Transcriptional control of tissue formation throughout root development

Moreno-Risueño, Miguel A.; Sozzani, Rosangela; Yardımcı, Galip Gürkan; Petricka, Jalean J.; Vernoux, Teva; Blilou, Ikram; Alonso, José M.; Winter, Cara M.; Ohler, Uwe; Scheres, Ben; Benfey, Philip N.

doi:10.1126/science.aad1171

Cited by 139 publications

(147 citation statements)

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“…Second, we observed that SCR, JKD, BLJ, and SCZ could function as ground tissue lineage determinants during de novo root organogenesis. The combined action of BLJ, JKD, and SCR is required to maintain the ground tissue lineage postembryonically, and lacking these three factors results in missing ground tissue initializations (hence fewer ground tissue cell rows are observed in cross sections: Moreno-Risueno et al, 2015). We observed that de novo formed roots in blj-1 jkd-4 scr-4 and jkd-4 scz-1 mutants were missing ground tissue cell rows shortly after emergence, which indicates incorrect specification of ground tissue initials during primordia formation or later on in the course of development.…”

Section: Root Primordia Initiation and Patterningmentioning

confidence: 99%

“…In addition, WUSCHEL-RELATED HO-MEOBOX5 (WOX5) is confined by auxin signaling into the QC and represses differentiation of the stem cell niche, primarily from the QC (Sarkar et al, 2007;Forzani et al, 2014;Pi et al, 2015;Zhang et al, 2015). Tissue formation in the primary root meristem also requires lineage-specific factors that function as cell fate determinants and as tissue endogenous signaling factors to incorporate positional information into patterning (Moreno-Risueno et al, 2015). However, little is known about how tissues are formed de novo.…”

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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: Root Primordia Initiation and Patterningmentioning

confidence: 99%

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confidence: 99%

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

et al. 2017

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“…Unlike their animal counterparts, the postembryonic development of higher plants depends on the activity of apical meristems residing at each end of the body Sena et al, 2009;Moreno-Risueno et al, 2015). In the shoot apical meristem (SAM), pluripotent stem cells reside in a specialized microenvironment termed the stem cell niche, which gives rise to the aerial part of the plant (Aichinger et al, 2012;Zhou et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Type-B ARABIDOPSIS RESPONSE REGULATORs Specify the Shoot Stem Cell Niche by Dual Regulation of WUSCHEL

et al. 2017

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ORCID IDs: 0000-0003-3103-8629 (W.J.M.); 0000-0002-3129-5206 (X.S.Z.)Plants are known for their capacity to regenerate the whole body through de novo formation of apical meristems from a mass of proliferating cells named callus. Exogenous cytokinin and auxin determine cell fate for the establishment of the stem cell niche, which is the vital step of shoot regeneration, but the underlying mechanisms remain unclear. Here, we show that type-B ARABIDOPSIS RESPONSE REGULATORs (ARRs), critical components of cytokinin signaling, activate the transcription of WUSCHEL (WUS), which encodes a key regulator for maintaining stem cells. In parallel, type-B ARRs inhibit auxin accumulation by repressing the expression of YUCCAs, which encode a key enzyme for auxin biosynthesis, indirectly promoting WUS induction. Both pathways are essential for de novo regeneration of the shoot stem cell niche. In addition, the dual regulation of type-B ARRs on WUS transcription is required for the maintenance of the shoot apical meristem in planta. Thus, our results reveal a long-standing missing link between cytokinin signaling and WUS regulator, and the findings provide critical information for understanding cell fate specification.

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“…In addition, it provides a selective barrier for nutrients and acts as a major storage tissue in many plants (1)(2)(3). In Arabidopsis, an elaborate regulatory network has been established for the asymmetric divisions within the ground tissue that give rise to the two ground tissue cell types in the root: endodermis and cortex (4)(5)(6)(7)(8)(9)(10). This network revolves around the central transcriptional regulator SHORT-ROOT (SHR) that moves from the stele into the ground tissue where it is required in the nucleus to maintain endodermis identity and promote asymmetric division in the daughter cells of the ground tissue stem cells to generate separate endodermis and cortex layers (4)(5)(6)(7)(8)(9)(10).…”

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confidence: 99%

“…In Arabidopsis, an elaborate regulatory network has been established for the asymmetric divisions within the ground tissue that give rise to the two ground tissue cell types in the root: endodermis and cortex (4)(5)(6)(7)(8)(9)(10). This network revolves around the central transcriptional regulator SHORT-ROOT (SHR) that moves from the stele into the ground tissue where it is required in the nucleus to maintain endodermis identity and promote asymmetric division in the daughter cells of the ground tissue stem cells to generate separate endodermis and cortex layers (4)(5)(6)(7)(8)(9)(10). The nuclear retention of SHR depends on the activity of SCARECROW (SCR) and the BIRD family of transcription factors that are required to maintain ground tissue identity postembryonically (4,6,(8)(9)(10).…”

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confidence: 99%

Auxin response cell-autonomously controls ground tissue initiation in the early Arabidopsis embryo

Möller

Hove

Xiang

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Significance Higher plants are built from three major tissue types: epidermis, ground tissue, and vascular tissue. Each of these differentiates into several functionally distinct cell types. Although identity switches for the different cell types within the major three tissues have been identified, mechanisms that trigger the initiation of the three tissues themselves have remained obscure. Auxin response, in particular the auxin-dependent transcription factor MONOPTEROS (MP), plays a critical role in Arabidopsis embryonic root initiation. In our study, we identify a set of embryonic MP target genes and show that MP acts as a very first regulator of ground tissue initiation. Moreover, our data provide a framework for the simultaneous formation of multiple cell types by the same transcriptional regulator.

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Transcriptional control of tissue formation throughout root development

Cited by 139 publications

References 32 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

Type-B ARABIDOPSIS RESPONSE REGULATORs Specify the Shoot Stem Cell Niche by Dual Regulation of WUSCHEL

Auxin response cell-autonomously controls ground tissue initiation in the early Arabidopsis embryo

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