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Identification and characterization of three PeSHRs and one PeSCR involved in adventitious root development of Populus

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Abstract

The plant-specific GRAS family transcription factors, SHORT-ROOT (SHR) and SCARECROW (SCR), are key regulators of both the specification of the root stem cell niche and the differentiation potential of a subset of stem cells in the Arabidopsis root. Our previous microarray study indicated that SHR and SCR genes were involved in adventitious root development from hardwood cuttings in Populus. Here, we isolated and characterized three genes encoding SHR proteins and one gene encoding SCR proteins: PeSHR1, PeSHR2, PeSHR3 and PeSCR. Sequence and structure analysis showed that these proteins contained five well-conserved domains: leucine heptad repeat I (LHR I), the VHIID motif, leucine heptad repeat II (LHR II), the PFYRE motif, and the SAM motif. Temporal and spatial expression patterns of these genes were profiled during adventitious root development. Subcellular localization demonstrated that PeSHR1, PeSHR2 and PeSCR were localized to the nucleus, while PeSHR3 was localized to the cytoplasm. Finally, we adapted bimolecular fluorescence complementation to demonstrate that there was interaction between PeSHR1 and PeSCR. Collectively, these results contribute to improving our understanding of conserved and divergent aspects of SHR and SCR in various species.

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References

  • Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218:683–692

    Article  PubMed  CAS  Google Scholar 

  • Bradshaw HD, Ceulemans R, Davis J, Stettler R (2000) Emerging model systems in plant biology: poplar (Populus) as a model forest tree. J Plant Growth Regul 19:306–313

    Article  CAS  Google Scholar 

  • Cruz-Ramírez A, Díaz-Triviño S, Blilou I, Grieneisen VA, Sozzani R, Zamioudis C, Miskolczi P, Nieuwland J, Benjamins R, Dhonukshe P, Caballero-Pérez J, Horvath B, Long Y, Mähönen AP, Zhang H, Xu J, Murray JAH, Benfey PN, Bako L, Marée AFM, Scheres B (2012) A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetric stem cell division. Cell 150:1002–1015

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ, Gallagher KL, Wang JY, Blilou I, Scheres B, Benfey PN (2007) An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316:421–425

    Article  PubMed  CAS  Google Scholar 

  • Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, Hahn MG, Feldmann KA, Benfey PN (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86:423–433

    Article  PubMed  Google Scholar 

  • Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119:71–84

    PubMed  CAS  Google Scholar 

  • Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101:555–567

    Article  PubMed  CAS  Google Scholar 

  • Imin N, Nizamidin M, Wu T, Rolfe BG (2007) Factors involved in root formation in Medicago truncatula. J Exp Bot 58:439–451

    Article  PubMed  CAS  Google Scholar 

  • Jansson S, Douglas CJ (2007) Populus: a model system for plant biology. Annu Rev Plant Biol 58:435–458

    Article  PubMed  CAS  Google Scholar 

  • Kamiya N, Itoh JI, Morikami A, Nagato Y, Matsuoka M (2003) The SCARECROW gene’s role in asymmetric cell divisions in rice plants. Plant J 36:45–54

    Article  PubMed  CAS  Google Scholar 

  • Koizumi K, Wu S, MacRae-Crerar A, Gallagher KL (2011) An essential protein that interacts with endosomes and promotes movement of the SHORT-ROOT transcription factor. Curr Biol 21:1559–1564

    Article  PubMed  CAS  Google Scholar 

  • Koizumi K, Hayashi T, Wu S, Gallagher KL (2012) The SHORT-ROOT protein acts as a mobile, dose-dependent signal in patterning the ground tissue. Proc Natl Acad Sci 109:13010–13015

    Article  PubMed Central  PubMed  Google Scholar 

  • Levesque MP, Vernoux T, Busch W, Cui H, Wang JY, Blilou I, Hassan H, Nakajima K, Matsumoto N, Lohmann JU, Scheres B, Benfey PN (2006) Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis. PLoS Biol 4:e143

    Article  PubMed Central  PubMed  Google Scholar 

  • Lim J, Helariutta Y, Specht CD, Jung J, Sims L, Bruce WB, Diehn S, Benfey PN (2000) Molecular analysis of the SCARECROW gene in maize reveals a common basis for radial patterning in diverse meristems. Plant Cell Online 12:1307–1318

    Article  CAS  Google Scholar 

  • Nakajima K, Sena G, Nawy T, Benfey PN (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413:307–311

    Article  PubMed  CAS  Google Scholar 

  • Pysh LD, Wysocka-Diller JW, Camilleri C, Bouchez D, Benfey PN (1999) The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J 18:111–119

    Article  PubMed  CAS  Google Scholar 

  • Ramírez-Carvajal GA, Morse AM, Dervinis C, Davis JM (2009) The cytokinin type-B response regulator PtRR13 is a negative regulator of adventitious root development in Populus. Plant Physiol 150:759–771

    Article  PubMed Central  PubMed  Google Scholar 

  • Rigal A, Yordanov YS, Perrone I, Karlberg A, Tisserant E, Bellini C, Busov VB, Martin F, Kohler A, Bhalerao R, Legué V (2012) The AINTEGUMENTA LIKE1 homeotic transcription factor PtAIL1 controls the formation of adventitious root primordia in poplar. Plant Physiol 160:1996–2006

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Scheres B (2013) Rooting plant development. Development 140:939–941

    Article  PubMed  CAS  Google Scholar 

  • Schrader J, Nilsson J, Mellerowicz E, Berglund A, Nilsson P, Hertzberg M, Sandberga G (2004) A high-resolution transcript profile across the wood-forming meristem of poplar identifies potential regulators of cambial stem cell identity. Plant Cell 16:2278–2292

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Solé A, Sánchez C, Vielba JM, Valladares S, Abarca D, Díaz-Sala C (2008) Characterization and expression of a Pinus radiata putative ortholog to the Arabidopsis SHORT-ROOT gene. Tree Physiol 28:1629–1639

    Article  PubMed  Google Scholar 

  • Sozzani R, Cui H, Moreno-Risueno MA, Busch W, Van Norman JM, Vernoux T, Brady SM, Dewitte W, Murray JAH, Benfey PN (2010) Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth. Nature 466:128–132

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Tan B, Xu M, Chen Y, Huang M (2013) Transient expression for functional gene analysis using Populus protoplasts. Plant Cell, Tissue Organ Cult 114:11–18

    Article  CAS  Google Scholar 

  • Taylor G (2002) Populus: Arabidopsis for forestry. Do we need a model tree? Ann Bot 90:681–689

    Article  PubMed  CAS  Google Scholar 

  • Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Déjardin A, Depamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjärvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leplé JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouzé P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  PubMed  CAS  Google Scholar 

  • Walter M, Chaban C, Schütze K, Batistic O, Weckermann K, Näke C, Blazevic D, Grefen C, Schumacher K, Oecking C, Harter K, Kudla J (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40:428–438

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Andersson-Gunnerås S, Gaboreanu I, Hertzberg M, Tucker MR, Zheng B, Leśniewska J, Mellerowicz EJ, Laux T, Sandberg G, Jones B (2011) Reduced expression of the SHORT-ROOT gene increases the rates of growth and development in hybrid poplar and Arabidopsis. PLoS ONE 6:e28878

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wu S, Gallagher KL (2013) Intact microtubules are required for the intercellular movement of the SHORT-ROOT transcription factor. Plant J 74:148–159

    Article  PubMed  CAS  Google Scholar 

  • Wu X, Weigel D, Wigge PA (2002) Signaling in plants by intercellular RNA and protein movement. Genes Dev 16:151–158

    Article  PubMed  CAS  Google Scholar 

  • Xu M, Zhang B, Su X, Zhang S, Huang M (2011) Reference gene selection for quantitative real-time polymerase chain reaction in Populus. Anal Biochem 408:337–339

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This project was supported by Grants from the Natural Science Foundation of the Jiangsu Higher Education Institutions of China (13KJA220002), the National Natural Science Foundation of China (31100484), the Innovative Research Project for Postgraduates in Colleges of Jiangsu Province (CXZZ13_0549), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

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Authors and Affiliations

  1. Jiangsu Key Laboratory for Poplar Germplasm Enhancement and Variety Improvement, Nanjing Forestry University, Nanjing, 210037, China

    Lei Xuan, Meng Xu, Caihui Chen, Chunxia Yang, Li’an Xu & Minren Huang

  2. Key Laboratory of Forest Genetics and Biotechnology, Ministry of Education, Nanjing Forestry University, Nanjing, 210037, China

    Lei Xuan, Meng Xu, Caihui Chen, Chunxia Yang, Li’an Xu & Minren Huang

Authors
  1. Lei Xuan
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  2. Meng Xu
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  3. Caihui Chen
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  4. Chunxia Yang
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  5. Li’an Xu
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  6. Minren Huang
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Correspondence to Meng Xu or Minren Huang.

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Lei Xuan and Meng Xu have contributed equally to this work.

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Xuan, L., Xu, M., Chen, C. et al. Identification and characterization of three PeSHRs and one PeSCR involved in adventitious root development of Populus . Plant Cell Tiss Organ Cult 117, 253–264 (2014). https://doi.org/10.1007/s11240-014-0437-0

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  • DOI: https://doi.org/10.1007/s11240-014-0437-0

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