PLETHORA Genes Control Regeneration by a Two-Step Mechanism

Kareem, Abdul; Durgaprasad, Kavya; Sugimoto, Keiko; Du, Yujuan; Pulianmackal, Ajai J.; Trivedi, Zankhana B.; Abhayadev, Pazhoor V.; Pinon, Violaine; Meyerowitz, Elliot M.; Scheres, Ben; Prasad, Kalika

doi:10.1016/j.cub.2015.02.022

Cited by 245 publications

(323 citation statements)

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“…We also confirmed the previously reported upregulation of PLT1, 2, 3, 5, and 7 and CUC2 in explants cultured on CIM (Kareem et al, 2015) but found that none of their activation requires functional ESR1 ( Figure 7B). …”

Section: The Wind1-esr1 Pathway Is Required For Shoot Regeneration Insupporting

confidence: 92%

“…Accordingly, many regulators of lateral root development, including ABERRANT LAT-ERAL ROOT4, AUXIN RESPONSE FACTOR7 (ARF7), ARF19, LATERAL ORGAN BOUNDARIES DOMAIN16 (LBD16), LBD17, LBD18, and LBD29, are required for callus formation on CIM (Sugimoto et al, 2010, Fan et al, 2012, Ikeuchi et al, 2013. A recent study has demonstrated that additional regulators, PLETHORA3 (PLT3), PLT5, and PLT7, are also needed to make CIM-induced callus pluripotent (Kareem et al, 2015). Key players acting downstream of PLT3, PLT5, and PLT7 to confer pluripotency are PLT1 and PLT2, which are also known for their role in root meristem development (Aida et al, 2004;Galinha et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

“…Key players acting downstream of PLT3, PLT5, and PLT7 to confer pluripotency are PLT1 and PLT2, which are also known for their role in root meristem development (Aida et al, 2004;Galinha et al, 2007). PLT3, PLT5, and PLT7, in addition, induce CUP SHAPED COT-YLEDON1 (CUC1) and CUC2, important regulators of shoot meristem development during embryogenesis (Aida et al, 1997(Aida et al, , 1999, presumably to introduce the potential to form shoots in the callus (Kareem et al, 2015). While CUC1 and CUC2 do not show an organized pattern of expression in CIM-induced callus, some root meristem regulators, such as WUSCHEL-RELATED HOMEO-BOX5 (WOX5) and SCARECROW, display expression patterns similar to those observed in the root meristem (Gordon et al, 2007;Atta et al, 2009;Sugimoto et al, 2010).…”

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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Section: The Wind1-esr1 Pathway Is Required For Shoot Regeneration Insupporting

confidence: 92%

Section: Introductionmentioning

confidence: 99%

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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“…These results indicate that additional reprogramming processes are required. PLT1 and PLT2 have been shown to be required to establish pluripotency during de novo shoot regeneration (Kareem et al, 2015). Our results show that during de novo root formation, PLT1 and PLT2, in combination with SHR, could also be involved in specification of root founder cells, which are pluripotent.…”

Section: Specification Of Root Founder Cellsmentioning

confidence: 62%

“…In addition, persistent expression of PLT1, PLT2, and SHR appears to be necessary during subsequent formative stages to maintain primordia growth, as the very primordia found in shr-2 plt1-4 plt2-2 quickly differentiate. In contrast, in the de novo shoot regeneration system, transient induction of PLT2 has been shown to be sufficient to specify shoot progenitors, whereas subsequent expression of other regulators is required to accomplish de novo shoot formation from these progenitors (Kareem et al, 2015).…”

Section: Specification Of Root Founder Cellsmentioning

confidence: 97%

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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Pericycle

Dubrovsky

Rost

2023

Encyclopedia of Life Sciences

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Pericycle is a primary tissue of plant roots with meristematic properties and is the site for the initiation of lateral roots and two secondary meristems, the vascular cambium and phellogen (cork cambium). Pericycle pluripotent cell properties are also revealed during cultivation of root explants in shoot regeneration media. In this article, the characteristics of the pericycle related to each of its functions are reviewed. During lateral root development, five important and coordinated events take place in the pericycle: founder cell identity acquisition, cell division competence, asymmetric cell division, new organ growth axis establishment and lateral inhibition. Cellular and molecular bases of these processes as well as transcriptomic insights in pericycle cell identity are discussed. Cell cycle and related genetic control in pericycle development are also addressed. Cellular and molecular bases of participation of pericycle in the formation of lateral meristems, vascular cambium and phellogen (cork cambium), differences among eudicots and monocots in pericycle development, as well as participation of pericycle in loading of mineral nutrients and unloading of organic compounds are also reviewed. Key Concepts The pericycle is a primary tissue with pluripotent properties that participates in lateral root (LR) formation. In eudicots, it also gives rise to two lateral meristems: vascular cambium and cork cambium (phellogen). Pericycle is typical of plant roots and is the most external cell layer (or layers) of the vascular cylinder. In other plant organs, pericycle or pericycle‐like cell layers can also be present depending on taxon. Outside the root apical meristem, in the root differentiation zone of eudicots, the xylem pole pericycle (XPP) maintains its proliferation activity. Due to its proliferation activity, pericycle possesses high regenerative properties involved in regeneration of shoots from roots. The XPP and phloem pole pericycle (PPP) are characterised by distinct transcriptomic profiles related to their adjacent vascular tissues. Pericycle cells committed for LR development in monocots and eudicots retain the common features related to cell cycle, active auxin synthesis, transport and signalling, and responsiveness to nitrates. LR formation starts from pericycle founder cell specification which is auxin dependent and implies drastic developmental changes in genetic programs involved in asymmetric cell division, new organ growth axis establishment and lateral inhibition. The first founder cell specification is followed by the recruitment of neighbouring pericycle cells that leads to the formation of a morphogenetic field of founder cells giving rise to a LR. The transition from primary to secondary growth starts in the pericycle and procambium and leads to the formation of vascular cambium and phellogen which are coordinated processes dependent on auxin and cytokinin. Pericycle maintains high metabolic activity and participates in loading phloem and xylem and in unloading phloem and thus is involved in shoot‐to‐root and root‐to‐shoot long‐distance transport.

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PLETHORA Genes Control Regeneration by a Two-Step Mechanism

Cited by 245 publications

References 44 publications

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

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

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

Pericycle

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