Plant Callus: Mechanisms of Induction and Repression

doi:10.1105/TPC.113.116053

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Plant Callus: Mechanisms of Induction and Repression

Journal Article•DOI•

Plant Callus: Mechanisms of Induction and Repression

Momoko Ikeuchi, Keiko Sugimoto, Akira Iwase

01 Sep 2013-The Plant Cell (American Society of Plant Biologists)-Vol. 25, Iss: 9, pp 3159-3173

TL;DR: This review will first provide a brief overview of callus development in nature and in vitro and then describe the current knowledge of genetic and epigenetic mechanisms underlying callus formation.

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Abstract: Plants develop unorganized cell masses like callus and tumors in response to various biotic and abiotic stimuli. Since the historical discovery that the combination of two growth-promoting hormones, auxin and cytokinin, induces callus from plant explants in vitro, this experimental system has been used extensively in both basic research and horticultural applications. The molecular basis of callus formation has long been obscure, but we are finally beginning to understand how unscheduled cell proliferation is suppressed during normal plant development and how genetic and environmental cues override these repressions to induce callus formation. In this review, we will first provide a brief overview of callus development in nature and in vitro and then describe our current knowledge of genetic and epigenetic mechanisms underlying callus formation.

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Journal Article•DOI•

Advancing Crop Transformation in the Era of Genome Editing

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Fredy Altpeter¹, Nathan M. Springer², Laura E. Bartley³, Ann E. Blechl⁴, Thomas P. Brutnell⁵, Vitaly Citovsky⁶, Liza J. Conrad⁷, Stanton B. Gelvin⁸, David A. Jackson⁹, Albert P. Kausch¹⁰, Peggy G. Lemaux¹¹, June I. Medford¹², Martha L. Orozco-Cárdenas¹³, David M. Tricoli¹⁴, Joyce Van Eck¹⁵, Daniel F. Voytas², Virginia Walbot¹⁶, Kan Wang¹⁷, Zhanyuan J. Zhang¹⁸, C. Neal Stewart¹⁹ - Show less +16 more•Institutions (19)

University of Florida¹, University of Minnesota², University of Oklahoma³, United States Department of Agriculture⁴, Donald Danforth Plant Science Center⁵, Stony Brook University⁶, Eckerd College⁷, Purdue University⁸, Cold Spring Harbor Laboratory⁹, University of Rhode Island¹⁰, University of California, Berkeley¹¹, Colorado State University¹², University of California, Riverside¹³, University of California, Davis¹⁴, Boyce Thompson Institute for Plant Research¹⁵, Stanford University¹⁶, Iowa State University¹⁷, University of Missouri¹⁸, University of Tennessee¹⁹

01 Jul 2016-The Plant Cell

TL;DR: The state of plant transformation is reviewed and innovations needed to enable genome editing in crops are pointed to, including a potential game-changer in crop genetics when plant transformation systems are optimized.

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Abstract: Plant transformation has enabled fundamental insights into plant biology and revolutionized commercial agriculture. Unfortunately, for most crops, transformation and regeneration remain arduous even after more than thirty years of technological advances. Genome editing provides new opportunities to enhance crop productivity, but relies on genetic transformation and plant regeneration, which are bottlenecks in the process. Herein we review the state of plant transformation and point to innovations needed to enable genome editing in crops. Plant tissue culture methods need optimization and simplification for efficiency and minimize time in culture. Currently, specialized facilities exist for crop transformation. Single cell and robotic techniques should be developed for high throughput genomic screens. Utilization of plant genes involved in developmental reprogramming, wound response, and/or homologous recombination could boost recovery of transformed plants. Engineering universal Agrobacterium strains and recruitment of other microbes, such as Ensifer or Rhizobium, could facilitate delivery of DNA and proteins into plant cells. Synthetic biology should be employed for de novo design of transformation systems. Genome editing is a potential game-changer in crop genetics when plant transformation systems are optimized.

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419 citations

Cites background from "Plant Callus: Mechanisms of Inducti..."

...…2012); cytokinin type-B ARABIDOPSIS RESPONSE REGULATORs (Sakai et al., 2001; Tajima et al., 2004); transcription factors, such as LEAFY COTYLEDON1 (LEC1),WUSCHEL (WUS), andBABYBOOM (ODP2); AGAMOUS-LIKE15; and the SOMATIC EMBRYOGENESIS RECEPTOR KINASE (reviewed in Ikeuchi et al., 2013; Fehér, 2015)....
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...The molecular mechanisms for induction of cultured tissues from somatic cells are becoming better understood, and stress plays a striking role in this process (Florentin et al., 2013; Ikeuchi et al., 2013; Fehér, 2015; Grafi and Barack, 2015)....
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Journal Article•DOI•

Somatic embryogenesis - Stress-induced remodeling of plant cell fate.

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Attila Fehér¹•Institutions (1)

Hungarian Academy of Sciences¹

01 Apr 2015-Biochimica et Biophysica Acta

TL;DR: The present knowledge on chromatin-based mechanisms potentially involved in the somatic-to-embryogenic developmental transition is summarized, emphasizing the potential role of the chromatin to integrate stress, hormonal, and developmental pathways leading to the activation of the embryogenic program.

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352 citations

Cites background from "Plant Callus: Mechanisms of Inducti..."

...Although this finding raised a debate about the inherent pluri/totipotency of differentiated plant cells [8,9], it cannot explain all types of plant regeneration that most likely can follow various pathways [3,4,10] such as during somatic embryogenesis ([11]; and see Section 3 for details)....
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...Wound-induced calli are considered to be the result of dedifferentiation regulated by the AP2/ERF transcription factor, WOUND INDUCED DEDIFFERENTIATION1 (WIND1), and its close homologues WIND2, WIND3, and WIND4 [10,77,79]....
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...overproliferation of certain cells in whole plants as reviewed in [10]....
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...In addition, callus formation in response to wounding has been reported to initiate from different cell layers of various plant organs [10,77]....
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...However, calli are very diverse and the term callus indeed includes cells with various degrees of differentiation [10]....
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Journal Article•DOI•

Plant regeneration: cellular origins and molecular mechanisms

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Momoko Ikeuchi, Yoichi Ogawa, Akira Iwase, Keiko Sugimoto

01 May 2016-Development

TL;DR: This Review article summarizes the current understanding of how plants control various types of regeneration and discusses how developmental and environmental constraints influence these regulatory mechanisms.

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Abstract: Compared with animals, plants generally possess a high degree of developmental plasticity and display various types of tissue or organ regeneration. This regenerative capacity can be enhanced by exogenously supplied plant hormones in vitro, wherein the balance between auxin and cytokinin determines the developmental fate of regenerating organs. Accumulating evidence suggests that some forms of plant regeneration involve reprogramming of differentiated somatic cells, whereas others are induced through the activation of relatively undifferentiated cells in somatic tissues. We summarize the current understanding of how plants control various types of regeneration and discuss how developmental and environmental constraints influence these regulatory mechanisms.

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347 citations

Cites background from "Plant Callus: Mechanisms of Inducti..."

...2), wound stimuli may in fact provide a primary inductive trigger for this phenomenon (Birnbaum and Sánchez Alvarado, 2008; Ikeuchi et al., 2013; Sugiyama, 2015)....
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Journal Article•DOI•

WOX11 and 12 Are Involved in the First-Step Cell Fate Transition during de Novo Root Organogenesis in Arabidopsis

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Jingchun Liu¹, Lihong Sheng¹, Yingqiang Xu¹, Yingqiang Xu², Jiqin Li¹, Zhong-Nan Yang², Hai Huang¹, Lin Xu¹ - Show less +4 more•Institutions (2)

Chinese Academy of Sciences¹, Shanghai Normal University²

01 Mar 2014-The Plant Cell

TL;DR: The cellular and molecular framework of de novo root organogenesis from leaf explants of Arabidopsis thaliana is revealed and shows that auxin-induced WOX11 expression marks the first-step cell fate transition in this process.

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Abstract: De novo organogenesis is a process through which wounded or detached plant tissues or organs regenerate adventitious roots and shoots. Plant hormones play key roles in de novo organogenesis, whereas the mechanism by which hormonal actions result in the first-step cell fate transition in the whole process is unknown. Using leaf explants of Arabidopsis thaliana, we show that the homeobox genes WUSCHEL RELATED HOMEOBOX11 (WOX11) and WOX12 are involved in de novo root organogenesis. WOX11 directly responds to a wounding-induced auxin maximum in and surrounding the procambium and acts redundantly with its homolog WOX12 to upregulate LATERAL ORGAN BOUNDARIES DOMAIN16 (LBD16) and LBD29, resulting in the first-step cell fate transition from a leaf procambium or its nearby parenchyma cell to a root founder cell. In addition, our results suggest that de novo root organogenesis and callus formation share a similar mechanism at initiation.

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329 citations

Cites background from "Plant Callus: Mechanisms of Inducti..."

...In recent decades, the regulation of de novo organogenesis in plants has been studied extensively, and phytohormones are considered to be the critical factors affecting this process (Skoog and Miller, 1957; Sangwan et al., 1997; De Klerk et al., 1999; Duclercq et al., 2011; Ikeuchi et al., 2013)....
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Journal Article•DOI•

PLETHORA Genes Control Regeneration by a Two-Step Mechanism.

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Abdul Kareem¹, Kavya Durgaprasad¹, Kaoru Sugimoto², Yujuan Du³, Ajai J. Pulianmackal¹, Zankhana B. Trivedi¹, Pazhoor V. Abhayadev¹, Violaine Pinon³, Elliot M. Meyerowitz², Ben Scheres³, Kalika Prasad¹ - Show less +7 more•Institutions (3)

Indian Institute of Science Education and Research, Thiruvananthapuram¹, California Institute of Technology², Wageningen University and Research Centre³

20 Apr 2015-Current Biology

TL;DR: The findings uncouple the acquisition of competence to regenerate shoot progenitor cells from completion of shoot formation, indicating a two-step mechanism of de novo shoot regeneration that operates in all tested plant tissues irrespective of their origin.

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196 citations

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References

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Journal Article•DOI•

The enhancement of plant growth by free-living bacteria

[...]

Bernard R. Glick

01 Feb 1995-Canadian Journal of Microbiology

TL;DR: The ways in which plant growth promoting rhizobacteria facilitate the growth of plants are considered and discussed and the possibility of improving plant growth promotion by specific genetic manipulation is critically examined.

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Abstract: The ways in which plant growth promoting rhizobacteria facilitate the growth of plants are considered and discussed. Both indirect and direct mechanisms of plant growth promotion are dealt with. Th...

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2,529 citations

"Plant Callus: Mechanisms of Inducti..." refers background in this paper

...Many of these bacteria produce auxin and cytokinin (Morris, 1986; Glick, 1995) to promote tumorization in host plants (Manulis et al., 1998)....
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...Many of these bacteria produce auxin and cytokinin (Morris, 1986; Glick, 1995) to promote tumorization in host plants (Manulis et al....
[...]

Book•

Plant Propagation by Tissue Culture

[...]

Edwin F. George

01 Jan 1984

TL;DR: The Anatomy and Morphology of Tissue Cultured Plants M.V. Moshkov, G. V. Novikova, M. Stasolla, E. Zazimalova and E.F. George reveal the secrets of successful tissue culture and the challenges faced in implementing and sustaining such a system.

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Abstract: Biographical Notes on Contributors.- 1.Plant Tissue Culture Procedure - Background E.F. George.- 2.Micropropagation: Uses and Methods E.F. George and P.C. Debergh.- 3.The Components Of Plant Tissue Culture Media I : Macro- and Micronutrients E.F. George and G-J. de Klerk.- 4.The Components Of Plant Tissue Culture Media II : Organic supplements, Organic Acids, Osmotic and pH Effects and Support systems T. Thorpe, C. Stasolla, E.C. Yeung, G-J. de Klerk, A. Roberts and E.F. George.- 5.Plant Growth Regulators: Introduction I: Auxins, Their Analogues And Inhibitors I. Machakova, E. Zazimalova and E.F. George.- 6.Plant Growth Regulators II: Cytokinins, Their Analogues And Antagonists J. van Staden, E. Zazimalova and E.F. George.- 7.Plant Growth Regulators III: Gibberellins, Ethylene, Abscisic Acid, Their Analogues And Inhibitors Miscellaneous Compounds I.E. Moshkov, G.V. Novikova, M.A. Hall and E.F. George.- 8.Developmental Biology D. Chriqui.- 9.Somatic Embryogenesis S. Von Arnold.- 10.Adventitious Regeneration P.B. Gahan and E.F. George.- 11.Stock Plant Physiological Factors Affecting Growth and Morphogenesis J. Preece.- 12.Effects Of The Physical Environment E.F. George and W. Davies.- 13.The Anatomy And Morphology Of Tissue Cultured Plants M. Ziv and J. Chen

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2,358 citations

"Plant Callus: Mechanisms of Inducti..." refers background in this paper

...After the groundbreaking discovery that callus can be generated artificially in vitro (Gautheret, 1939; Nobécourt, 1939; White, 1939) and that the balance between two plant hormones, auxin and cytokinin, determines the state of differentiation and dedifferentiation (Skoog and Miller, 1957), callus has been widely used in both basic research and industrial applications (George and Sherrington, 1984; Bourgaud et al., 2001)....
[...]
...…1939) and that the balance between two plant hormones, auxin and cytokinin, determines the state of differentiation and dedifferentiation (Skoog and Miller, 1957), callus has been widely used in both basic research and industrial applications (George and Sherrington, 1984; Bourgaud et al., 2001)....
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Journal Article•

Chemical regulation of growth and organ formation in plant tissues cultured in vitro.

[...]

F Skoog, C O Miller

01 Jan 1957-Symposia of the Society for Experimental Biology

2,227 citations

"Plant Callus: Mechanisms of Inducti..." refers background in this paper

...After the groundbreaking discovery that callus can be generated artificially in vitro (Gautheret, 1939; Nobécourt, 1939; White, 1939) and that the balance between two plant hormones, auxin and cytokinin, determines the state of differentiation and dedifferentiation (Skoog and Miller, 1957), callus has been widely used in both basic research and industrial applications (George and Sherrington, 1984; Bourgaud et al....
[...]
...Generally speaking, an intermediate ratio of auxin and cytokinin promotes callus induction, while a high ratio of auxin-to-cytokinin or cytokinin-to-auxin induces root and shoot regeneration, respectively (Skoog and Miller, 1957)....
[...]
...…1939) and that the balance between two plant hormones, auxin and cytokinin, determines the state of differentiation and dedifferentiation (Skoog and Miller, 1957), callus has been widely used in both basic research and industrial applications (George and Sherrington, 1984; Bourgaud et…...
[...]

Journal Article•DOI•

Role of WUSCHEL in Regulating Stem Cell Fate in the Arabidopsis Shoot Meristem

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Klaus F. X. Mayer¹, Heiko Schoof¹, Achim Haecker¹, Michael Lenhard¹, Gerd Jürgens¹, Thomas Laux¹ - Show less +2 more•Institutions (1)

University of Tübingen¹

11 Dec 1998-Cell

TL;DR: It is shown that WUS encodes a novel homeodomain protein which presumably acts as a transcriptional regulator and suggests that stem cells in the shoot meristem are specified by an underlying cell group which is established in the 16-cell embryo and becomes localized to its prospective domain of function by asymmetric cell divisions.

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1,524 citations

"Plant Callus: Mechanisms of Inducti..." refers background in this paper

...The homeodomain-containing transcription factor WUSCHEL (WUS) is expressed in the stem cell organizing center of shoot meristems and is required to maintain stem cells in a relatively undifferentiated state (Laux et al., 1996; Mayer et al., 1998)....
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Journal Article•DOI•

Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection.

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Dirk Valvekens, Marc Van Montagu, Mieke Van Lijsebettens

01 Aug 1988-Proceedings of the National Academy of Sciences of the United States of America

TL;DR: A transformation procedure for Arabidopsis root explants based on kanamycin selection was established and an Agrobacterium tumor-inducing Ti plasmid carrying a chimeric neomycin phosphotransferase II gene (neo) was introduced, resulting in transformed seed-producing plants obtained with an efficiency between 20% and 80% within 3 months after gene transfer.

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Abstract: Culture conditions were developed that induce Arabidopsis thaliana (L.) Heynh. root cuttings to regenerate shoots rapidly and at 100% efficiency. The shoots produce viable seeds in vitro or after rooting in soil. A transformation procedure for Arabidopsis root explants based on kanamycin selection was established. By using this regeneration procedure and an Agrobacterium tumor-inducing Ti plasmid carrying a chimeric neomycin phosphotransferase II gene (neo), transformed seed-producing plants were obtained with an efficiency between 20% and 80% within 3 months after gene transfer. F(1) seedlings of these transformants showed Mendelian segregation of the kanamycin-resistance trait. The transformation method could be applied to three different Arabidopsis ecotypes. In addition to the neo gene, a chimeric bar gene conferring resistance to the herbicide Basta was introduced into Arabidopsis. The expression of the bar gene was shown by enzymatic assay.

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1,316 citations

"Plant Callus: Mechanisms of Inducti..." refers background in this paper

...In Arabidopsis, shoot or root explants incubated on auxin- and cytokinin-containing callus-inducing medium (CIM) form callus from pericycle cells adjacent to the xylem poles (Valvekens et al., 1988; Atta et al., 2009) (Figures 1B and 2A)....
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