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

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Abstract

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.

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Abbreviations

CBF:

CCAAT-binding factor

cDNA-AFLP:

Complementary DNA-amplified fragment length polymorphism

CK:

Centromeric knob

DCL:

Dicer-like

DE:

Distal euchromatin

DH:

Distal heterochromatin

DPE:

Distal portion of proximal euchromatin

hc-siRNA:

Heterochromatic small interfering RNA

miRNA:

MicroRNA

NAM:

No apical meristem

NAT-siRNA:

Natural antisense transcript small interfering RNA

NCBI:

National Center for Biotechnology Information

PE:

Proximal euchromatin

Phased siRNA:

Phased small interfering RNA

PPE:

Proximal portion of proximal euchromatin

RISC:

RNA-induced silencing complex

RT-PCR:

Reverse transcriptase-polymerase chain reaction

sRNA:

Small RNA

SRA:

Sequence read archive

References

  • Ahmad SF, Martins C (2019) The modern view of B chromosomes under the impact of high scale omics analysis. Cells 8:156

    CAS  PubMed Central  Google Scholar 

  • Alfenito MR, Birchler JA (1993) Molecular characterization of a maize B chromosome centric sequence. Genetics 135:589–597

    CAS  PubMed  PubMed Central  Google Scholar 

  • Axtell MJ (2013) Classification and comparison of small RNAs from plants. Annu Rev Plant Biol 64:137–159

    CAS  PubMed  Google Scholar 

  • Carlson WR (1973) A procedure for localizing genetic factors controlling mitotic nondisjunction in the B chromosome of maize. Chromosoma 42:127–136

    Google Scholar 

  • Carlson WR (1986) The B chromosome of maize. CRC Crit Rev Plant Sci 3:201–226

    Google Scholar 

  • Carlson WR, Roseman RR (1992) A new property of the maize B chromosome. Genetics 131:211–223

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carraro N, Peaucelle A, Laufs P, Yraas J (2006) Cell differentiation and organ initiation at shoot apical meristem. Plant Mol Biol 60:811–826

    CAS  PubMed  Google Scholar 

  • Cheng YM, Lin BY (2003) Cloning and characterization of maize B chromosome sequences derived from microdissection. Genetics 164:299–310

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 86:743–748

    CAS  PubMed  Google Scholar 

  • 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 85:1851–1585

    Google Scholar 

  • 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 144:227–236

    CAS  PubMed  Google Scholar 

  • 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 40:37–52

    PubMed  Google Scholar 

  • Goiz JF (2006) Signaling between the shoot apical meristem and developing lateral organs. Plant Mol Biol 60:889–903

    Google Scholar 

  • 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 90:122–129

    PubMed  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • Jones RN, Viegas W, Houben A (2008) A century of B chromosomes in plants: So what? Ann Bot 101:767–775

    PubMed  Google Scholar 

  • Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    CAS  PubMed  Google Scholar 

  • 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 290:431–441

    CAS  Google Scholar 

  • Kidner CA, Martienssen RA (2004) Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428:81–84

    CAS  PubMed  Google Scholar 

  • Kuwada Y (1915) Ueber die Chromosomenzahl von Zea mays L. Bot Mag Tokoyo 29:83–89

    Google Scholar 

  • Lamb JC, Kato A, Birchler JA (2005) Sequences associated with A chromosome centromeres are present throughout the maize B chromosome. Chromosoma 113:337–349

    CAS  PubMed  Google Scholar 

  • 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 15:383–398

    CAS  Google Scholar 

  • Li AL, Mao L (2007) Evolution of plant microRNA gene families. Cell Res 17:212–218

    CAS  PubMed  Google Scholar 

  • Lin BY (1977) A squash technique for studying the cytology of maize endosperm and other tissues. Stain Technol 52:197–201

    CAS  PubMed  Google Scholar 

  • Lin BY (1978) Regional control of nondisjunction of the B-chromosome in maize. Genetics 90:613–627

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lin BY (1979) Two new B-10L translocations involved in the control of nondisjunction of the B chromosome in maize. Genetics 92:931–945

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Lippman Z, Martienssen R (2004) The role of RNA interference in heterochromatic silencing. Nature 431:364–370

    CAS  PubMed  Google Scholar 

  • Lisch D (2013) How important are transposons for plant evolution? Nat Rev Genet 14:49–61

    CAS  PubMed  Google Scholar 

  • Liu Q, Chen YQ (2009) Insight into the mechanism of plant development: interactions of miRNA pathway with phytohormone response. Biochem Biophys Res Commun 384:1–5

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Longley AE (1927) Supernumerary chromosomes in Zea mays. J Agric Res 35:769–784

    Google Scholar 

  • Lu C, Tei SS, Luo S, Haudenschild CD, Meyers BC, Green PJ (2005) Elucidation of the small RNA component of the transcriptome. Science 309:1567–1569

    CAS  PubMed  Google Scholar 

  • Mallory AC, Vaucheret H (2006) Functions of microRNAs and related small RNAs in plants. Nat Genet 38:S31–S36

    CAS  PubMed  Google Scholar 

  • 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 14:1035–1046

    CAS  PubMed  Google Scholar 

  • Marques A, Klemme S, Houben A (2018) Evolution of plant B chromosome enriched sequences. Genes 9:515

    PubMed Central  Google Scholar 

  • Nag A, Jack Y (2010) Sculpting the flower; the role of miRNAs in flower development. Curr Top Dev Biol 91:349–378

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Randolph LF (1941) Genetic characteristics of the B chromosomes in maize. Genetics 26:608–631

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

  • Rhoades MM, Dempsey E (1972) On the mechanism of chromatin loss induced by the B chromosome of maize. Genetics 71:73–96

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roman H (1947) Mitotic nondisjunction in the case of interchanges involving the B-type chromosome in maize. Genetics 32:391–409

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roman H (1948) Directed fertilization in maize. Proc Natl Acad Sci U S A34:36–42

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 4:15–23

    CAS  Google Scholar 

  • Staub RW (1987) Leaf striping correlated with the presence of B chromosomes in maize. J Hered 78:71–74

    Google Scholar 

  • 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 3:12

    PubMed  PubMed Central  Google Scholar 

  • 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 17:2204–2216

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ward E (1973) Nondisjunction: localization of the controlling site in the maize B chromosome. Genetics 73:387–391

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e1000716

    PubMed  PubMed Central  Google Scholar 

Download references

Funding

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).

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Correspondence to Ya-Ming Cheng.

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Huang, YH., Peng, SF., Lin, YP. et al. The maize B chromosome is capable of expressing microRNAs and altering the expression of microRNAs derived from A chromosomes. Chromosome Res 28, 129–138 (2020). https://doi.org/10.1007/s10577-019-09620-2

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  • DOI: https://doi.org/10.1007/s10577-019-09620-2

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