Transcriptional activation by WRKY23 and derepression by removal of bHLH041 coordinately establish callus pluripotency in Arabidopsis regeneration

Chongyi Xu; Pengjie Chang; Shiqi Guo; Xinchun Liu; Baofeng Sui; Dongxue Yu; Wei Xin; Yuxin Hu

doi:10.1093/plcell/koad255

journal article Oct 06, 2023

Transcriptional activation by WRKY23 and derepression by removal of bHLH041 coordinately establish callus pluripotency in Arabidopsis regeneration

Chongyi Xu

The Plant Cell Vol. 36 No. 1 pp. 158-173 · Oxford University Press (OUP)

View at Publisher Save 10.1093/plcell/koad255

Abstract

Abstract
Induction of the pluripotent cell mass termed callus from detached organs or tissues is an initial step in typical in vitro plant regeneration, during which auxin-induced ectopic activation of root stem cell factors is required for subsequent de novo shoot regeneration. While Arabidopsis (Arabidopsis thaliana) AUXIN RESPONSE FACTOR 7 (ARF7) and ARF19 and their downstream transcription factors LATERAL ORGAN BOUNDARIES DOMAIN (LBD) are known to play key roles in directing callus formation, the molecules responsible for activation of root stem cell factors and thus establishment of callus pluripotency are unclear. Here, we identified Arabidopsis WRKY23 and BASIC HELIX-LOOP-HELIX 041 (bHLH041) as a transcriptional activator and repressor, respectively, of root stem cell factors during establishment of auxin-induced callus pluripotency. We show that auxin-induced WRKY23 downstream of ARF7 and ARF19 directly activates the transcription of PLETHORA 3 (PLT3) and PLT7 and thus that of the downstream genes PLT1, PLT2, and WUSCHEL-RELATED HOMEOBOX 5 (WOX5), while LBD-induced removal of bHLH041 derepresses the transcription of PLT1, PLT2, and WOX5. We provide evidence that transcriptional activation by WRKY23 and loss of bHLH041-imposed repression act synergistically in conferring shoot-regenerating capability on callus cells. Our findings thus disclose a transcriptional mechanism underlying auxin-induced cellular reprogramming, which, together with previous studies, outlines the molecular framework of auxin-induced pluripotent callus formation for in vitro plant regeneration programs.

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References

67

[1]

Aida "The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche" Cell (2004) 10.1016/j.cell.2004.09.018

[2]

Atta "Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro" Plant J (2009) 10.1111/j.1365-313x.2008.03715.x

[3]

Birnbaum "Slicing across kingdoms: regeneration in plants and animals" Cell (2008) 10.1016/j.cell.2008.01.040

[4]

Bowler "Chromatin techniques for plant cells" Plant J (2004) 10.1111/j.1365-313x.2004.02169.x

[5]

Che "Global and hormone-induced gene expression changes during shoot development in Arabidopsis" Plant Cell (2002) 10.1105/tpc.006668

[6]

Che "Developmental steps in acquiring competence for shoot development in Arabidopsis tissue culture" Planta (2007) 10.1007/s00425-007-0565-4

[7]

Che "Gene expression programs during shoot, root, and callus development in Arabidopsis tissue culture" Plant Physiol (2006) 10.1104/pp.106.081240

[8]

Chinnusamy "ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis" Genes Dev (2003) 10.1101/gad.1077503

[9]

Clough "Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana" Plant J (1998) 10.1046/j.1365-313x.1998.00343.x

[10]

Deng "GhTCE1-GhTCEE1 dimers regulate transcriptional reprogramming during wound-induced callus formation in cotton" Plant Cell (2022) 10.1093/plcell/koac252

[11]

Duclercq "De novo shoot organogenesis: from art to science" Trends Plant Sci (2011) 10.1016/j.tplants.2011.08.004

[12]

Fan "LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration" Cell Res (2012) 10.1038/cr.2012.63

[13]

Tissue‐specific expression of stabilized SOLITARY‐ROOT/IAA14 alters lateral root development in Arabidopsis

Hidehiro Fukaki, Yoko Nakao, Yoko Okushima et al.

The Plant Journal 2005 10.1111/j.1365-313x.2005.02537.x

[14]

Fukaki "Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis" Plant J (2002) 10.1046/j.0960-7412.2001.01201.x

[15]

Funakoshi "Small epitope-linker modules for PCR-based C-terminal tagging in Saccharomyces cerevisiae" Yeast (2009) 10.1002/yea.1658

[16]

Gallie "A translational enhancer derived from tobacco mosaic virus is functionally equivalent to a Shine-Dalgarno sequence" Proc Natl Acad Sci U S A (1989) 10.1073/pnas.86.1.129

[17]

Gallie "Visualizing mRNA expression in plant protoplasts: factors influencing efficient mRNA uptake and translation" Plant Cell (1989)

[18]

Goh "Multiple AUX/IAA-ARF modules regulate lateral root formation: the role of Arabidopsis SHY2/IAA3-mediated auxin signalling" Philos Trans R Soc Lond B Biol Sci (2012) 10.1098/rstb.2011.0232

[19]

Gordon "Pattern formation during de novo assembly of the Arabidopsis shoot meristem" Development (2007) 10.1242/dev.010298

[20]

Grunewald "Transcription factor WRKY23 assists auxin distribution patterns during Arabidopsis root development through local control on flavonol biosynthesis" Proc Natl Acad Sci U S A (2012) 10.1073/pnas.1121134109

[21]

Grunewald "A role for AtWRKY23 in feeding site establishment of plant-parasitic nematodes" Plant Physiol (2008) 10.1104/pp.108.119131

[22]

Haecker "Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana" Development (2004) 10.1242/dev.00963

[23]

Hu "The Arabidopsis auxin-inducible gene ARGOS controls lateral organ size" Plant Cell (2003) 10.1105/tpc.013557

[24]

Ikeuchi "Plant callus: mechanisms of induction and repression" Plant Cell (2013) 10.1105/tpc.113.116053

[25]

Imayoshi "bHLH factors in self-renewal, multipotency, and fate choice of neural progenitor cells" Neuron (2014) 10.1016/j.neuron.2014.03.018

[26]

Kareem "PLETHORA Genes control regeneration by a two-step mechanism" Curr Biol (2015) 10.1016/j.cub.2015.02.022

[27]

Kim "Epigenetic reprogramming by histone acetyltransferase HAG1/AtGCN5 is required for pluripotency acquisition in Arabidopsis" EMBO J (2018) 10.15252/embj.201798726

[28]

Lavy "Mechanisms of auxin signaling" Development (2016) 10.1242/dev.131870

[29]

Lateral Organ Boundaries Domain16 and 18 Act Downstream of the AUXIN1 and LIKE-AUXIN3 Auxin Influx Carriers to Control Lateral Root Development in Arabidopsis

Han Woo Lee, Chuloh Cho

Plant Physiology 2015 10.1104/pp.15.00578

[30]

Lee "Dimerization in LBD16 and LBD18 transcription factors is critical for lateral root formation" Plant Physiol (2017) 10.1104/pp.17.00013

[31]

Lee "LBD18 acts as a transcriptional activator that directly binds to the EXPANSIN14 promoter in promoting lateral root emergence of Arabidopsis" Plant J (2013) 10.1111/tpj.12013

[32]

Lee "LBD18/ASL20 regulates lateral root formation in combination with LBD16/ASL18 downstream of ARF7 and ARF19 in Arabidopsis" Plant Physiol (2009) 10.1104/pp.109.143685

[33]

Lee "Arabidopsis ATXR2 deposits H3K36me3 at the promoters of LBD genes to facilitate cellular dedifferentiation" Sci Signal (2017) 10.1126/scisignal.aan0316

[34]

Lin "An Arabidopsis SUMO E3 ligase, SIZ1, negatively regulates photomorphogenesis by promoting COP1 activity" PLoS Genet (2016) 10.1371/journal.pgen.1006016

[35]

Liu "The WOX11-LBD16 pathway promotes pluripotency acquisition in callus cells during de novo shoot regeneration in tissue culture" Plant Cell Physiol (2018) 10.1093/pcp/pcy010

[36]

Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method

Kenneth J. Livak, Thomas D. Schmittgen

Methods 2001 10.1006/meth.2001.1262

[37]

Okushima "ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis" Plant Cell (2007) 10.1105/tpc.106.047761

[38]

Powers "Nucleo-cytoplasmic partitioning of ARF proteins controls auxin responses in Arabidopsis thaliana" Mol Cell (2019) 10.1016/j.molcel.2019.06.044

[39]

Prát "WRKY23 Is a component of the transcriptional network mediating auxin feedback on PIN polarity" PLoS Genet (2018) 10.1371/journal.pgen.1007177

[40]

Radhakrishnan "Shoot regeneration: a journey from acquisition of competence to completion" Curr Opin Plant Biol (2018) 10.1016/j.pbi.2017.08.001

[41]

Optimizing the stability of single-chain proteins by linker length and composition mutagenesis

Clifford R. Robinson, Robert T. Sauer

Proceedings of the National Academy of Sciences 1998 10.1073/pnas.95.11.5929

[42]

Shang "Very-long-chain fatty acids restrict regeneration capacity by confining pericycle competence for callus formation in Arabidopsis" Proc Natl Acad Sci U S A (2016) 10.1073/pnas.1522466113

[43]

Skoog "Chemical regulation of growth and organ formation in plant tissues cultured in vitro" Symp Soc Exp Biol (1957)

[44]

Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants

Imogen A Sparkes, JOHN RUNIONS, Anne Kearns et al.

Nature Protocols 2006 10.1038/nprot.2006.286

[45]

Sugimoto "Regeneration in plants and animals: dedifferentiation, transdifferentiation, or just differentiation?" Trends Cell Biol (2011) 10.1016/j.tcb.2010.12.004

[46]

Sugimoto "Arabidopsis regeneration from multiple tissues occurs via a root development pathway" Dev Cell (2010) 10.1016/j.devcel.2010.02.004

[47]

Sugiyama "Partnership for callusing" Nat Plants (2018) 10.1038/s41477-018-0104-2

[48]

Tatematsu "MASSUGU2 encodes Aux/IAA19, an auxin-regulated protein that functions together with the transcriptional activator NPH4/ARF7 to regulate differential growth responses of hypocotyl and formation of lateral roots in Arabidopsis thaliana" Plant Cell (2004) 10.1105/tpc.018630

[49]

Tessadori "Large-scale dissociation and sequential reassembly of pericentric heterochromatin in dedifferentiated Arabidopsis cells" J Cell Sci (2007) 10.1242/jcs.000026

[50]

Tian "Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene" Development (1999) 10.1242/dev.126.4.711

Showing 50 of 67 references

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Details

Published: Oct 06, 2023
Vol/Issue: 36(1)
Pages: 158-173
License: View

Authors

C

Chongyi Xu

Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, China National Botanical Garden , Beijing 100093 , China

P

Pengjie Chang