Journal of Plant Research

, Volume 128, Issue 3, pp 389–397 | Cite as

WIND1-based acquisition of regeneration competency in Arabidopsis and rapeseed

  • Akira Iwase
  • Kento Mita
  • Satoko Nonaka
  • Momoko Ikeuchi
  • Chie Koizuka
  • Mariko Ohnuma
  • Hiroshi Ezura
  • Jun Imamura
  • Keiko Sugimoto
JPR Symposium Reprogramming of plant cells as adaptive strategies

Abstract

Callus formation and de novo organogenesis often occur in the wounded tissues of plants. Although this regenerative capacity of plant cells has been utilized for many years, molecular basis for the wound-induced acquisition of regeneration competency is yet to be elucidated. Here we find that wounding treatment is essential for shoot regeneration from roots in the conventional tissue culture of Arabidopsis thaliana. Furthermore, we show that an AP2/ERF transcription factor WOUND INDUCED DEDIFFERENTIATION1 (WIND1) plays a pivotal role for the acquisition of regeneration competency in the culture system. Ectopic expression of WIND1 can bypass both wounding and auxin pre-treatment and increase de novo shoot regeneration from root explants cultured on shoot-regeneration promoting media. In Brassica napus, activation of Arabidopsis WIND1 also greatly enhances de novo shoot regeneration, further corroborating the role of WIND1 in conferring cellular regenerative capacity. Our data also show that sequential activation of WIND1 and an embryonic regulator LEAFY COTYLEDON2 enhances generation of embryonic callus, suggesting that combining WIND1 with other transcription factors promote efficient and organ-specific regeneration. Our findings in the model plant and crop plant point to a possible way to efficiently induce callus formation and regeneration by utilizing transcription factors as a molecular switch.

Keywords

Regeneration Callus formation Plant tissue culture Phytohormones AP2/ERF transcription factor 

References

  1. Asahina M, Azuma K, Pitaksaringkarn W et al (2011) Spatially selective hormonal control of RAP2.6L and ANAC071 transcription factors involved in tissue reunion in Arabidopsis. Proc Natl Acad Sci. 108:16128–16132. doi:10.1073/pnas.1110443108 CrossRefPubMedCentralPubMedGoogle Scholar
  2. Atta R, Laurens L, Boucheron-Dubuisson E et al (2009) Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro. Plant J 57:626–644. doi:10.1111/j.1365-313X.2008.03715.x CrossRefPubMedGoogle Scholar
  3. Banno H, Ikeda Y, Niu Q, Chua N (2001) Overexpression of Arabidopsis ESR1 induces initiation of shoot regeneration. Plant Cell 13:2609–2618. doi:10.1105/tpc.010234 CrossRefPubMedCentralPubMedGoogle Scholar
  4. Birnbaum KD, Sánchez-Alvarado A (2008) Slicing across kingdoms: regeneration in plants and animals. Cell 132:697–710. doi:10.1016/j.cell.2008.01.040 CrossRefPubMedCentralPubMedGoogle Scholar
  5. Bostock RM, Stermer BA (1989) Perspectives on wound healing in resistance to pathogens. Annu Rev Phytopathol 27:343–371. doi:10.1146/annurev.py.27.090189.002015 CrossRefGoogle Scholar
  6. Che P, Gingerich DJ, Lall S, Howell SH (2002) Global and hormone-induced gene expression changes during shoot development in Arabidopsis. Plant Cell 14:2771–2785. doi:10.1105/tpc.006668 CrossRefPubMedCentralPubMedGoogle Scholar
  7. Che P, Lall S, Nettleton D, Howell SH (2006) Gene expression programs during shoot, root, and callus development in Arabidopsis tissue culture. Plant Physiol 141:620–637. doi:10.1104/pp.106.081240 CrossRefPubMedCentralPubMedGoogle Scholar
  8. Chupeau M-C, Granier F, Pichon O et al (2013) Characterization of the early events leading to totipotency in an Arabidopsis protoplast liquid culture by temporal transcript profiling. Plant Cell 25:2444–2463. doi:10.1105/tpc.113.109538 CrossRefPubMedCentralPubMedGoogle Scholar
  9. Duclercq J, Sangwan-Norreel B, Catterou M, Sangwan RS (2011) De novo shoot organogenesis: from art to science. Trends Plant Sci 16:597–606. doi:10.1016/j.tplants.2011.08.004 CrossRefPubMedGoogle Scholar
  10. Gallois J-L, Nora FR, Mizukami Y, Sablowski R (2004) WUSCHEL induces shoot stem cell activity and developmental plasticity in the root meristem. Genes Dev 18:375–380. doi:10.1101/gad.291204 CrossRefPubMedCentralPubMedGoogle Scholar
  11. Guzzo F, Baldan B, Levi M et al (1995) Early cellular events during induction of carrot explants with 2,4-D. Protoplasma 185:28–36CrossRefGoogle Scholar
  12. Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J 34:733–739. doi:10.1046/j.1365-313X.2003.01759.x CrossRefPubMedGoogle Scholar
  13. Ikeuchi M, Sugimoto K, Iwase A (2013) Plant callus: mechanisms of induction and repression. Plant Cell 25:3159–3173. doi:10.1105/tpc.113.116053 CrossRefPubMedCentralPubMedGoogle Scholar
  14. Ishikawa M, Murata T, Sato Y et al (2011) Physcomitrella cyclin-dependent kinase A links cell cycle reactivation to other cellular changes during reprogramming of leaf cells. Plant Cell 23:2924–2938. doi:10.1105/tpc.111.088005 CrossRefPubMedCentralPubMedGoogle Scholar
  15. Iwase A, Ishii H, Aoyagi H, Ohme-Takagi M, Tanaka H (2005) Comparative analyses of the gene expression profiles of Arabidopsis intact plant and cultured cells. Biotechnol Lett 27:1097–1103. doi:10.1007/s10529-005-8456-x CrossRefPubMedGoogle Scholar
  16. Iwase A, Mitsuda N, Koyama T et al (2011a) The AP2/ERF transcription factor WIND1 controls cell dedifferentiation in Arabidopsis. Curr Biol 21:508–514. doi:10.1016/j.cub.2011.02.020 CrossRefPubMedGoogle Scholar
  17. Iwase A, Ohme-Takagi M, Sugimoto K (2011b) WIND1: a key molecular switch for plant cell dedifferentiation. Plant Signal Behav 6:1943–1945. doi:10.4161/psb.6.12.18266 CrossRefPubMedCentralPubMedGoogle Scholar
  18. Iwase A, Mitsuda N, Ikeuchi M et al (2013) Arabidopsis WIND1 induces callus formation in rapeseed, tomato, and tobacco. Plant Signal Behav 8:e27432. doi:10.4161/psb.27432 CrossRefPubMedCentralPubMedGoogle Scholar
  19. Kohno-Murase J, Murase M, Ichikawa H, Imamura J (1994) Effects of an antisense napin gene on seed storage compounds in transgenic. Plant Mol Biol 26:1115–1124. doi:10.1007/BF00040693 CrossRefPubMedGoogle Scholar
  20. Ledwoń A, Gaj MD (2009) LEAFY COTYLEDON2 gene expression and auxin treatment in relation to embryogenic capacity of Arabidopsis somatic cells. Plant Cell Rep 28:1677–1688. doi:10.1007/s00299-009-0767-2 CrossRefPubMedGoogle Scholar
  21. Maden M (1976) Blastemal kinetics and pattern formation during amphibian limb regeneration. J Embryol Exp Morphol 36:561–574PubMedGoogle Scholar
  22. Motte H, Vercauteren A, Depuydt S et al (2014) Combining linkage and association mapping identifies RECEPTOR-LIKE PROTEIN KINASE1 as an essential Arabidopsis shoot regeneration gene. Proc Natl Acad Sci USA 111:8305–8310. doi:10.1073/pnas.1404978111 CrossRefPubMedCentralPubMedGoogle Scholar
  23. Ohbayashi I, Konishi M, Ebine K, Sugiyama M (2011) Genetic identification of Arabidopsis RID2 as an essential factor involved in pre-rRNA processing. Plant J 67:49–60. doi:10.1111/j.1365-313X.2011.04574.x CrossRefPubMedGoogle Scholar
  24. Ohtani M, Sugiyama M (2005) Involvement of SRD2-mediated activation of snRNA transcription in the control of cell proliferation competence in Arabidopsis. Plant J 43:479–490. doi:10.1111/j.1365-313X.2005.02469.x CrossRefPubMedGoogle Scholar
  25. Ozawa S, Yasutani I, Fukuda H, Komamine A, Sugiyama M (1998) Organogenic responses in tissue culture of srd mutants of Arabidopsis thaliana. Development 125:135–142PubMedGoogle Scholar
  26. Perianez-Rodriguez J, Manzano C, Moreno-Risueno MA (2014) Post-embryonic organogenesis and plant regeneration from tissues: two sides of the same coin? Front Plant Sci 5:219. doi:10.3389/fpls.2014.00219 CrossRefPubMedCentralPubMedGoogle Scholar
  27. Robert HS, Friml J (2009) Auxin and other signals on the move in plants. Nat Chem Biol 5:325–332. doi:10.1038/nchembio.170 CrossRefPubMedGoogle Scholar
  28. Sangwan RS, Bourgeois Y, Brown S et al (1992) Characterization of competent cells and early events of Agrobacterium-mediated genetic transformation in Arabidopsis thaliana. Planta 188:439–456CrossRefPubMedGoogle Scholar
  29. Skoog F, Miller CO (1957) Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp Soc Exp Biol 11:118–130PubMedGoogle Scholar
  30. Stobbe H, Schmitt U, Eckstein D, Dujesiefken D (2002) Developmental stages and fine structure of surface callus formed after debarking of living lime trees (Tilia sp.). Ann Bot 89:773–782. doi:10.1093/aob/mcf137 CrossRefPubMedCentralPubMedGoogle Scholar
  31. Sugimoto K, Jiao Y, Meyerowitz EM (2010) Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev Cell 18:463–471. doi:10.1016/j.devcel.2010.02.004 CrossRefPubMedGoogle Scholar
  32. Sun HJ, Uchii S, Watanabe S, Ezura H (2006) A highly efficient transformation protocol for Micro-Tom, a model cultivar for tomato functional genomics. Plant Cell Physiol 47:426–431. doi:10.1093/pcp/pci251 CrossRefPubMedGoogle Scholar
  33. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676. doi:10.1016/j.cell.2006.07.024 CrossRefPubMedGoogle Scholar
  34. Tamaki H, Konishi M, Daimon Y et al (2009) Identification of novel meristem factors involved in shoot regeneration through the analysis of temperature-sensitive mutants of Arabidopsis. Plant J 57:1027–1039. doi:10.1111/j.1365-313X.2008.03750.x CrossRefPubMedGoogle Scholar
  35. Thorpe T (2012) History of plant tissue culture. Methods Mol Biol 877:9–27. doi:10.1007/978-1-61779-818-4_2 CrossRefPubMedGoogle Scholar
  36. Valvekens D, Van Montagu M, Van Lijsebettens M (1988) Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc Natl Acad Sci USA 85:5536–5540CrossRefPubMedCentralPubMedGoogle Scholar
  37. Vogel G (2005) How does a single somatic cell become a whole plant? Science 309:86. doi:10.1126/science.309.5731.86 CrossRefPubMedGoogle Scholar
  38. Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69:843–859. doi:10.1016/0092-8674(92)90295-N CrossRefPubMedGoogle Scholar
  39. Yadav SR, Bishopp A, Helariutta Y (2010) Plant development: early events in lateral root initiation. Curr Biol 20:R843–R845. doi:10.1016/j.cub.2010.09.010 CrossRefPubMedGoogle Scholar
  40. Zhou C, Guo J, Feng Z, Cui X, Zhu J (2012) Molecular characterization of a novel AP2 transcription factor ThWIND1-L from Thellungiella halophila. Plant Cell Tissue Organ Cult 110:423–433. doi:10.1007/s11240-012-0163-4 CrossRefGoogle Scholar
  41. Zuo J, Niu Q-W, Chua N-H (2000) An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J 24:265–273. doi:10.1046/j.1365-313x.2000.00868.x CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2015

Authors and Affiliations

  • Akira Iwase
    • 1
  • Kento Mita
    • 2
  • Satoko Nonaka
    • 3
  • Momoko Ikeuchi
    • 1
  • Chie Koizuka
    • 2
  • Mariko Ohnuma
    • 1
  • Hiroshi Ezura
    • 3
  • Jun Imamura
    • 2
  • Keiko Sugimoto
    • 1
  1. 1.RIKEN Center for Sustainable Resource ScienceYokohamaJapan
  2. 2.Graduate School of AgricultureTamagawa UniversityMachidaJapan
  3. 3.Gene Research CenterUniversity of TsukubaTsukubaJapan

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