Skip to main content
SpringerLink
Log in

Identification and characterization of PaGL1-like genes from Platanus acerifolia related to the regulation of trichomes

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Key Message

Two PaGL1-like genes were identified in London plane and functional in Arabidopsis, moreover, may play an important role in the regulation of trichome development in London plane.

Abstract

Trichome development is governed by a complex regulatory network. In Arabidopsis, subgroup 15 of the R2R3 MYB transcription factor family, which includes GLABRA1 (GL1), is involved in trichome development. In this study, we isolated and characterized two PaGL1-like genes from London plane (Platanus acerifolia). Sequence alignment and phylogenetic analysis indicated that these PaGL1-like genes are homologous to AtGL1. Quantitative real-time PCR (qRT-PCR) analysis showed that PaGL1-like1 was expressed in all of the tested organs taken from adult London plane trees, including trichomes, petioles after trichome removal, stems after trichome removal, and leaves after trichome removal, and also in the roots, cotyledons, hypocotyls and true leaves of seedlings. By contrast, the PaGL1-like2 was expressed only in the trichomes and leaves after trichome removal from adult trees, and in the cotyledons and true leaves of seedlings. Overexpression of PaGL1-like genes caused trichome abortion when transferred into wild type Arabidopsis and promoted trichome formation in the gl1 mutant. The expression profiles of some trichome-related genes were changed in transgenic Arabidopsis lines, and yeast two-hybrid analysis indicated that PaGL1-like proteins can directly interact with trichome-related bHLH proteins from both P. acerifolia and Arabidopsis. These results suggest that PaGL1-like genes are functional in Arabidopsis and may play an important role in the regulation of trichome development in London plane.

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
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Baumann K, Perez-Rodriguez M, Bradley D, Venail J, Bailey P, Jin HL, Koes R, Roberts K, Martin C (2007) Control of cell and petal morphogenesis by R2R3 MYB transcription factors. Development 134:1691–1701

    CAS  PubMed  Google Scholar 

  • Bernhardt C, Zhao M, Gonzalez A, Lloyd A, Schiefelbein J (2005) The bHLH genes GL3 and EGL3 participate in an intercellular regulatory circuit that controls cell patterning in the Arabidopsis root epidermis. Development 132:291–298

    CAS  PubMed  Google Scholar 

  • Besnard G, Tagmount A, Baradat P, Vigouroux A, Berville A (2002) Molecular approach of genetic affinities between wild and ornamental Platanus. Euphytica 126:401–412

    CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    CAS  Google Scholar 

  • Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581

    CAS  PubMed  Google Scholar 

  • Feller A, Machemer K, Braun EL, Grotewold E (2011) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 66:94–116

    CAS  PubMed  Google Scholar 

  • Fernandez-Gonzalez M, Guedes A, Abreu I, Rodriguez-Rajo FJ (2013) Pla a_1 aeroallergen immunodetection related to the airborne Platanus pollen content. Sci Total Environ 463:855–860

    PubMed  Google Scholar 

  • Galway ME, Masucci JD, Lloyd AM, Walbot V, Davis RW, Schiefelbein JW (1994) The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root. Dev Biol 166:740–754

    CAS  PubMed  Google Scholar 

  • Gan LJ, Xia K, Chen JG, Wang SC (2011) Functional characterization of TRICHOMELESS2, a new single-repeat R3 MYB transcription factor in the regulation of trichome patterning in Arabidopsis. BMC Plant Biol 11:176

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang MK, Hu YL, Liu X, Li YG, Hou XL (2015) Arabidopsis LEAFY COTYLEDON1 controls cell fate determination during post-embryonic development. Front Plant Sci 6:955

    PubMed  PubMed Central  Google Scholar 

  • Hülskamp M (2004) Plant trichomes: a model for cell differentiation. Nat Rev Mol Cell Biol 5:471–480

    PubMed  Google Scholar 

  • Hülskamp M (2019) Trichomes. Curr Biol 29:R273–R274

    PubMed  Google Scholar 

  • Hülskamp M, Schnittger A (1998) Spatial regulation of trichome formation in Arabidopsis thaliana. Semin Cell Dev Biol 9:213–220

    PubMed  Google Scholar 

  • Ishida T, Hattori S, Sano R, Inoue K, Shirano Y, Hayashi H, Shibata D, Sato S, Kato T, Tabata S, Okada K, Wada T (2007) Arabidopsis TRANSPARENT TESTA GLABRA2 is directly regulated by R2R3 MYB transcription factors and is involved in regulation of GLABRA2 transcription in epidermal differentiation. Plant Cell 19:2531–2543

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ishida T, Kurata T, Okada K, Wada TA (2008) Genetic regulatory network in the development of trichomes and root hairs. Annu Rev Plant Biol 59:365–386

    CAS  PubMed  Google Scholar 

  • Jakoby MJ, Falkenhan D, Mader MT, Brininstool G, Wischnitzki E, Platz N, Hudson A, Lskamp MHR, Larkin J, Schnittger A (2008) Transcriptional profiling of mature Arabidopsis trichomes reveals that NOECK encodes the MIXTA like transcriptional regulator MYB106. Plant Physiol 148:1583–1602

    CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson HB (1975) Plant pubescence: an ecological perspective. Bot Rev 41:233–258

    Google Scholar 

  • Kang YH, Kirik V, Hülskamp M, Nam KH, Hagely K, Lee MM, Schiefelbeind J (2009) The MYB23 gene provides a positive feedback loop for cell fate specification in the Arabidopsis root epidermis. Plant Cell 21:1080–1094

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kirik V, Schnittger A, Radchuk V, Adler K, Hülskamp M, Baumlein H (2001) Ectopic expression of the Arabidopsis AtMYB23 gene induces differentiation of trichome cells. Dev Biol 235:366–377

    CAS  PubMed  Google Scholar 

  • Kirik V, Simon M, Hülskamp M, Schiefelbein J (2004a) The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. Dev Biol 268:506–513

    CAS  PubMed  Google Scholar 

  • Kirik V, Simon M, Wester K, Schiefelbein J, Hülskamp M (2004b) ENHANCER of TRY and CPC2 (ETC2) reveals redundancy in the region-specific control of trichome development of Arabidopsis. Plant Mol Biol 55:389–398

    CAS  PubMed  Google Scholar 

  • Kirik V, Lee MM, Wester K, Herrmann U, Zheng Z, Oppenheimer D, Schiefelbein J, Hülskamp M (2005) Functional diversification of MYB23 and GL1 genes in trichome morphogenesis and initiation. Development 132:1477–1485

    CAS  PubMed  Google Scholar 

  • Larkin JC, Oppenheimer DG, Lloyd AM, Paparozzi ET, Marks MD (1994) Roles of the GLABROUS1 and TRANSPARENT TESTA GLABRA genes in Arabidopsis trichome development. Plant Cell 6:1065–1076

    CAS  PubMed  PubMed Central  Google Scholar 

  • Larkin JC, Marks MD, Nadeau J, Sack F (1997) Epidermal cell fate and patterning in leaves. Plant Cell 9:1109–1120

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee MM, Schiefelbein J (1999) WEREWOLF, a MYB-related protein in Arabidopsis, is a position-dependent regulator of epidermal cell patterning. Cell 99:473–483

    CAS  PubMed  Google Scholar 

  • Li Z, Liu G, Zhang J, Zhang J, Bao M (2008) Extraction of high quality tissue-specific RNA from London plane trees (Platanus acerifolia), permitting the construction of a female inflorescence cDNA library. Funct Plant Biol 35:159–165

    CAS  PubMed  Google Scholar 

  • Liang G, He H, Li Y, Ai Q, Yu DQ (2014) MYB82 functions in regulation of trichome development in Arabidopsis. J Exp Bot 65:3215–3223

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu G, Bao M (2003) Adventitious shoot regeneration from in vitro-cultured leaves of London plane tree (Platanus acerifolia Willd.). Plant Cell Rep 21:640–644

    CAS  PubMed  Google Scholar 

  • Liu H, Liu SB, Jiao JJ, Lu TJ, Xu F (2017) Trichomes as a natural biophysical barrier for plants and their bioinspired applications. Soft Matter 13:5096–5106

    CAS  PubMed  Google Scholar 

  • Maes L, Inze D, Goossens A (2008) Functional specialization of the TRANSPARENT TESTA GLABRA1 network allows differential hormonal control of laminal and marginal trichome initiation in Arabidopsis rosette leaves. Plant Physiol 148:1453–1464

    CAS  PubMed  PubMed Central  Google Scholar 

  • Matsui K, Hiratsu K, Koyama T, Tanaka H, Ohme-Takagi M (2005) A chimeric AtMYB23 repressor induces hairy roots, elongation of leaves and stems, and inhibition of the deposition of mucilage on seed coats in Arabidopsis. Plant Cell Physiol 46:147–155

    CAS  PubMed  Google Scholar 

  • Mauricio R, Rausher MD (1997) Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution 51:1435–1444

    PubMed  Google Scholar 

  • Meinke DW, Franzmann LH, Nickle TC, Yeung EC (1994) Leafy cotyledon mutants of Arabidopsis. Plant Cell 6:1049–1064

    CAS  PubMed  PubMed Central  Google Scholar 

  • Morohashi K, Zhao M, Yang M, Read B, Lloyd A, Lamb R, Grotewold E (2007) Participation of the Arabidopsis bHLH factor GL3 in trichome initiation regulatory events. Plant Physiol 145:736–746

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ohashi Y, Oka A, Ruberti I, Morelli G, Aoyama T (2002) Entopically additive expression of GLABRA2 alters the frequency and spacing of trichome initiation. Plant J 29:359–369

    CAS  PubMed  Google Scholar 

  • Pattanaik S, Patra B, Singh SK, Yuan L (2014) An overview of the gene regulatory network controlling trichome development in the model plant, Arabidopsis. Front Plant Sci 5:259

    PubMed  PubMed Central  Google Scholar 

  • Payne CT, Zhang F, Lloyd AM (2000) GL3 encodes a bHLH protein that regulates trichome development in Arabidopsis through interaction with GL1 and TTG1. Genetics 156:1349–1362

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pesch M, Hülskamp M (2009) One, two, three..models for trichome patterning in Arabidopsis? Curr Opin Plant Biol 12:587–592

    CAS  PubMed  Google Scholar 

  • Pesch M, Hülskamp M (2011) Role of TRIPTYCHON in trichome patterning in Arabidopsis. BMC Plant Biol 11:130

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qing L, Aoyama T (2012) Pathways for epidermal cell differentiation via the homeobox gene GLABRA2: update on the roles of the classic regulator. J Integr Plant Biol 54:729–737

    PubMed  Google Scholar 

  • Rerie WG, Feldmann KA, Marks MD (1994) The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev 8:1388–1399

    CAS  PubMed  Google Scholar 

  • Schellmann S, Schnittger A, Kirik V, Wada T, Okada K, Beermann A, Thumfahrt J, Jürgens G, Hülskamp M (2002) TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J 21:5036–5046

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schnittger A, Folkers U, Schwab B, Jürgens G, Hülskamp M (1999) Generation of a spacing pattern: the role of TRIPTYCHON in trichome patterning in Arabidopsis. Plant Cell 11:1105–1116

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4:447–456

    CAS  PubMed  Google Scholar 

  • Subiza J, Cabrera M, Valdivieso R, Subiza JL, Jerez M, Jimenez JA, Narganes MJ, Subiza E (1994) Seasonal asthma caused by airborne platanus pollen. Clin Exp Allergy 24:1123–1129

    CAS  PubMed  Google Scholar 

  • Tominaga R, Iwata M, Sano R, Inoue K, Okada K, Wada T (2008) Arabidopsis CAPRICE-LIKE MYB 3 (CPL3) controls endoreduplication and flowering development in addition to trichome and root hair formation. Development 135:1335–1345

    CAS  PubMed  Google Scholar 

  • Tominaga-Wada R, Wada T (2017) Extended C termini of CPC-LIKE MYB proteins confer functional diversity in Arabidopsis epidermal cell differentiation. Development 144:2375–2380

    CAS  PubMed  Google Scholar 

  • Tominaga-Wada R, Nukumizu Y, Sato S, Kato T, Tabata S, Wada T (2012) Functional divergence of MYB-Related genes, WEREWOLF and AtMYB23 in Arabidopsis. Biosci Biotechnol Biochem 76:883–887

    CAS  PubMed  Google Scholar 

  • Varela S, Subiza J, Subiza JL, Rodriguez R, Garcia B, Jerez M, Jimenez JA, Panzani R (1997) Platanus pollen as an important cause of pollinosis. J Allergy Clin Immun 100:748–754

    CAS  PubMed  Google Scholar 

  • Wada T, Tachibana T, Shimura Y, Okada K (1997) Epidermal cell differentiation in Arabidopsis determined by a Myb homolog CPC. Science 277:1113–1116

    CAS  PubMed  Google Scholar 

  • Walker AR, Davison PA, Bolognesi-Winfield AC, James CM, Srinivasan N, Blundell TL, Esch JJ, Marks MD, Gray JC (1999) The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11:1337–1349

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Wang JW, Yu N, Li CH, Luo B, Gou JY, Wang LJ, Chen XY (2004) Control of plant trichome development by a cotton fiber MYB gene. Plant Cell 16:2323–2334

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Kwak SH, Zeng Q, Ellis BE, Chen XY, Schiefelbein J, Chen JG (2007) TRICHOMELESS1 regulates trichome patterning by suppressing GLABRA1 in Arabidopsis. Development 134:3873–3882

    CAS  PubMed  Google Scholar 

  • Wang S, Hubbard L, Chang Y, Guo J, Schiefelbein J, Chen JG (2008) Comprehensive analysis of single-repeat R3 MYB proteins in epidermal cell patterning and their transcriptional regulation in Arabidopsis. BMC Plant Biol 8:81

    PubMed  PubMed Central  Google Scholar 

  • Wang Z, Ye SF, Li JJ, Zheng B, Bao MZ, Ning GG (2011) Fusion primer and nested integrated PCR (FPNI-PCR): a new high-efficiency strategy for rapid chromosome walking or flanking sequence cloning. BMC Biotechnol 11:109

    PubMed  PubMed Central  Google Scholar 

  • Werker E (2000) Trichome diversity and development. Adv Bot Res 31:1–35

    Google Scholar 

  • West MAL, Yee KM, Danao J, Zimmerman JL, Fischer RL, Goldberg RB, Harada JJ (1994) LEAFY COTYLEDON1 is an essential regulator of late embryogenesis and cotyledon identity in Arabidopsis. Plant Cell 6:1731–1745

    Google Scholar 

  • Wester K, Digiuni S, Geier F, Timmer J, Fleck C, Hülskamp M (2009) Functional diversity of R3 single-repeat genes in trichome development. Development 136:1487–1496

    CAS  PubMed  Google Scholar 

  • Zhang F, Gonzalez A, Zhao MZ, Payne CT, Lloyd A (2003) A network of redundant bHLH proteins functions in all TTG1- dependent pathways of Arabidopsis. Development 130:4859–4869

    CAS  PubMed  Google Scholar 

  • Zhang BP, Chopra D, Schrader A, Hülskamp M (2019) Evolutionary comparison of competitive protein-complex formation of MYB, bHLH, and WDR proteins in plants. J Exp Bot 70:3197–3209

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao M, Morohashi K, Hatlestad G, Grotewold E, Lloyd A (2008) The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci. Development 135:1991–1999

    CAS  PubMed  Google Scholar 

  • Zimmermann IM, Heim MA, Weisshaar B, Uhrig JF (2004) Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like bHLH proteins. Plant J 40:22–34

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was funded by the National Natural Science Foundation of China (Grant Nos. 31672187 and 31570696). We thank Dr Alex McCormac (Mambo-Tox Ltd., Southampton, UK) for help with editing of the manuscript and all colleagues in our laboratory for technical assistance.

Author information

Authors and Affiliations

  1. Key Laboratory of Horticultural Plant Biology, Ministry of Education, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, People’s Republic of China

    Yanping Zhang, Changsheng Shao, Zhiru Bao, Fangfang Cai, Haofei Zhu, Jiaqi Zhang & Manzhu Bao

  2. Key Laboratory of Urban Agriculture in Central China, Ministry of Agriculture and Rural Affairs, Wuhan, 430070, People’s Republic of China

    Yanping Zhang, Changsheng Shao, Zhiru Bao, Fangfang Cai, Haofei Zhu, Jiaqi Zhang & Manzhu Bao

Authors
  1. Yanping Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Changsheng Shao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhiru Bao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fangfang Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Haofei Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jiaqi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Manzhu Bao
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YZ, JZ and MB designed the experiments; YZ performed the majority of experiments; CS, ZB, FC and HZ supplied the materials; YZ and JZ analyzed experimental results. YZ prepared the initial manuscript draft; JZ and MB produced the final manuscript version. All of the authors approved the final manuscript.

Corresponding authors

Correspondence to Jiaqi Zhang or Manzhu Bao.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Y., Shao, C., Bao, Z. et al. Identification and characterization of PaGL1-like genes from Platanus acerifolia related to the regulation of trichomes. Plant Mol Biol 104, 235–248 (2020). https://doi.org/10.1007/s11103-020-01028-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-020-01028-5

Keywords

Search

Navigation