Skip to main content
SpringerLink
Log in

Feminized tassels of maize mop1 and ts1 mutants exhibit altered levels of miR156 and specific SBP-box genes

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Development of the unisexual maize inflorescences requires the abortion of pistillate primordia in the florets of the developing tassel and the arrest of staminate primordia in the florets of the developing ears. Mutations of many genes that lie within this sexual differentiation pathway, such as tasselseed1 (ts1), or that influence this pathway, such as mediator of paramutation 1 (mop1), result in feminization of the normally male tassel. Here, we show the loss of mop1 or ts1 function results in increased mRNA levels for several members of the SBP-box gene family. Our analyses of this family expand the number of maize SBP-box genes from 9 to 31 members. Intron–exon structures as well as phylogenetic data support the division of these family members into six groups. The SBP-box genes upregulated in feminized tassels fall into two groups, share common structural motifs and include the presence of a target site for miR156. Small RNA blots show miR156 levels are decreased in both mop1 and ts1 mutants. While there is a correlation between miR156 levels and SBP-box gene transcript levels, this correlation is not absolute, and thus we hypothesize that decreased levels of miR156 may provide competency for SBP-box gene upregulation by other common factors yet to be identified. We present a model that provides a putative link between ts1, ts2, ts4, Ts6, and mop1 in the sex-determination pathway.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abbott AL, Alvarez-Saavedra E, Miska EA, Lau NC, Bartel DP, Horvitz HR, Ambros V (2005) The let-7 microRNA family members mir-48, mir-84, and mir-241 function together to regulate developmental timing in Caenorhabditis elegans. Dev Cell 9:403–414

    Article  PubMed  CAS  Google Scholar 

  • Alleman M, Sidorenko L, McGinnis K, Seshadri V, Dorweiler JE, White J, Sikkink K, Chandler VL (2006) An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 442:295–298

    Article  PubMed  CAS  Google Scholar 

  • Becraft PW, Bongard-Pierce DK, Sylvester AW, Poethig RS, Freeling M (1990) The liguleless-1 gene acts tissue specifically in maize leaf development. Dev Biol 141:220–232

    Article  PubMed  CAS  Google Scholar 

  • Birkenbihl RP, Jach G, Saedler H, Huijser P (2005) Functional dissection of the plant-specific SBP-domain: overlap of the DNA-binding and nuclear localization domains. J Mol Biol 352:585–596

    Article  PubMed  CAS  Google Scholar 

  • Calderon-Urrea A, Dellaporta SL (1999) Cell death and cell protection genes determine the fate of pistils in maize. Development 126:435–441

    PubMed  CAS  Google Scholar 

  • Cardon GH, Hohmann S, Nettesheim K, Saedler H, Huijser P (1997) Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3: a novel gene involved in the floral transition. Plant J 12:367–377

    Article  PubMed  CAS  Google Scholar 

  • Cardon G, Hohmann S, Klein J, Nettesheim K, Saedler H, Huijser P (1999) Molecular characterisation of the Arabidopsis SBP-box genes. Gene 237:91–104

    Article  PubMed  CAS  Google Scholar 

  • Cheng PC, Greyson RI, Walden DB (1983) Organ initiation and the development of unisexual flowers in the tassel and ear of Zea mays. Am J Bot 70:450–462

    Article  Google Scholar 

  • Chuck G, Cigan AM, Saeteurn K, Hake S (2007a) The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 39:544–549

    Article  PubMed  CAS  Google Scholar 

  • Chuck G, Meeley R, Irish E, Sakai H, Hake S (2007b) The maize tasselseed4 microRNA controls sex determination and meristem cell fate by targeting Tasselseed6/indeterminate spikelet1. Nat Genet 39:1517–1521

    Article  PubMed  CAS  Google Scholar 

  • DeLong A, Calderon-Urrea A, Dellaporta SL (1993) Sex determination gene TASSELSEED2 of maize encodes a short-chain alcohol dehydrogenase required for stage-specific floral organ abortion. Cell 74:757–768

    Article  PubMed  CAS  Google Scholar 

  • Dorweiler JE, Doebley J (1997) Developmental analysis of teosinte glume architecure 1: a key locus in the evolution of maize (Poaceae). Am J Bot 84:1313–1322

    Article  Google Scholar 

  • Dorweiler JE, Stec A, Kermicle JL, Doebley J (1993) Teosinte glume architecture-1: a genetic locus controlling a key step in maize evolution. Science 262:233–235

    Article  PubMed  Google Scholar 

  • Dorweiler JE, Carey CC, Kubo KM, Hollick JB, Kermicle JL, Chandler VL (2000) Mediator of paramutation1 is required for establishment and maintenance of paramutation at multiple maize loci. Plant Cell 12:2101–2118

    Article  PubMed  CAS  Google Scholar 

  • Eck RV, Dayhoff MO (1966) Atlas of protein sequence and structure, National Biomedical Research Foundation, Silver Springs

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed  CAS  Google Scholar 

  • Emerson RA (1920) Heritable characters of maize. II. Pistillate flowered maize plants. J Hered 11:65–76

    Google Scholar 

  • Emerson RA, Beadle GW, Fraser AC (1935) A summary of linkage studies in maize. Cornell Univ Agric Exp Sta Mem 180:1–83

    Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Gandikota M, Birkenbihl RP, Hohmann S, Cardon GH, Saedler H, Huijser P (2007) The miRNA156/157 recognition element in the 3′ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J 49:683–693

    Article  PubMed  CAS  Google Scholar 

  • Gaut BS, Doebley JF (1997) DNA sequence evidence for the segmental allotetraploid origin of maize. Proc Natl Acad Sci USA 94:6809–6814

    Article  PubMed  CAS  Google Scholar 

  • Hardison RC (1996) A brief history of hemoglobins: plant, animal, protist, and bacteria. Proc Natl Acad Sci USA 93:5675–5679

    Article  PubMed  CAS  Google Scholar 

  • Irish EE, Langdale JA, Nelson TM (1994) Interactions between tassel seed genes and other sex determining genes in maize. Dev Genet 15:155–171

    Article  Google Scholar 

  • Jones DF (1932) The interaction of specific genes determining sex in dioecious maize. Proc Sixth Int Cong Genet 2:104–107

    Google Scholar 

  • Jones DF (1934) Unisexual maize plants and their bearing on sex differentiation in other plants and in animals. Genetics 19:552–567

    PubMed  CAS  Google Scholar 

  • Klein J, Saedler H, Huijser P (1996) A new family of DNA binding proteins includes putative transcriptional regulators of the Antirrhinum majus floral meristem identity gene SQUAMOSA. Mol Gen Genet 250:7–16

    PubMed  CAS  Google Scholar 

  • Lauter N, Kampani A, Carlson S, Goebel M, Moose SP (2005) MicroRNA172 down-regulates glossy15 to promote vegetative phase change in maize. Proc Natl Acad Sci USA 102:9412–9417

    Article  PubMed  CAS  Google Scholar 

  • Lee RC, Ambros V (2001) An extensive class of small RNAs in Caenorhabditis elegans. Science 294:862–864

    Article  PubMed  CAS  Google Scholar 

  • Manning K, Tor M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38:948–952

    Article  PubMed  CAS  Google Scholar 

  • McSteen P, Laudencia-Chingcuanco D, Colasanti J (2000) A floret by any other name: control of meristem identity in maize. TIPS 5:61–66

    CAS  Google Scholar 

  • Millar AA, Waterhouse PM (2005) Plant and animal microRNAs: similarities and differences. Funct Integr Genomics 5:129–135

    Article  PubMed  CAS  Google Scholar 

  • Miska EA, Alvarez-Saavedra E, Abbott AL, Lau NC, Hellman AB, McGonagle SM, Bartel DP, Ambros VR, Horvitz HR (2007) Most Caenorhabditis elegans microRNAs are individually not essential for development or viability. PLoS Genet 3:e215

    Article  PubMed  Google Scholar 

  • Moreno MA, Harper LC, Krueger RW, Dellaporta SL, Freeling M (1997) Liguleless1 encodes a nuclear-localized protein required for induction of ligules and auricles during maize leaf organogenesis. Genes Dev 11:616–628

    Article  PubMed  CAS  Google Scholar 

  • Moss EG (2007) Heterochronic genes and the nature of developmental time. Curr Biol 17:R425–R434

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  • Neuffer M, Coe EH Jr, Wessler SR (1997) Mutants of maize, Cold Spring Harbor Laboratory Press

  • Nickerson NH, Dale EE (1955) Tassel modifications in Zea mays. Ann Mo Bot Gard 42:195–212

    Article  Google Scholar 

  • Olsen PH, Ambros V (1999) The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev Biol 216:671–680

    Article  PubMed  CAS  Google Scholar 

  • Paquette SM, Bak S, Feyereisen R (2000) Intron–exon organization and phylogeny in a large superfamily, the paralogous cytochrome P450 genes of Arabidopsis thaliana. DNA Cell Biol 19:307–317

    Article  PubMed  CAS  Google Scholar 

  • Parkinson SE, Gross SM, Hollick JB (2007) Maize sex determination and abaxial leaf fates are canalized by a factor that maintains repressed epigenetic states. Dev Biol 308:462–473

    Article  PubMed  CAS  Google Scholar 

  • Peirson SN, Butler JN, Foster RG (2003) Experimental validation of novel and conventional approaches to quantitative real-time PCR data analysis. Nucleic Acids Res 31:e73

    Article  PubMed  Google Scholar 

  • Phipps I (1928) Heritable characters in maize. XXXI. Tassel seed-4. J Hered 19:399–404

    Google Scholar 

  • Pontes O, Li CF, Nunes PC, Haag J, Ream T, Vitins A, Jacobsen SE, Pikaard CS (2006) The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell 126:79–92

    Article  PubMed  CAS  Google Scholar 

  • Rogozin IB, Wolf YI, Sorokin AV, Mirkin BG, Koonin EV (2003) Remarkable interkingdom conservation of intron positions and massive, lineage-specific intron loss and gain in eukaryotic evolution. Curr Biol 13:1512–1517

    Article  PubMed  CAS  Google Scholar 

  • Ronemus M, Vaughn MW, Martienssen RA (2006) MicroRNA-targeted and small interfering RNA-mediated mRNA degradation is regulated by argonaute, dicer, and RNA-dependent RNA polymerase in Arabidopsis. Plant Cell 18:1559–1574

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Schwarz S, Grande AV, Bujdoso N, Saedler H, Huijser P (2008) The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis. Plant Mol Biol 67:183–195

    Article  PubMed  CAS  Google Scholar 

  • Stone JM, Liang X, Nekl ER, Stiers JJ (2005) Arabidopsis AtSPL14, a plant-specific SBP-domain transcription factor, participates in plant development and sensitivity to fumonisin B1. Plant J 41:744–754

    Article  PubMed  CAS  Google Scholar 

  • Sylvester AW, Cande WZ, Freeling M (1990) Division and differentiation during normal and liguleless-1 maize leaf development. Development 110:985–1000

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Unte US, Sorensen AM, Pesaresi P, Gandikota M, Leister D, Saedler H, Huijser P (2003) SPL8, an SBP-box gene that affects pollen sac development in Arabidopsis. Plant Cell 15:1009–1019

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Nussbaum-Wagler T, Li B, Zhao Q, Vigouroux Y, Faller M, Bomblies K, Lukens L, Doebley JF (2005) The origin of the naked grains of maize. Nature 436:714–719

    Article  PubMed  CAS  Google Scholar 

  • Wijeratne AJ, Zhang W, Sun Y, Liu W, Albert R, Zheng Z, Oppenheimer DG, Zhao D, Ma H (2007) Differential gene expression in Arabidopsis wild-type and mutant anthers: insights into anther cell differentiation and regulatory networks. Plant J 52:14–29

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547

    Article  PubMed  CAS  Google Scholar 

  • Xie K, Wu C, Xiong L (2006) Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 142:280–293

    Article  PubMed  CAS  Google Scholar 

  • Xie Z, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD, Zilberman D, Jacobsen SE, Carrington JC (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2:E104

    Article  PubMed  Google Scholar 

  • Yang Z, Wang X, Gu S, Hu Z, Xu H, Xu C (2008) Comparative study of SBP-box gene family in Arabidopsis and rice. Gene 407:1–11

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Schwarz S, Saedler H, Huijser P (2007) SPL8, a local regulator in a subset of gibberellin-mediated developmental processes in Arabidopsis. Plant Mol Biol 63:429–439

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the Maize Genome Sequencing Consortium for making genomic sequence available prior to publication, Amanda R. Robinson for assistance collecting some of the tassel RNA samples and Theresa A. Miller, Michael Schläppi, and anonymous reviewers for helpful comments on the manuscript. This project was supported by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service, grant number 2004-35301-14495.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Marquette University, P.O. Box 1881, Milwaukee, WI, 53201-1881, USA

    Judd F. Hultquist & Jane E. Dorweiler

Authors
  1. Judd F. Hultquist
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jane E. Dorweiler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jane E. Dorweiler.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hultquist, J.F., Dorweiler, J.E. Feminized tassels of maize mop1 and ts1 mutants exhibit altered levels of miR156 and specific SBP-box genes. Planta 229, 99–113 (2008). https://doi.org/10.1007/s00425-008-0813-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-008-0813-2

Keywords

Search

Navigation