An organ boundary‐enriched gene regulatory network uncovers regulatory hierarchies underlying axillary meristem initiation

Tian, Caihuan; Zhang, Xiaoni; He, Jun; Yu, Haopeng; Wang, Ying; Shi, Bihai; Han, Yingying; Wang, Guoxun; Feng, Xiaoming; Zhang, Cui; Wang, Jin; Qi, Jiyan; Yu, Rong; Jiao, Yuling

doi:10.15252/msb.20145470

Cited by 115 publications

(126 citation statements)

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“…Genetic studies in Arabidopsis thaliana and other species have shown that AM initiation is regulated by several transcription factors, such as LATERAL SUPPRESSOR (LAS), REGULATOR OF AXILLARY MERISTEMS (RAX), and REVOLUTA (REV) (Talbert et al, 1995;Greb et al, 2003;Müller et al, 2006). Genetic and molecular studies revealed direct and indirect interactions among these genes in a regulatory network (Raman et al, 2008;Tian et al, 2014). WUS is expressed in the AM as in the SAM, but how WUS expression is established during AM initiation remains enigmatic.…”

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confidence: 99%

Cytokinin Signaling Activates WUSCHEL Expression during Axillary Meristem Initiation

et al. 2017

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The homeodomain transcription factor WUSCHEL (WUS) defines the shoot stem cell niche, but the mechanisms underlying the establishment of WUS expression remain unclear. Here, we show that cytokinin signaling precedes WUS expression in leaf axils and activates WUS expression de novo in the leaf axil to promote axillary meristem initiation. Furthermore, type-B Arabidopsis response regulator proteins, which are transcriptional activators in the cytokinin signaling pathway, directly bind to the WUS promoter and activate its expression. Finally, we show that cytokinin activation of WUS in the leaf axil correlates with increased histone acetylation and methylation markers associated with transcriptional activation, supporting the fact that WUS expression requires a permissive epigenetic environment to restrict it to highly defined meristematic tissues. Taken together, these findings explain how cytokinin regulates axillary meristem initiation and establish a mechanistic framework for the postembryonic establishment of the shoot stem cell niche.

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Section: Introductionmentioning

confidence: 99%

Cytokinin Signaling Activates WUSCHEL Expression during Axillary Meristem Initiation

et al. 2017

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“…This process, known as floral evocation, results in new patterns of growth at the shoot apex, including production of flowers, and an increase in stem elongation, called bolting. Lateral organ boundaries are specialized domains of restricted growth that separate meristem and organ compartments and produce axillary meristems (for review, see Aida and Tasaka, 2006;Tian et al, 2014). Early in the transition to flowering, the IM produces cauline leaves and axillary meristems that develop as secondary inflorescences.…”

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Repression of lateral organ boundary genes by PENNYWISE and POUND-FOOLISH is essential for meristem maintenance and flowering in Arabidopsis thaliana1

et al. 2015

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ORCID IDs: 0000-0002-0050-4001 (B.C.S.); 0000-0002-3526-7982 (J.L.); 0000-0001-7896-6049 (M.P.); 0000-0001-7144-1274 (D.X.); 0000-0001-5026-095X (S.Ci.); 0000-0002-6496-3792 (S.R.H.); 0000-0003-1808-5172 (V.P.).In the model plant Arabidopsis (Arabidopsis thaliana), endogenous and environmental signals acting on the shoot apical meristem cause acquisition of inflorescence meristem fate. This results in changed patterns of aerial development seen as the transition from making leaves to the production of flowers separated by elongated internodes. Two related BEL1-like homeobox genes, PENNYWISE (PNY) and POUND-FOOLISH (PNF), fulfill this transition. Loss of function of these genes impairs stem cell maintenance and blocks internode elongation and flowering. We show here that pny pnf apices misexpress lateral organ boundary genes BLADE-ON-PETIOLE1/2 (BOP1/2) and KNOTTED-LIKE FROM ARABIDOPSIS THALIANA6 (KNAT6) together with ARABIDOPSIS THALIANA HOMEOBOX GENE1 (ATH1). Inactivation of genes in this module fully rescues pny pnf defects. We further show that BOP1 directly activates ATH1, whereas activation of KNAT6 is indirect. The pny pnf restoration correlates with renewed accumulation of transcripts conferring floral meristem identity, including FD, SQUAMOSA PROMOTER-BINDING PROTEIN LIKE genes, LEAFY, and APETALA1. To gain insight into how this module blocks flowering, we analyzed the transcriptome of BOP1-overexpressing plants. Our data suggest a central role for the microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE-microRNA172 module in integrating stress signals conferred in part by promotion of jasmonic acid biosynthesis. These data reveal a potential mechanism by which repression of lateral organ boundary genes by PNY-PNF is essential for flowering.Plant development relies on the activity of the shoot apical meristem (SAM) as a continuous source of founder cells for production of new leaves, shoots, and internodes throughout the life cycle (for review, see Aichinger et al., 2012). A tight balance between the allocation of cells to developing primordia and the perpetuation of pluripotent stem cells in the central zone maintains the SAM at a constant size. In Arabidopsis (Arabidopsis thaliana), the vegetative SAM produces leaves in a spiral phyllotaxy with dormant axillary meristems. In conjunction, internode elongation is repressed, resulting in a basal rosette. The transition to flowering is governed by internal and external signals that converge at the SAM to promote acquisition of inflorescence meristem (IM) fate (for review, see Amasino and Michaels, 2010;Srikanth and Schmid, 2011;Andrés and Coupland, 2012). This process, known as floral evocation, results in new patterns of growth at the shoot apex, including production of flowers, and an increase in stem elongation, called bolting. Lateral organ boundaries are specialized domains of restricted growth that separate meristem and organ compartments and produce axillary meristems (for review, see Aida and Tasaka, 2006;Tian et al., 2014). Early in the transition t...

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“…52,46 Among those are ANT, CLF, AS1, AS2 that are expressed mainly in the growing organ and, CUC1, 2 and 3, the expression of which is restricted to the boundary domain. 43,46,52,54 The pattern of stress anisotropy is represented by color bar with green corresponding to the regions with lower stress anisotropy (central zone and organ) and orange in the boundary domain where stress anisotropy is maximal. This stress and gene expression pattern correlates with the distribution of the plant hormone auxin that has its local maximum where new organ initiates and its local minimum at the organ boundary.…”

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Interplay between miRNA regulation and mechanical stress forCUCgene expression at the shoot apical meristem

Fal

Landrein

Hamant

2016

Plant Signaling & Behavior

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The shoot apical meristem is the central organizer of plant aerial organogenesis. The molecular bases of its functions involve several cross-talks between transcription factors, hormones and microRNAs. We recently showed that the expression of the homeobox transcription factor STM is induced by mechanical perturbations, adding another layer of complexity to this regulation. Here we provide additional evidence that mechanical perturbations impact the promoter activity of CUC3, an important regulator of boundary formation at the shoot meristem. Interestingly, we did not detect such an effect for CUC1. This suggests that the robustness of expression patterns and developmental programs is controlled via a combined action of molecular factors as well as mechanical cues in the shoot apical meristem. KEYWORDSCUC genes; mechanical stress; Meristem; micro-RNAs Throughout their lifetime, plants are exposed to a number of external mechanical perturbations, such as wind or touch. This leads to changes in mRNA level of many genes, and long-term developmental responses such as stem thickening and flowering delay 5 In addition to these external factors, plants are also constantly affected by intrinsic tensile stresses, notably because plant cells are under high turgor pressure. There is now accumulating evidence that these internal stresses are affecting many aspects of the cells, thus channeling growth in the long term.14 The shoot apical meristem (SAM) is the central organizer of plant aerial organogenesis. Initiation of new organs and maintenance of SAM is achieved through the concomitant action of multiple regulatory pathways. Genetic screens have identified many key players, including transcription factors, hormones, and microRNAs. 38,48,53,55 In addition to these biochemical factors, mechanical forces are also present within the meristem. In particular, the boundary domain that separates newly emerging organ from the meristem is under highly anisotropic tensile stresses. 4,15,32 A key question for the future is the analysis of the interplay between mechanical forces and the molecular regulators of meristem function (Fig. 1A).In a recent article, 26 we showed that a master regulator of meristem maintenance, the homeodomain protein SHOOT MERISTEMLESS (STM) is expressed at a higher level in the boundary domain, and that this local increase in promoter activity can be related to mechanical stress: mechanical perturbations are sufficient to induce STM expression in the meristem. Interestingly, mechanical perturbations do not affect all boundary-expressed genes in the same way. For instance, the promoter activity of the PINOID gene, which is also increased in the boundary domain, is not affected by mechanical perturbations. 26Here we focus on the most canonical genetic markers of boundary identity, the CUP SHAPED COTYLEDON (CUC) genes. CUC1, CUC2 and CUC3, belong to a group of NAC domain transcription factors and show a high level of functional redundancy. They play an essential role in shoot meristem initiation throug...

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An organ boundary‐enriched gene regulatory network uncovers regulatory hierarchies underlying axillary meristem initiation

Cited by 115 publications

References 87 publications

Cytokinin Signaling Activates WUSCHEL Expression during Axillary Meristem Initiation

Cytokinin Signaling Activates WUSCHEL Expression during Axillary Meristem Initiation

Repression of lateral organ boundary genes by PENNYWISE and POUND-FOOLISH is essential for meristem maintenance and flowering in Arabidopsis thaliana1

Interplay between miRNA regulation and mechanical stress forCUCgene expression at the shoot apical meristem

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