Jones RN (1995) B chromosomes in plants. New Phytol 131:411–434
Jones N, Houben A (2003) B chromosomes in plants: escapees from the A chromosome genome? Trends Plant Sci 8:417–423
Jones RN, Rees H (1982) B chromosomes. Academic, London
Jones RN, Viegas W, Houben A (2008) A century of B chromosomes in plants: so what? Ann Bot 101:767–775
Kao KW, Lin CY, Peng SF, Cheng YM (2015) Characterization of four B-chromosome-specific RAPDs and the development of SCAR markers on the maize B-chromosome. Mol Genet Genomics 290:431–441
Kaszás E, Birchler JA (1996) Misdivision analysis of centromere structure in maize. EMBO J 15:5246–5255
Kato A, Zheng YZ, Auger DL et al (2005) Minichromosomes derived from the B chromosome of maize. Cytogenet Genome Res 109:156–165
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
Lapitan NL, Sears RG, Gill BS (1984) Translocations and other karyotypic structural changes in wheat x rye hybrids regenerated from tissue culture. Theor Appl Genet 68:547–554
Lima-De-Faria A (1962) Genetic interaction in rye expressed at the chromosome phenotype. Genetics 47:1455–1462
Lin BY (1977) A squash technique for studying the cytology of maize endosperm and other tissues. Stain Technol 52:197–201
Lin BY (1978) Regional control of nondisjunction of the B chromosome in maize. Genetics 90:613–627
Lin BY, Chou HP (1997) Physical mapping of four RAPDs in the B chromosome of maize. Theor Appl Genet 94:534–538
Lin HZ, Lin WD, Lin CY, Peng SF, Cheng YM (2014) Characterization of maize B-chromosome-related transcripts isolated via cDNA-AFLP. Chromosoma 123:597–607
Liu Y, Su H, Pang J et al (2015) Sequential de novo centromere formation and inactivation on a chromosomal fragment in maize. Proc Natl Acad Sci USA 112:E1263–E1271
Lo KL, Lin YP, Chen LJ, Lin BY (2009) Isolation and characterization of new maize B sequences from a microdissected library. Plant Mol Biol Report 27:350–354
Longley AE (1927) Supernumerary chromosomes in Zea mays. J Agric Res 35:769–784
Longley AE (1956) The origin of diminutive B-type chromosomes in maize. Am J Bot 43:18–22
Marques A, Klemme S, Guerra M, Houben A (2012) Cytomolecular characterization of de novo formed rye B chromosome variants. Mol Cytogenet 5:34
Masonbrink RE, Fu S, Han F, Birchler JA (2013) Heritable loss of replication control of a minichromosome derived from the B chromosome of maize. Genetics 193:77–84
McClintock B (1933) The association of non-homologous parts of chromosomes in the mid-prophase of meiosis in Zea mays. Z Zellforsch Mikrosk Anat 19:191–237
McClintock B (1939) The behavior in successive nuclear divisions of a chromosome broken at meiosis. Proc Natl Acad Sci USA 25:405–416
McClintock B (1941) The stability of broken ends of chromosomes in Zea mays. Genetics 26:234–282
Mroczek RJ, Dawe RK (2003) Distribution of retroelements in centromeres and neocentromeres of maize. Genetics 165:809–819
Parker JS, Lozano R, Taylor S, Rejón MR (1991) Chromosomal structure of populations of Scilla autumnalis in the Iberian Peninsula. Heredity 67:287–297
Peng SF, Cheng YM (2011) Characterization of satellite CentC repeats from heterochromatic regions on the long arm of maize B-chromosome. Chromosome Res 19:183–191
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
Randolph LF (1941) Genetic characteristics of the B chromosome in maize. Genetics 26:608–631
Roman H (1947) Mitotic nondisjunction in the case of interchanges involving the B-type chromosome in maize. Genetics 32:391–490
Roman H (1948) Directed fertilization in maize. Proc Natl Acad Sci USA 34:36–42
Stark EA, Connerton I, Bennett ST, Barnes SR, Parker JS, Forster JW (1996) Molecular analysis of the structure of the maize B-chromosome. Chromosome Res 4:15–23
Wang CJ, Chen CC (2003) Localization of centromere and telomere sequences on maize pachytene chromosomes by fluorescence in situ hybridization. BioFormosa 38:17–25
Ward EJ (1973) Nondisjunction: localization of the controlling site in the maize B chromosome. Genetics 73:387–391
Wilson EB (1907) The supernumerary chromosomes of Hemiptera. Science 26:870–871
Yu W, Han F, Gao Z, Vega JM, Birchler JA (2007) Construction and behavior of engineered minichromosomes in maize. Proc Natl Acad Sci USA 104:8924–8929
Zheng YZ, Roseman RR, Carlson WR (1999) Time course study of the chromosome-type breakage-fusion-bridge cycle in maize. Genetics 153:1435–1444
Acknowledgments
This study was supported by grants from the National Science Council grant of Taiwan (NSC 102-2311-B-005-001) and the Ministry of Science and Technology of Taiwan (MOST 104-2311-B-005-012-MY3).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Jiming Jiang.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplemental Fig. S1
Mitotic behavior of B chromosome variants. Cells in mitotic metaphase (a, d, g), anaphase (b, e, h), and telophase (c, f, i) carrying one copy of the B (a-c), Bta (d-f), or Btb (g-i) chromosome were hybridized with the CentC (green) and the B-repeat (red) probes. Chromosomes were stained with DAPI (blue). White arrows indicate the B chromosome or B variants. Scale bars all equal to 10 μm (GIF 95 kb)
Supplemental Fig. S2
Locations of six B-specific molecular markers on the B chromosome. The figure was modified from Kao et al. (2015) and shows where four B-specific SCAR markers (SCAR313, SCAR345, SCAR349 and SCAR426) were mapped using the breakpoints of 15 B-A translocations (Arrows). The locations of the CL-repeat and Stark markers were indicated based on the results of Cheng (2010) and Lamb et al. (2007), respectively. Black lines indicate the mapped positions of the six B-specific markers. Dotted lines represent regions in which the presence of the markers cannot be verified. S, short arm; CK, centromeric knob; PE, proximal euchromatin; DH1-DH4, four blocks of distal heterochromatin; DE, distal euchromatin (GIF 24 kb)
Supplemental Fig. S3
Amplification of six B-specific molecular markers from B chromosome variants. Genomic DNA from L289 plants lacking the B chromosome (0B) and containing one B (1B), Bta, or Btb chromosome was amplified using primers for the B-specific markers CL-repeat, Stark, SCAR426, SCAR313, SCAR345 and SCAR349. Quality and an equal quantity of the genomic DNA of different genotypes were conducted by amplification using a maize Actin primer pair. M molecular weight marker (molecular weights are shown at the left) (GIF 188 kb)
Supplemental Table 1
(DOCX 56 kb)
Supplemental Table 2
(DOCX 56 kb)
Supplemental Table 3
(DOCX 54 kb)
Rights and permissions
About this article
Cite this article
Cheng, YM., Feng, YR., Lin, YP. et al. Cytomolecular characterization and origin of de novo formed maize B chromosome variants. Chromosome Res 24, 183–195 (2016). https://doi.org/10.1007/s10577-015-9516-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10577-015-9516-2