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Identification, characterization of an AP2/ERF transcription factor that promotes adventitious, lateral root formation in Populus

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Abstract

Using activation tagging in Populus, we have identified five mutant lines showing changes in their adventitious rooting. Among the affected lines, three showed increased and two decreased adventitious rooting. We have positioned the tag in the mutant lines via recovering genomic sequences flanking the left-hand border of the activation tagging vector and validated the transcriptional activation of the proximal genes. We further characterized one line in which the cause of the observed rooting phenotype was up-regulation of a gene encoding a transcription factor of the AP2/ERF family of unknown function (PtaERF003). We show, through retransformation, that this gene has a positive effect on both adventitious and lateral root proliferation. Comparative expression analyses show that the phenotype does not result from ectopic expression but rather up-regulation of the native expression pattern of the gene. PtaERF003 function is linked to auxin signal transduction pathway, as suggested by the rapid induction and accentuated phenotypes of the transgenic plants in presence of the hormone. Upregulation of PtaERF003 led to most significant metabolic changes in the shoot suggesting of a broader regulatory role of the gene that is not restricted to root growth and development. Our study shows that dominant tagging approaches in poplar can successfully identify novel molecular factors controlling adventitious and lateral root formation in woody plants. Such discoveries can lead to technologies that can increase root proliferation and, thus, have significant economic and environmental benefits.

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References

  • Aharoni A, Dixit S, Jetter R, Thoenes E, Van Arkel G, Pereira A (2004) The SHINE clade of AP2 domain transcription factors activate wax biosynthesis, alter cuticle properties and confer drought tolerance when overexpressed in Arabidopsis. Plant Cell 16:2463–2480

    Article  PubMed  CAS  Google Scholar 

  • Albrectsen BR, Gutierrez L, Fritz RS, Fritz RD, Orians CM (2007) Does the differential seedling mortality caused by slugs alter the foliar traits and subsequent susceptibility of hybrid willows to a generalist herbivore? Ecol Entomol 32:211–220

    Google Scholar 

  • Aloni R, Aloni E, Langhans M, Ullrich CI (2006) Role of cytokinin and auxin in shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Ann Bot 97:883–893

    Article  PubMed  CAS  Google Scholar 

  • Biondi S, Diaz T, Iglesias I, Gamberini G, Bagni N (1990) Polyamines and ethylene in relation to adventitious root formation in Prunus avium shoot cultures. Physiol Plantarum 78:474–483

    Article  Google Scholar 

  • Broun P, Poindexter P, Osborne E, Jiang CZ, Riechmann JL (2004) WIN1, a transcriptional activator of epidermal wax accumulation in Arabidopsis. P Nalt Acad Aci USA 101:4706–4711

    Article  CAS  Google Scholar 

  • Busov VB, Meilan R, Pearce DW, Ma C, Rood SB, Strauss SH (2003) Activation tagging of a dominant gibberellin catabolism gene (GA 2-oxidase) from poplar that regulates tree stature. Plant Physiol 132:1–9

    Article  Google Scholar 

  • Busov VB, Brunner AM, Meilan R, Filichkin S, Ganio L, Gandhi S, Strauss SH (2005a) Genetic transformation: a powerful tool for dissection of adaptive traits in trees. New Phytol 167:9–18

    Article  PubMed  CAS  Google Scholar 

  • Busov VB, Fladung M, Groover A, Strauss SH (2005b) Insertional mutagenesis in Populus: relevance and feasibility. Tree Genet Genomes 1:135–142

    Article  Google Scholar 

  • Busov V, Meilan R, Pearce DW, Rood SB, Ma C, Tschaplinski TJ, Strauss SH (2006) Transgenic modification of gai or rgl1 causes dwarfing and alters gibberellins, root growth, and metabolite profiles in Populus. Planta 224:288–299

    Article  PubMed  CAS  Google Scholar 

  • Busov V, Yordanov Y, Gou J, Meilan R, Ma C, Regan S, Strauss S (2010) Activation tagging is an effective gene tagging system in Populus. Tree Genet Genomes 7:91–101

    Article  Google Scholar 

  • Cheng JC, Seeley KA, Sung Z (1995) RML1 and RML2, Arabidopsis genes required for cell proliferation at the root tip. Plant Physiol 107:365–376

    Article  PubMed  CAS  Google Scholar 

  • Chenna R, Sugawara H, Koike T, Lopex R, Gibson TJ, Higgins DJ, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497–3500

    Article  PubMed  CAS  Google Scholar 

  • De Klerk GJ (2002) Rooting of microcuttings: theory and practice. In Vitro Cell Dev-Pl 38:415–422

    Article  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 

  • Dörmann P, Hoffmann-Benning S, Balbo I, Benning C (1995) Isolation and characterization of an Arabidopsis mutant deficient in the thylakoid lipid digalactosyl diacylglycerol. Plant Cell 7:1801–1810

    PubMed  Google Scholar 

  • Filichkin SE, Qian W, Busov VB, Meilan R, Lanz-Garcia C, Groover A, Goldgarb B, Ma C, Dharmawardhana P, Brunner A, Strauss S (2006) Enhancer trapping in woody plants: isolation of the ET304 gene encoding a putative AT-hook motif transcription factor and characterization of the expression patterns conferred by its promoter in transgenic Populus and Arabidopsis. Plant Sci 17:206–216

    Article  Google Scholar 

  • Fladung M, Polak O (2012) Ac/Ds-transposon activation tagging in poplar: a powerful tool for gene discovery. BMC Genomics 13:61

    Article  PubMed  CAS  Google Scholar 

  • Gutierrez L, Bussell JD, Pacurar DI, Schwambach J, Pacurar M, Bellini C (2009) Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell 21:3119–3132

    Article  PubMed  CAS  Google Scholar 

  • Gutierrez L, Mongelard G, Floková K, Păcurar DI, Novák O, Staswick P, Kowalczyk M, Păcurara M, Demailly H, Geiss G, Bellini C (2012) Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell 24:2515–2527

    Article  PubMed  CAS  Google Scholar 

  • Harrison E, Bush M, Plett JM, McPhee DP, Vitez R, O’Malley B, Sharma V, Bosnich W, Seguin A, MacKay J, Regan S (2007) Diverse developmental mutants revealed in an activation-tagged population of poplar. Can J Bot 85:1071–1081

    Article  CAS  Google Scholar 

  • Hartel H, Lokstein H, Dormann P, Grimm B, Benning C (1997) Changes in the composition of the photosynthetic apparatus in the galactolipid-deficient dgd1 mutant of Arabidopsis thaliana. Plant Physiol 115:1175–1184

    Article  PubMed  CAS  Google Scholar 

  • Heidstra R, Welch D, Scheres B (2004) Mosaic analyses using marked activation and deletion clones dissect Arabidopsis SCARECROW action in asymmetric cell division. Genes Develop 18:1964–1969

    Article  PubMed  CAS  Google Scholar 

  • Himanen K, Vuylsteke M, Vanneste S, Vercruysse S, Boucheron E, Alard P, Chriqui D, Van Montagu M, Inze D, Beeckman T (2004) Transcript profiling of early lateral root initiation. P Nalt Acad Aci USA 101:5146–5151

    Article  CAS  Google Scholar 

  • Holsters M, de Waele D, Depicker A, Messens E, Van Montagu M, Schell J (1978) Transfection and transformation of Agrobacterium tumefaciens. Mol Gen Genet 163:181–187

    Article  PubMed  CAS  Google Scholar 

  • Hua J, Meyerowitz EM (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94:261–271

    Article  PubMed  CAS  Google Scholar 

  • Ivanchenko MG, Muday GK, Dubrovsky JG (2008) Ethylene-auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. Plant J 55:335–347

    Article  PubMed  CAS  Google Scholar 

  • Jofuku KD, den Boer BG, Van Montagu M, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211–1225

    PubMed  CAS  Google Scholar 

  • Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193–195

    Article  PubMed  CAS  Google Scholar 

  • Kim MJ, Ruzicka D, Shin R, Schachtman DP (2012) The Arabidopsis AP2/ERF transcription factor RAP2.11 modulates plant response to low-potassium conditions. Mol Plant 5:1042–1057

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi K, Kondo M, Fukuda H, Nishimura M, Ohta H (2007) Galactolipid synthesis in chloroplast inner envelope is essential for proper thylakoid biogenesis, photosynthesis, and embryogenesis. P Nalt Acad Aci USA 104:17216–17221

    Article  CAS  Google Scholar 

  • Lindroth R, Hwang SY (1996) Clonal variation in foliar chemistry of quaking aspen (Populus tremuloides Michx.). Biochem Syst Ecol 24:357–364

    Article  CAS  Google Scholar 

  • Liu YG, Mitsukawa N, Oosumi T, Whittier RF (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J 8:457–463

    Article  PubMed  CAS  Google Scholar 

  • Lyzenga WJ, Stone SL (2012) Regulation of ethylene biosynthesis through protein degradation. Plant Signal Behav 7:1438–1442

    Article  PubMed  CAS  Google Scholar 

  • Moellering ER, Benning C (2011) Galactoglycerolipid metabolism under stress: a time for remodelling. Trends Plant Sci 16:98–107

    Article  PubMed  CAS  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    Article  PubMed  CAS  Google Scholar 

  • Negi S, Ivanchenko MG, Muday GK (2008) Ethylene regulates lateral root formation and auxin transport in Arabidopsis thaliana. Plant J 55:175–187

    Article  PubMed  CAS  Google Scholar 

  • Negi S, Sukumar P, Liu X, Cohen JD, Muday GK (2010) Genetic dissection of the role of ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato. Plant J 61:3–15

    Article  PubMed  CAS  Google Scholar 

  • Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182

    PubMed  CAS  Google Scholar 

  • Orians CM, Fritz RS (1995) Secondary chemistry of hybrid and parental willows-phenolic glycosides and condensed tannins in Salix sericeaS. eriocephala, and their hybrids. J Chem Ecol 21:1245–1253

    Article  CAS  Google Scholar 

  • Orians CM, Huang C, Wild A, Dorfman KA, Zee P, Dao MTT, Fritz RS (1997) Willow hybridization differentially affects preference and performance of herbivorous beetles. Entomol Exp Appl 83:285–294

    Article  Google Scholar 

  • Plett JM, Wilkins O, Campbell MM, Ralph SG, Regan S (2010) Endogenous overexpression of Populus MYB186 increases trichome density, improves insect pest resistance, and impacts plant growth. Plant J 64:419–432

    Article  PubMed  CAS  Google Scholar 

  • Prasad ME, Schofield A, Lyzenga W, Liu HX, Stone SL (2010) Arabidopsis RING E3 ligase XBAT32 regulates lateral root production through its role in ethylene biosynthesis. Plant Physiol 153:1587–1596

    Article  PubMed  CAS  Google Scholar 

  • Ramirez-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  CAS  Google Scholar 

  • Richter GL, Monshausen GB, Krol A, Gilroy S (2009) Mechanical stimuli modulate lateral root organogenesis. Plant Physiol 151:1855–1866

    Article  PubMed  CAS  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  CAS  Google Scholar 

  • Sakai H, Hua J, Chen QG, Chang C, Medrano LJ, Bleecker AB, Meyerowitz EM (1998) ETR2 is an ETR1-like gene involved in ethylene signaling in Arabidopsis. P Nalt Acad Aci USA 95:5812–5817

    Article  CAS  Google Scholar 

  • Sanchez C, Vielba JM, Ferro E, Covelo G, Sole A, Abarca D, De Mier BS, Diaz-Sala C (2007) Two SCARECROW-LIKE genes are induced in response to exogenous auxin in rooting-competent cuttings of distantly related forest species. Tree Physiol 27:1459–1470

    Article  PubMed  CAS  Google Scholar 

  • Smith DL, Fedoroff NV (1995) A gene expressed in lateral and adventitious root primordia of Arabidopsis. Plant Cell 7:735–745

    PubMed  CAS  Google Scholar 

  • Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GTS, Sandberg G, Bhalerao R, Ljung K, Bennett MJ (2007) Ethylene up-regulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19:2186–2196

    Article  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 

  • Trupiano D, Di Iorio A, Montagnoli A, Lasserre B, Rocco M, Grosso A, Scaloni A, Marra M, Chiatante D, Scippa GS (2012) Involvement of lignin and hormones in the response of woody poplar taproots to mechanical stress. Physiol Plantarum 146:39–52

    Article  CAS  Google Scholar 

  • Woeste KE, Vogel JP, Kieber JJ (1999) Factors regulating ethylene biosynthesis in etiolated Arabidopsis thaliana seedlings. Physiol Plantarum 105:478–484

    Article  CAS  Google Scholar 

  • Wysocka-Diller JW, Helariutta Y, Fukaki H, Malamy JE, Benfey PN (2000) Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot. Development 127:595–603

    PubMed  CAS  Google Scholar 

  • Yordanov YS, Regan S, Busov V (2010) Members of the LATERAL ORGAN BOUNDARIES DOMAIN transcription factor family are involved in the regulation of secondary growth in Populus. Plant Cell 22:3662–3677

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported in part by grants from the US Department of Energy (DOE), Poplar Genome Based Research for Carbon Sequestration in Terrestrial Ecosystems (DE-FG02-06ER64185, DE-FG02-05ER64113), the Consortium for Plant Biotechnology Research, Inc. (GO12026-203A), the United States Department of Agriculture (USDA) CSREES, the USDA-NRI Plant Genome program (2003-04345) and USDA CSREES, the Biotechnology Risk Assessment Research Grants Program (2004-35300-14687), Plant Feedstock Genomics for Bioenergy: A Joint Research Program of USDA and DOE (2009-65504-05767). The research at ORNL was supported by the Office of Biological and Environmental Research in the DOE Office of Science. This manuscript has been authored by a contractor of the U.S. Government under contract DE-AC05-00OR22725.

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Correspondence to Victor Busov.

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Trupiano, D., Yordanov, Y., Regan, S. et al. Identification, characterization of an AP2/ERF transcription factor that promotes adventitious, lateral root formation in Populus . Planta 238, 271–282 (2013). https://doi.org/10.1007/s00425-013-1890-4

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