Plant regeneration: cellular origins and molecular mechanisms

Ikeuchi, Momoko; Ogawa, Yoichi; Iwase, Akira; Sugimoto, Keiko

doi:10.1242/dev.134668

Cited by 403 publications

(351 citation statements)

References 126 publications

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“…Plant regeneration through de novo organogenesis can be achieved through hormonal induction, directly or indirectly (Ikeuchi et al, 2013), but also in hormone free medium. The molecular pathways involved (Ikeuchi et al, 2016;Kareem et al, 2016) and the relationship between hormonal-induced and endogenous programs are not well understood. Moreover, callus formation, which is a prerequisite for hormonal-induced regeneration, does not appear to occur during endogenous organogenesis, although both processes share regulation (Sugimoto et al, 2010;Liu et al, 2014;Perianez-Rodriguez et al, 2014;Ramirez-Parra et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

Regulation of Hormonal Control, Cell Reprogramming, and Patterning during De Novo Root Organogenesis

et al. 2017

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Body regeneration through formation of new organs is a major question in developmental biology. We investigated de novo root formation using whole leaves of Arabidopsis (Arabidopsis thaliana). Our results show that local cytokinin biosynthesis and auxin biosynthesis in the leaf blade followed by auxin long-distance transport to the petiole leads to proliferation of J0121-marked xylem-associated tissues and others through signaling of INDOLE-3-ACETIC ACID INDUCIBLE28 (IAA28), CRANE (IAA18), WOODEN LEG, and ARABIDOPSIS RESPONSE REGULATORS1 (ARR1), ARR10, and ARR12. Vasculature proliferation also involves the cell cycle regulator KIP-RELATED PROTEIN2 and ABERRANT LATERAL ROOT FORMATION4, resulting in a mass of cells with rooting competence that resembles callus formation. Endogenous callus formation precedes specification of postembryonic root founder cells, from which roots are initiated through the activity of SHORT-ROOT, PLETHORA1 (PLT1), and PLT2. Primordia initiation is blocked in shr plt1 plt2 mutant. Stem cell regulators SCHIZORIZA, JACKDAW, BLUEJAY, and SCARECROW also participate in root initiation and are required to pattern the new organ, as mutants show disorganized and reduced number of layers and tissue initials resulting in reduced rooting. Our work provides an organ regeneration model through de novo root formation, stating key stages and the primary pathways involved.Plants have striking regeneration capacities, and can produce new organs from postembryonic tissues (Hartmann et al., 2010;Chen et al., 2014;Liu et al., 2014) as well as reconstitute damaged organs upon wounding (Xu et al., 2006;Heyman et al., 2013; PerianezRodriguez et al., 2014;Melnyk et al., 2015;Efroni et al., 2016). Intriguingly, root regeneration upon stem cell damage recruits embryonic pathways (Hayashi et al., 2006;Efroni et al., 2016), whereas in contrast, postembryonic formation of whole new organs, such as lateral roots, appears to use specific postembryonic pathways (Lavenus et al., 2013).Cross talk between auxin and cytokinin signaling is required for many aspects of plant development and regeneration (El-Showk et al., 2013), although how their synergistic interaction is implemented at the molecular level has not been clarified (Skoog and Miller, 1957;Chandler and Werr, 2015). Exogenous in vitro supplementation of these two hormones results in continuous cell proliferation, to form a characteristic structure termed "callus". Callus emerges as a common regenerative mechanism for almost all plant organs through in vitro culture (Atta et al., 2009;Sugimoto et al., 2010). There is increasing evidence that callus formation requires hormone-mediated activation of a lateral and meristematic root development program in pericycle-like cells defined by expression of the J0121 marker 1 This work was supported by grants from Ministerio de Economía y Competitividad (MINECO) of Spain, the European Regional Development Fund (ERDF) and FP7 Funds of the European Commission, BFU2013-41160-P, BFU2016-80315-P, and PCIG11-GA-2012-322082 to M.A....

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Section: Discussionmentioning

confidence: 99%

Regulation of Hormonal Control, Cell Reprogramming, and Patterning during De Novo Root Organogenesis

et al. 2017

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“…Plants, in particular, maintain high developmental plasticity during postembryonic development and display diverse forms of regeneration (Ikeuchi et al, 2016). One common example of plant regeneration is de novo organogenesis, i.e., the formation of new organs such as shoots and roots, from cut sites.…”

Section: Introductionmentioning

confidence: 99%

“…As in animals, plant regeneration is initiated by at least two cellular mechanisms. One is by the reactivation of relatively undifferentiated cells existing in the somatic tissue and the other is by the reprogramming of mature somatic cells (Birnbaum and Sánchez Alvarado, 2008;Tanaka and Reddien, 2011;Ikeuchi et al, 2016). In some cases, these initiating cells directly regenerate new organs, but in other cases they first develop callus, a mass of dividing cells, from which new organs form (Hicks, 1994).…”

Section: Introductionmentioning

confidence: 99%

“…Given that CIM-induced callus possesses root meristem-like properties, regenerating roots after transfer to root-inducing medium might be relatively straightforward, requiring further establishment of root meristem identity and execution of root developmental program by an auxin-induced transcriptional cascade (Ozawa et al, 1998;Che et al, 2002;Ikeuchi et al, 2016). By contrast, shoot regeneration on SIM ought to be more complex as it requires the conversion of root meristem fate into shoot meristem fate.…”

Section: Introductionmentioning

confidence: 99%

“…Importantly, WIND1 substitutes the early wound response and confers pluripotency, since plants overexpressing WIND1 regenerate shoots on SIM without wound stress (Iwase et al, 2015). Conversely, dominant repression of WIND1 in WIND1-SRDX explants strongly blocks shoot regeneration, suggesting that WIND proteins function as key regulators of cellular reprogramming in response to wound stress (Iwase et al, 2015;Ikeuchi et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

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WIND1 Promotes Shoot Regeneration through Transcriptional Activation of ENHANCER OF SHOOT REGENERATION1 in Arabidopsis

et al. 2016

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Many plant species display remarkable developmental plasticity and regenerate new organs after injury. Local signals produced by wounding are thought to trigger organ regeneration but molecular mechanisms underlying this control remain largely unknown. We previously identified an AP2/ERF transcription factor WOUND INDUCED DEDIFFERENTIATION1 (WIND1) as a central regulator of wound-induced cellular reprogramming in plants. In this study, we demonstrate that WIND1 promotes callus formation and shoot regeneration by upregulating the expression of the ENHANCER OF SHOOT REGENERATION1 (ESR1) gene, which encodes another AP2/ERF transcription factor in Arabidopsis thaliana. The esr1 mutants are defective in callus formation and shoot regeneration; conversely, its overexpression promotes both of these processes, indicating that ESR1 functions as a critical driver of cellular reprogramming. Our data show that WIND1 directly binds the vascular system-specific and wound-responsive cis-element-like motifs within the ESR1 promoter and activates its expression. The expression of ESR1 is strongly reduced in WIND1-SRDX dominant repressors, and ectopic overexpression of ESR1 bypasses defects in callus formation and shoot regeneration in WIND1-SRDX plants, supporting the notion that ESR1 acts downstream of WIND1. Together, our findings uncover a key molecular pathway that links wound signaling to shoot regeneration in plants.

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Molecular Aspects of Grafting in Woody Plants

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Tedesco

Fevereiro

2021

Annual Plant Reviews Online

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Grafting is an ancient technique especially used in horticulture and in orchards as a tool for plant propagation and improvement. Although grafting has brought incredible benefits to agriculture and is being used worldwide in the cultivation of almost every fruit tree, the mechanisms, and pathways driving the formation or the incompatibilities of graft unions are still largely unknown. Recently, the potential of grafting has resurfaced in the literature and molecular approaches are currently contributing to the understanding of graft union formation and the phenomenon of scion–rootstock graft incompatibility. This work focuses on the cellular and molecular mechanisms of graft formation in woody plants, highlighting the identified regulators of this process in molecular terms. We review how the healing of the union proceeds in incompatible grafts, the challenge of phenotyping graft incompatibility, and the detection methods developed for its prediction. In the pursuit of finding sustainable solutions for agriculture, while faced with the alarming predictions of climate changes, grafting is being revaluated as a new biotechnological tool. Therefore, some examples of how we can broaden the scope of useful grafting applications, exploit biodiversity in a unique chimeric plant, and manipulate phenotypic traits by delivering proteins and RNAs across graft unions, are also discussed. Research in this field still has a long way to go before the exciting prospect of deliberately combining multiple plant traits becomes reality.

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Plant regeneration: cellular origins and molecular mechanisms

Cited by 403 publications

References 126 publications

Regulation of Hormonal Control, Cell Reprogramming, and Patterning during De Novo Root Organogenesis

Regulation of Hormonal Control, Cell Reprogramming, and Patterning during De Novo Root Organogenesis

WIND1 Promotes Shoot Regeneration through Transcriptional Activation of ENHANCER OF SHOOT REGENERATION1 in Arabidopsis

Molecular Aspects of Grafting in Woody Plants

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