The maize B chromosome is capable of expressing microRNAs and altering the expression of microRNAs derived from A chromosomes

  • Yen-Hua Huang
  • Shu-Fen Peng
  • Yao-Pin Lin
  • Ya-Ming ChengEmail author
Original Article


Supernumerary B chromosomes (Bs) are nonessential chromosomes that are considered genetically inert. However, the maize B carries control elements that direct its behavior, such as that of nondisjunction, during the second pollen mitosis, and affects normal A chromosomes during cell division. Recently, the maize B has been found to contain transcriptionally active sequences and to affect the transcription of genes on A chromosomes. To better understand the regulatory mechanisms underlying the maize B, we constructed two small RNA libraries from maize B73 inbred lines with and without Bs. The sequencing results revealed that 18 known microRNAs (miRNAs) were significantly differentially expressed in response to the presence of the B, and most target mRNAs were characterized as transcription factors. Moreover, three novel B-derived miRNAs were identified via stem-loop reverse transcriptase-polymerase chain reaction (RT-PCR)-based analysis, and all showed consistent B-specific expression in almost all analyzed inbred lines and in all tissue types, including leaves, roots, and pollen grains. By the use of B-10L translocations, the three B-derived miRNAs were mapped to specific B regions. The results from this study suggest that the maize B can express miRNAs and affect the expression of A-derived miRNAs, which could regulate the expression of A-located genes.


B chromosome microRNA small RNA sequencing maize B-10L translocation 



CCAAT-binding factor


Complementary DNA-amplified fragment length polymorphism


Centromeric knob




Distal euchromatin


Distal heterochromatin


Distal portion of proximal euchromatin


Heterochromatic small interfering RNA




No apical meristem


Natural antisense transcript small interfering RNA


National Center for Biotechnology Information


Proximal euchromatin

Phased siRNA

Phased small interfering RNA


Proximal portion of proximal euchromatin


RNA-induced silencing complex


Reverse transcriptase-polymerase chain reaction


Small RNA


Sequence read archive


Funding information

This work was supported by grants from the Ministry of Science and Technology of Taiwan (MOST 104-2311-B-005-012-MY3 and MOST 107-2311-B-005-003).

Supplementary material

10577_2019_9620_MOESM1_ESM.xlsx (13 kb)
ESM 1 (XLSX 13 kb)


  1. Ahmad SF, Martins C (2019) The modern view of B chromosomes under the impact of high scale omics analysis. Cells 8:156PubMedCentralCrossRefGoogle Scholar
  2. Alfenito MR, Birchler JA (1993) Molecular characterization of a maize B chromosome centric sequence. Genetics 135:589–597PubMedPubMedCentralGoogle Scholar
  3. Axtell MJ (2013) Classification and comparison of small RNAs from plants. Annu Rev Plant Biol 64:137–159PubMedCrossRefPubMedCentralGoogle Scholar
  4. Carlson WR (1973) A procedure for localizing genetic factors controlling mitotic nondisjunction in the B chromosome of maize. Chromosoma 42:127–136CrossRefGoogle Scholar
  5. Carlson WR (1986) The B chromosome of maize. CRC Crit Rev Plant Sci 3:201–226CrossRefGoogle Scholar
  6. Carlson WR, Roseman RR (1992) A new property of the maize B chromosome. Genetics 131:211–223PubMedPubMedCentralGoogle Scholar
  7. Carraro N, Peaucelle A, Laufs P, Yraas J (2006) Cell differentiation and organ initiation at shoot apical meristem. Plant Mol Biol 60:811–826PubMedCrossRefPubMedCentralGoogle Scholar
  8. Cheng YM, Lin BY (2003) Cloning and characterization of maize B chromosome sequences derived from microdissection. Genetics 164:299–310PubMedPubMedCentralGoogle Scholar
  9. Chiavarino AM, González-Sánchez M, Poggio L, Puertas MJ, Rosato M, Rosi P (2001) Is maize B chromosome preferential fertilization controlled by a single gene? Heredity 86:743–748PubMedCrossRefPubMedCentralGoogle Scholar
  10. Chiavarino AM, Rosato M, Rosi P, Poggio L, Naranjo CA (1998) Localization of the gene controlling B chromosome transmission rate in maize (Zea mays ssp. mays, Poaceae). Am J Bot 85:1851–1585CrossRefGoogle Scholar
  11. Chien YL, Lin CY, Lo KL, Cheng YM (2014) Development and mapping of CL-repeat display markers on the maize B chromosome. Cytogenetic Genome Research 144:227–236PubMedCrossRefPubMedCentralGoogle Scholar
  12. Friedländer MR, Mackowiak SD, Li N, Chen W, Rajewsky N (2012) miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Res 40:37–52PubMedCrossRefPubMedCentralGoogle Scholar
  13. Goiz JF (2006) Signaling between the shoot apical meristem and developing lateral organs. Plant Mol Biol 60:889–903CrossRefGoogle Scholar
  14. González-Sánchez M, González-González E, Molina F, Chiavarino AM, Rosato M, Puertas MJ (2003) One gene determines maize B chromosome accumulation by preferential fertilization; another gene(s) determines their meiotic loss. Heredity 90:122–129PubMedCrossRefPubMedCentralGoogle Scholar
  15. 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 16:88PubMedPubMedCentralCrossRefGoogle Scholar
  16. Jones RN, Viegas W, Houben A (2008) A century of B chromosomes in plants: So what? Ann Bot 101:767–775PubMedCrossRefPubMedCentralGoogle Scholar
  17. Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53PubMedCrossRefPubMedCentralGoogle Scholar
  18. 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 Gen Genomics 290:431–441CrossRefGoogle Scholar
  19. Kidner CA, Martienssen RA (2004) Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428:81–84PubMedCrossRefGoogle Scholar
  20. Kuwada Y (1915) Ueber die Chromosomenzahl von Zea mays L. Bot Mag Tokoyo 29:83–89CrossRefGoogle Scholar
  21. Lamb JC, Kato A, Birchler JA (2005) Sequences associated with A chromosome centromeres are present throughout the maize B chromosome. Chromosoma 113:337–349PubMedCrossRefPubMedCentralGoogle Scholar
  22. Lamb JC, Riddle NC, Cheng YM, Theuri J, Birchler JA (2007) Localization and transcription of a retrotransposon-derived element on the maize B chromosome. Chromosom Res 15:383–398CrossRefGoogle Scholar
  23. Li AL, Mao L (2007) Evolution of plant microRNA gene families. Cell Res 17:212–218PubMedCrossRefPubMedCentralGoogle Scholar
  24. Lin BY (1977) A squash technique for studying the cytology of maize endosperm and other tissues. Stain Technol 52:197–201PubMedCrossRefPubMedCentralGoogle Scholar
  25. Lin BY (1978) Regional control of nondisjunction of the B-chromosome in maize. Genetics 90:613–627PubMedPubMedCentralGoogle Scholar
  26. Lin BY (1979) Two new B-10L translocations involved in the control of nondisjunction of the B chromosome in maize. Genetics 92:931–945PubMedPubMedCentralGoogle Scholar
  27. Lin HZ, Lin WD, Lin CY, Peng SF, Cheng YM (2014) Characterization of maize B-chromosome-related transcripts isolated via cDNA-AFLP. Chromosoma 123:597–607PubMedCrossRefPubMedCentralGoogle Scholar
  28. Lippman Z, Martienssen R (2004) The role of RNA interference in heterochromatic silencing. Nature 431:364–370PubMedCrossRefPubMedCentralGoogle Scholar
  29. Lisch D (2013) How important are transposons for plant evolution? Nat Rev Genet 14:49–61PubMedCrossRefPubMedCentralGoogle Scholar
  30. Liu Q, Chen YQ (2009) Insight into the mechanism of plant development: interactions of miRNA pathway with phytohormone response. Biochem Biophys Res Commun 384:1–5PubMedCrossRefPubMedCentralGoogle Scholar
  31. 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 27:350–354CrossRefGoogle Scholar
  32. Longley AE (1927) Supernumerary chromosomes in Zea mays. J Agric Res 35:769–784Google Scholar
  33. Lu C, Tei SS, Luo S, Haudenschild CD, Meyers BC, Green PJ (2005) Elucidation of the small RNA component of the transcriptome. Science 309:1567–1569PubMedCrossRefPubMedCentralGoogle Scholar
  34. Mallory AC, Vaucheret H (2006) Functions of microRNAs and related small RNAs in plants. Nat Genet 38:S31–S36PubMedCrossRefPubMedCentralGoogle Scholar
  35. Mallory AC, Dugas DV, Bartel DP, Bartel B (2004) MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Curr Biol 14:1035–1046PubMedCrossRefPubMedCentralGoogle Scholar
  36. Marques A, Klemme S, Houben A (2018) Evolution of plant B chromosome enriched sequences. Genes 9:515PubMedCentralCrossRefGoogle Scholar
  37. Nag A, Jack Y (2010) Sculpting the flower; the role of miRNAs in flower development. Curr Top Dev Biol 91:349–378PubMedCrossRefPubMedCentralGoogle Scholar
  38. Peng SF, Lin YP, Lin BY (2005) Characterization of AFLP sequences from regions of maize B chromosome defined by 12 B-10L translocations. Genetics 169:375–388PubMedPubMedCentralCrossRefGoogle Scholar
  39. Randolph LF (1941) Genetic characteristics of the B chromosomes in maize. Genetics 26:608–631PubMedPubMedCentralGoogle Scholar
  40. Rhoades MM (1968) Studies on the cytological basis of crossing over. In: Peacock WJ, Brock RD (eds) Replication and recombination of genetic material. Australian Acad Sci, Canberra, pp229–241.Google Scholar
  41. Rhoades MM, Dempsey E (1972) On the mechanism of chromatin loss induced by the B chromosome of maize. Genetics 71:73–96PubMedPubMedCentralGoogle Scholar
  42. Roman H (1947) Mitotic nondisjunction in the case of interchanges involving the B-type chromosome in maize. Genetics 32:391–409PubMedPubMedCentralGoogle Scholar
  43. Roman H (1948) Directed fertilization in maize. Proc Natl Acad Sci U S A34:36–42PubMedPubMedCentralCrossRefGoogle Scholar
  44. Stark EA, Connerton I, Bennett ST, Barnes SR, Parker JS, Forster JW (1996) Molecular analysis of the structure of the maize B-chromosome. Chromosom Res 4:15–23CrossRefGoogle Scholar
  45. Staub RW (1987) Leaf striping correlated with the presence of B chromosomes in maize. J Hered 78:71–74CrossRefGoogle Scholar
  46. Varkonyi-Gasic E, Wu R, Wood M, Walton EF, Hellens RP (2007) Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods 3:12PubMedPubMedCentralCrossRefGoogle Scholar
  47. Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Cen XY (2005) Control of root cap formation by MicroRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17:2204–2216PubMedPubMedCentralCrossRefGoogle Scholar
  48. Ward E (1973) Nondisjunction: localization of the controlling site in the maize B chromosome. Genetics 73:387–391PubMedPubMedCentralGoogle Scholar
  49. Zhang L, Chia JM, Kumari S, Stein JC, Liu Z, Narechania A, Maher CA, Guill K, McMullen MD, Ware D (2009) A genome-wide characterization of microRNA genes in maize. PLoS Genet 5:e1000716PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of AgronomyNational Chung Hsing UniversityTaichungTaiwan
  2. 2.Department of Medical ResearchChina Medical University HospitalTaichungTaiwan
  3. 3.Agricultural Biotechnology Research CenterAcademia SinicaTaipeiTaiwan

Personalised recommendations