Abstract
Supernumerary B chromosomes are dispensable parts of the nuclear genome and occur in all eukaryotic groups. They differ from the normal A chromosomes in morphology, genetic behavior, and inheritance. Because they are nonessential for individual development, B chromosomes are considered to be genetically inert and to lack functional genes. However, the maize B chromosome carries control elements that direct its behavior and affects A chromosomes during cell division. Therefore, the maize B chromosome might contain genic regions that differ from the genic regions of A chromosomes. Yet, only a few B-specific transcript sequences have been isolated. To identify more B-specific transcriptionally active sequences, we constructed de novo transcriptome assemblies for maize B73 inbred lines with 0B (+0B) and 2B (+2B). Comparative analysis of the B73 + 0B and B73 + 2B assemblies revealed that unigenes annotated to 201 gene ontology terms were differentially expressed. Using RT-PCR analysis of novel transcript sequences specific to B73 + 2B, we identified 32 novel B-related transcript sequences, and most sequences showed consistent B-specific transcription in different inbred lines. Moreover, 20 of those novel B-related transcript sequences were further confirmed to be located only on the B chromosome by genomic PCR analysis. A total of 19 novel B-specific transcript sequences were mapped to various positions along the B chromosome using B-10L translocations. Taken together, our results suggest that the maize B chromosome indeed affects the expression of A-located genes and that a substantial amount of novel B-specific transcriptionally active sequences are present throughout the maize B chromosome. Therefore, the maize B chromosome seems not to be genetically inert.
Similar content being viewed by others
Data availability
We deposited the B73 + 0B and B73 + 2B RNA-Seq libraries in the Sequence Read Archive (SRA) database under accession PRJNA482010.
Abbreviations
- cDNA-AFLP:
-
Complementary DNA-amplified fragment length polymorphism
- CK:
-
Centromeric knob
- DE:
-
Distal euchromatin
- DH:
-
Distal heterochromatin
- DPE:
-
Distal portion of proximal euchromatin
- FISH:
-
Fluorescence in situ hybridization
- FPKM:
-
Fragments per kilobase of transcript per million mapped reads
- GO:
-
Gene ontology
- InDel:
-
Insertion/deletion
- NCBI:
-
National Center for Biotechnology Information
- PAGE:
-
Parametric analysis of gene set enrichment
- PE:
-
Proximal euchromatin
- PPE:
-
Proximal portion of proximal euchromatin
- RAPD:
-
Random amplified polymorphic DNA
- RNA-Seq:
-
RNA-sequencing
- RT-PCR:
-
Reverse transcriptase-polymerase chain reaction
- SNP:
-
Single nucleotide polymorphism
References
Ahmad SF, Martins C (2019) The modern view of B chromosomes under the impact of high scale omics analysis. Cells 8:156
Alfentio MR, Birchler JA (1993) Molecular characterization of a maize B chromosome centric sequence. Genetics 135:589–597
Banaei-Moghaddam AM, Meier K, Karimi-Ashtiyani R, Houben A (2013) Formation and expression of pseudogenes on the B chromosome of rye. Plant Cell 25:2536–2544
Benetta ED, Akbari OS, Ferree PM (2019) Sequence expression of supernumerary B chromosomes: function or fluff? Genes 10:123
Beukeboom LW (1994) Bewildering Bs: an impression of the 1st B-chromosome conference. Heredity 73:328–336
Carlson WR (1986) The B chromosome of maize. CRC Crit Rev Plant Sci 3:201–226
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, Feng YR, Lin YP, Peng SF (2016) Cytomolecular characterization and origin of de novo formed maize B chromosome variants. Chromosome Res 24:183–195
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
Coleman JJ, Rounsley SD, Rodriguez-Carres M, Kuo A, Wasmann CC, Grimwood J, Schmutz J, Taga M, White GJ, Zhou S, Schwartz DC, Freitag M, Ma LJ, Danchin EG, Henrissat B, Coutinho PM, Nelson DR, Straney D, Napoli CA, Barker BM, Gribskov M, Rep M, Kroken S, Molnár I, Rensing C, Kennell JC, Zamora J, Farman ML, Selker EU, Salamov A, Shapiro H, Pangilinan J, Lindquist E, Lamers C, Grigoriev IV, Geiser DM, Covert SF, Temporini E, Vanetten HD (2009) The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genet 5:e1000618
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
Donald TM, Leach CR, Clough A, Timmis JN (1995) Ribosomal RNA genes and the B chromosome of Brachycome dichromosomatica. Heredity 74:556–561
Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:64–70
Houben A, Banaei-Moghaddam AM, Klemme S, Timmis JN (2014) Evolution and biology of supernumerary B chromosomes. Cell Mol Life Sci 71:467–478
Huang W, Du Y, Zhao X, Jin W (2016) B chromosome contains active genes and impacts the transcription of A chromosomes in maize (Zea mays L.). BMC Plant Biol 16:88
Jiang J, Gill BS, Wang GL, Ronald PC, Ward DC (1995) Metaphase and interphase fluorescence in situ hybridization mapping of the rice genome with bacterial artificial chromosomes. Proc Natl Acad Sci USA 92:4487–4491
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 development of SCAR markers on the maize B-chromosome. Mol Genet Genom 290:431–441
Kohany O, Gentles AJ, Hankus L, Jurka J (2006) Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinform 7:474
Kuwada Y (1915) Ueber die Chromosomenzahl von Zea mays L. Bot Mag Tokoyo 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
Leach CR, Houben A, Field B, Pistrick K, Demidov D, Timmis JN (2005) Molecular evidence for transcription of genes on a B chromosome in Crepis capillaries. Genetics 171:269–278
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 (1979) Two new B-10L translocations involved in the control of nondisjunction of the B chromosome in maize. Genetics 92:931–945
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
Longley AE (1927) Supernumerary chromosomes in Zea mays. J Agric Res 35:769–784
Ma W, Gabriel TS, Martis MM, Gursinsky T, Schubert V, Vrána J, Doležel J, Grundlach H, Altschmied L, Scholz U, Himmelbach A, Behrens SE, Banaei-Moghaddam AM, Houben A (2017) Rye B chromosomes encode a functional Argonaute-like protein with in vitro slicer activities similar to its A chromosome paralog. New Phytol 213:916–928
Marques A, Klemme S, Houben A (2018) Evolution of plant B chromosome enriched sequences. Genes 9:515
Martis MM, Klemme S, Banaei-Moghaddam AM, Blattner FR, Macas J, Schmutzer T, Scholz U, Gundlach H, Wicker T, Šimková H, Novák P, Neumann P, Kubaláková M, Bauer E, Haseneyer G, Fuchs J, Doležel J, Stein N, Mayer KF, Houben A (2012) Selfish supernumerary chromosome reveals its origin as a mosaic of host genome and organellar sequences. Proc Natl Acad Sci USA 109:13343–13346
Navarro-Dominguez B, Martin-Pecina M, Ruiz-Ruano FJ, Cabrero J, Corral JM, López-León MD, Sharbel TF, Camacho JPM (2019) Gene expression changes elicited by a parasitic B chromosome in the grasshopper Eyprepocnemis plorans are consistent with its phenotypic effects. Chromosoma 128:53–67
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 chromosomes in maize. Genetics 26:608–631
Rhoades MM (1968) Studies on the cytological basis of crossing over. In: Peacock WJ, Brock RD (eds) Replication and recombination of genetic material. Australian Academy of Science, Canberra, pp 229–241
Rhoades MM, Dempsey E (1972) On the mechanism of chromatin loss induced by the B chromosome of maize. Genetics 71:73–96
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
Roy SW, Peny D (2006) Patterns of intron loss and gain in plants: intron loss-dominated evolution and genome-wide comparison of O. sativa and A. thaliana. Mol Biol Evol 24:171–181
Smeds L, Künster A (2011) ConDetri—a content dependent read trimmer for illumina data. PLoS One 6:e26314
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
Staub RW (1987) Leaf striping correlated with the presence of B chromosomes in maize. J Hered 78:71–74
Supek F, Bošnjak M, Škunca N, Šmuc T (2011) REVIGO summaries and visualizes long lists of gene ontology terms. PLoS One 6:e21800
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2014) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515
Valente GT, Conte MA, Fantinatti BE, Cabral-de-Mello DC, Carvalho RF, Vicari MR, Kocher TD, Martins C (2014) Origin and evolution of B chromosomes in the Cichlid fish Astatotilapia latifasciata based on integrated genomic analyses. Mol Biol Evol 31:2061–2072
Wang H, Devos KM, Bennetzen JL (2014) Recurrent loss of specific introns during Angiosperm evolution. PLoS Genet 10:e1004843
Ward E (1973) Nondisjunction: localization of the controlling site in the maize B chromosome. Genetics 73:387–391
Wilson EB (1907) The supernumerary chromosome of Hemiptera. Science 26:870–871
Yoshida K, Terai Y, Mizoiri S, Aibara M, Nishihara H, Watanabe M, Kuroiwa A, Hirai H, Hirai Y, Matsuda Y, Okada N (2011) B chromosomes have a functional effect on female sex determination in Lake Victoria cichlid fishes. PLoS Genet 7:e1002203
Acknowledgements
We are thankful to the reviewers for the very helpful suggestions and corrections for improving the paper.
Funding
This study was funded by the Ministry of Science and Technology of Taiwan (Grant numbers: MOST 104-2311-B-005-012-MY3 and MOST 107-2311-B-005-003).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All the authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Communicated by Stefan Hohmann.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Hong, ZJ., Xiao, JX., Peng, SF. et al. Novel B-chromosome-specific transcriptionally active sequences are present throughout the maize B chromosome. Mol Genet Genomics 295, 313–325 (2020). https://doi.org/10.1007/s00438-019-01623-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-019-01623-2