Skip to main content
SpringerLink
Log in

The mRNA of a Knotted1-like transcription factor of potato is phloem mobile

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Potato Homeobox1 (POTH1) is a Knotted1-like transcription factor from the Three Amino Acid Loop Extension (TALE) superfamily that is involved in numerous aspects of development in potato (Solanum tuberosum L). POTH1 interacts with its protein partner, StBEL5, to facilitate binding to specific target genes to modulate hormone levels, mediate leaf architecture, and enhance tuber formation. In this study, promoter analyses show that the upstream sequence of POTH1 drives β-glucuronidase activity in response to light and in association with phloem cells in both petioles and stems. Because POTH1 transcripts have previously been detected in phloem cells, long-distance movement of its mRNA was tested. Using RT-PCR and transgenic potato lines over-expressing POTH1, in vitro micrografts demonstrated unilateral movement of POTH1 RNA in a rootward direction. Movement across a graft union into leaves from newly arising axillary shoots and roots of wild type stocks was verified using soil-grown tobacco heterografts. Leaves from the wild type stock containing the mobile POTH1 RNA exhibited a reduction in leaf size relative to leaves from wild type grafts. Both untranslated regions of POTH1 when fused to an expression marker β-glucuronidase, repressed its translation in tobacco protoplasts. RNA/protein binding assays demonstrated that the UTRs of POTH1 bind to two RNA-binding proteins, a polypyrimidine tract-binding protein and an alba-domain type. Conserved glycerol-responsive elements (GRE), specific to alba-domain interaction, are duplicated in both the 5′ and 3′ untranslated regions of POTH1. These results suggest that POTH1 functions as a mobile signal in regulating development.

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
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with image. J Biophotonics Inter 11:36–42

    Google Scholar 

  • Aravind L, Iyer LM, Anantharaman V (2003) The two faces of Alba: the evolutionary connection between proteins participating in chromatin structure and RNA metabolism. Genome Biol 4:R64

    Article  PubMed  CAS  Google Scholar 

  • Asano T, Masumura T, Kusano H, Kikuchi S, Kurita A, Shimada H, Kadowaki K (2002) Construction of a specialized cDNA library from plant cells isolated by laser capture microdissection: toward comprehensive analysis of the genes expressed in the rice phloem. Plant J 32:401–408

    Article  PubMed  CAS  Google Scholar 

  • Auweter SD, Allain FHT (2008) Structure-function relationships of the polypyrimidine tract binding protein. Cell Mol Life Sci 65:516–527

    Article  PubMed  CAS  Google Scholar 

  • Bailey-Serres J, Sorenson R, Juntawong P (2009) Getting the message across: cytoplasmic ribonucleoprotein complexes. Trends Plant Sci 14:443–453

    Article  PubMed  CAS  Google Scholar 

  • Banerjee AK, Chatterjee M, Yu Y, Suh SG, Miller WA, Hannapel DJ (2006a) Dynamics of a mobile RNA of potato involved in a long-distance signaling pathway. Plant Cell 18:3443–3457

    Article  PubMed  CAS  Google Scholar 

  • Banerjee AK, Prat S, Hannapel DJ (2006b) Efficient production of transgenic potato (S. tuberosum L. ssp. andigena) plants via Agrobacterium tumefaciens-mediated transformation. Plant Sci 170:732–738

    Article  CAS  Google Scholar 

  • Banerjee AK, Lin T, Hannapel DJ (2009) Untranslated regions of a mobile transcript mediate RNA metabolism. Plant Physiol 151:1831–1843

    Article  PubMed  CAS  Google Scholar 

  • Baranowskij N, Frohberg C, Prat S, Willmitzer L (1994) A novel DNA binding protein with homology to Myb oncoproteins containing only one repeat can function as a transcriptional activator. EMBO J 13:5383–5392

    PubMed  CAS  Google Scholar 

  • Box MS, Dodsworth S, Rudall PJ, Bateman RM, Glover BJ (2011) Characterization of Linaria KNOX genes suggests a role in petal-spur development. Plant J 68:703–714

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Bürglin TR (1997) Analysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plants and animals. Nucl Acid Res 25:4173–4180

    Article  Google Scholar 

  • Campbell B, Hallengren J, Hannapel DJ (2008) Accumulation of BEL1-like transcripts in solanaceous species. Planta 228:897–906

    Article  PubMed  CAS  Google Scholar 

  • Chang WC, Lee TY, Huang HD, Huang HY, Pan RL (2008) PlantPAN: plant promoter analysis navigator, for identifying combinatorial cis-regulatory elements with distance constraint in plant gene groups. BMC Genomics 9:561

    Article  PubMed  Google Scholar 

  • Chen H, Rosin FM, Hannapel DJ (2003) Interacting transcription factors from the three-amino acid loop extension superclass regulate tuber formation. Plant Physiol 132:1391–1404

    Article  PubMed  CAS  Google Scholar 

  • Chen H, Banerjee AK, Hannapel DJ (2004) The tandem complex of BEL and KNOX partners is required for transcriptional repression of ga20ox1. Plant J 38:276–284

    Article  PubMed  CAS  Google Scholar 

  • Colegrove-Otero LJ, Devaux A, Standart N (2005) The Xenopus ELAV protein ElrB represses Vg1 mRNA translation during oogenesis. Mol Cell Biol 25:9028–9039

    Article  PubMed  CAS  Google Scholar 

  • Ferrandon D, Elphick L, Nusslein-Volhard C, St Johnston D (1994) Staufen protein associates with the 3′ UTR of bicoid mRNA to form particles that move in a microtubule-dependent manner. Cell 79:1221–1223

    Article  PubMed  CAS  Google Scholar 

  • Furger A, Schurch N, Kurath U, Roditi I (1997) Elements in the 3′ untranslated region of procyclin mRNA regulate expression in insect forms of Trypanosoma brucei by modulating RNA stability and translation. Mol Cell Biol 17:4372–4380

    PubMed  CAS  Google Scholar 

  • Gu W, Deng Y, Zenklusen D, Singer RH (2004) A new yeast PUF family protein, Puf6p, represses ASH1 mRNA translation and is required for its localization. Genes Dev 18:1452–1465

    Article  PubMed  CAS  Google Scholar 

  • Ham BK, Brandom JL, Xoconostle-Cázares B, Ringgold V, Lough TJ, Lucas WJ (2009) A polypyrimidine tract binding protein, pumpkin RBP50, forms the basis of a phloem-mobile ribonucleoprotein complex. Plant Cell 21:197–215

    Article  PubMed  CAS  Google Scholar 

  • Hamant O, Pautot V (2010) Plant development: a TALE story. Comptes Rendus Biol 333:371–381

    Article  CAS  Google Scholar 

  • Hay A, Tsiantis M (2010) KNOX genes: versatile regulators of plant development and diversity. Devel 137:3153–3165

    CAS  Google Scholar 

  • Haywood V, Yu TS, Huang NC, Lucas WJ (2005) Phloem long-distance trafficking of GIBBERELLIC ACID-INSENSITIVE RNA regulates leaf development. Plant J 42(1):49–68

    Article  PubMed  CAS  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucl Acids Res 27:297–300

    Article  PubMed  CAS  Google Scholar 

  • Horsch RB, Rogers SG, Fraley RT (1985) Transgenic plants. Cold Spring Harb Symp Quant Biol 50:433–437

    Article  PubMed  CAS  Google Scholar 

  • Hotz HR, Hartmann C, Huober K, Hug M, Christine Clayton C (1997) Mechanisms of developmental regulation in Trypanosoma brucei: a polypyrimidine tract in the 3′-untranslated region of a surface protein mRNA affects RNA abundance and translation. Nucl Acids Res 25:3017–3025

    Article  PubMed  CAS  Google Scholar 

  • Huang NC, Yu TS (2009) The sequences of Arabidopsis GA-INSENSITIVE RNA constitute the motifs that are necessary and sufficient for RNA long-distance trafficking. Plant J 59:921–929

    Article  PubMed  CAS  Google Scholar 

  • Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Reporter 5:387–405

    Article  CAS  Google Scholar 

  • Kerstetter R, Vollbrecht E, Lowe B, Veit B, Yamaguchi J, Hake S (1994) Sequence analysis and expression patterns divide the maize knotted1-like homeobox genes into two classes. Plant Cell 6:1877–1887

    PubMed  CAS  Google Scholar 

  • Kim M, Canio W, Kessler S, Sinha N (2001) Developmental changes due to long-distance movement of a homeobox fusion transcript in tomato. Science 293:287–289

    Article  PubMed  CAS  Google Scholar 

  • Kim JY, Rim Y, Wang J, Jackson D (2005) A novel cell-to-cell trafficking assay indicates that the KNOX homeodomain is necessary and sufficient for intercellular protein and mRNA trafficking. Genes Dev 19:788–793

    Article  PubMed  CAS  Google Scholar 

  • Lin MK, Lee YJ, Lough TJ, Phinney BS, Lucas WJ (2009) Analysis of the pumpkin phloem proteome provides insights into angiosperm sieve tube function. Mol Cell Proteomics 8:343–856

    PubMed  CAS  Google Scholar 

  • Lucas WJ, Bouche-Pillon S, Jackson DP, Nguyen L, Baker L, Ding B, Hake S (1995) Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270:1980–1983

    Article  PubMed  CAS  Google Scholar 

  • Mani J, Güttinger A, Schimanski B, Heller M, Acosta-Serrano A, Pescher P, Späth G, Roditi I (2011) Alba-domain proteins of Trypanosoma brucei are cytoplasmic RNA-binding proteins that interact with the translation machinery. PLoS ONE 6:e22463

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Parnis A, Cohen O, Gutfinger T, Hareven D, Zamir MD, Lifschitz E (1997) The dominant developmental mutants of tomato, Mouse-ear and Curl, are associated with distinct modes of abnormal transcriptional regulation of a Knotted gene. Plant Cell 9:2143–2158

    PubMed  CAS  Google Scholar 

  • Ragni L, Truernit E, Pautot V (2007) KNOXing on the BELL: tALE homeobox genes and meristem activity. Inter J Plant Devel Biol 1:42–48

    Google Scholar 

  • Rosin FM, Hart JK, Horner HT, Davies PJ, Hannapel DJ (2003) Overexpression of a Knotted1-Like Homeobox gene of potato alters vegetative development by decreasing gibberellin accumulation. Plant Physiol 132:106–117

    Article  PubMed  CAS  Google Scholar 

  • Sinha NR, Williams RE, Hake S (1993) Overexpression of the maize homeobox gene, KNOTTED-1, causes a switch from determinate to indeterminate cell fates. Genes Devel 7:787–795

    Article  PubMed  CAS  Google Scholar 

  • Smith HMS, Boschke I, Hake S (2002) Selective interaction of plant homeodomain proteins mediates high DNA-binding affinity. Proc Natl Acad Sci USA 99:9579–9584

    Article  PubMed  CAS  Google Scholar 

  • St Johnston D, Beuchle D, Nusslein-Volhard C (1991) Staufen, a gene required to localize maternal RNAs in the Drosophila egg. Cell 66:51–63

    Article  PubMed  CAS  Google Scholar 

  • Tamaoki M, Kusaba S, Kano-Murakami Y, Matsuoka M (1997) Ectopic expression of a tobacco homeobox gene, NTH15, dramatically alters leaf morphology and hormone levels in transgenic tobacco. Plant Cell Physiol 38:917–927

    Article  PubMed  CAS  Google Scholar 

  • Uchida N, Kimura S, Koenig D, Sinha N (2010) Coordination of leaf development via regulation of KNOX1 genes. J Plant Res 123:7–14

    Article  PubMed  CAS  Google Scholar 

  • Vassella E, Probst M, Schneider A, Studer E, Renggli CK, Roditi I (2004) Expression of a major surface protein of Trypanosoma brucei insect forms is controlled by the activity of mitochondrial enzymes. Mol Biol Cell 15:3986–3993

    Article  PubMed  CAS  Google Scholar 

  • Vauterin M, Frankard V, Jacobs M (1999) The Arabidopsis thaliana dhdps gene encoding dihydrodipicolinate synthase, key enzyme of lysine biosynthesis, is expressed in a cell-specific manner. Plant Mol Biol 39:695–708

    Article  PubMed  CAS  Google Scholar 

  • Vilaine F, Palauqui JC, Amselem J, Kusiak C, Lemoine R, Dinant S (2003) Towards deciphering phloem: a transcriptome analysis of the phloem of Apium graveolens. Plant J 36:67–81

    Article  PubMed  CAS  Google Scholar 

  • Vollbrecht E, Veit B, Sinha N, Hake S (1991) The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature 350:241–243

    Article  PubMed  CAS  Google Scholar 

  • Vorst O, van Dam F, Oosterhoff-Teertstra R, Smeekens S, Weisbeek P (1990) Tissue-specific expression directed by an Arabidopsis thaliana pre-ferredoxin promoter in transgenic tobacco plants. Plant Mol Biol 14:491–499

    Article  PubMed  CAS  Google Scholar 

  • Waksman G, Lebrun M, Freyssinet G, De Biologie L, Veg C, Agrochimie RP (1987) Nucleotide sequence of a gene encoding sunflower ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit (rbcs). Nucl Acids Res 15:7181

    Article  PubMed  CAS  Google Scholar 

  • Walrad P, Paterou A, Acosta-Serrano A, Matthews KR (2009) Differential Trypanosome surface coat regulation by a CCCH protein that co-associates with procyclin mRNA cis-elements. PLoS Pathog 5(2):e1000317

    Article  PubMed  Google Scholar 

  • Wilhelm JE, Vale RD, Hegde RS (2000) Coordinate control of translation and localization of Vg1 mRNA in Xenopus oocytes. Proc Natl Acad Sci USA 97:13132–13137

    Article  PubMed  CAS  Google Scholar 

  • Xu L, Ye R, Zheng Y, Wang Z, Zhou P, Lin Y, Li D (2010) Isolation of the endosperm-specific LPAAT gene promoter from coconut (Cocos nucifera L.) and its functional analysis in transgenic rice plants. Plant Cell Rep 29:1061–1068

    Article  PubMed  CAS  Google Scholar 

  • Yu Y, Lashbrook CC, Hannapel DJ (2007) Tissue integrity and RNA quality of laser microdissected phloem of potato. Planta 226:797–803

    Article  PubMed  CAS  Google Scholar 

  • Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucl Acids Res 31:3406–3415

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Banerjee lab members gratefully acknowledge the support and core funding from Indian Institute of Science Education and Research (IISER), Pune. AM and SB acknowledge the fellowship provided by Department of Biotechnology (DBT) and Council of Scientific and Industrial Research (CSIR), India respectively. We also thank Dr. M. M. Jana, National Chemical Laboratory (NCL), Pune for his guidance in plant maintenance. Contributions of the Hannapel lab were supported by the National Science Foundation (NSF) Plant Genome Research Program award no. DBI-0820659. Thanks to Prof. Isabel Roditi for allowing us to use the Mfold model of the 3′ UTR of the GPEET transcript and to Marvin Wickens for providing the yeast three-hybrid plasmids and strains.

Author information

Author notes

  1. Il Ho Kang

    Present address: DuPont Company, Stine-Haskell Research Center, 1090 Elkton Road, Newark, DE, 19711, USA

Authors and Affiliations

  1. Indian Institute of Science Education and Research (IISER), 900, NCL Innovation Park, Dr. Homi Bhabha Road, Pune, 411008, India

    Ameya Mahajan, Sneha Bhogale & Anjan K. Banerjee

  2. Plant Biology Major, Iowa State University, Ames, IA, 50011-1100, USA

    Il Ho Kang & David J. Hannapel

Authors
  1. Ameya Mahajan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sneha Bhogale
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Il Ho Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David J. Hannapel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anjan K. Banerjee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anjan K. Banerjee.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PPT 558 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mahajan, A., Bhogale, S., Kang, I.H. et al. The mRNA of a Knotted1-like transcription factor of potato is phloem mobile. Plant Mol Biol 79, 595–608 (2012). https://doi.org/10.1007/s11103-012-9931-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-012-9931-0

Keywords

Search

Navigation