A high-resolution gene expression map of the<i>Arabidopsis</i>shoot meristem stem cell niche

Yadav, Ram Kishor; Tavakkoli, Montreh; Xie, Mingtang; Girke, Thomas; Reddy, G. Venugopala

doi:10.1242/dev.106104

Cited by 113 publications

(118 citation statements)

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“…Most studies have been focused on the cross-talk between phytohormones, such as auxin and cytokinin, and gene expression in these processes (25,26). Little is known whether, and if so how, external signals like light and temperature contribute to meristem regulation.…”

Section: Discussionmentioning

confidence: 99%

FAR-RED ELONGATED HYPOCOTYL3 activates SEPALLATA2 but inhibits CLAVATA3 to regulate meristem determinacy and maintenance in Arabidopsis

Guo

et al. 2016

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

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Plant meristems are responsible for the generation of all plant tissues and organs. Here we show that the transcription factor (TF) FAR-RED ELONGATED HYPOCOTYL3 (FHY3) plays an important role in both floral meristem (FM) determinacy and shoot apical meristem maintenance in Arabidopsis, in addition to its well-known multifaceted roles in plant growth and development during the vegetative stage. Through genetic analyses, we show that WUSCHEL (WUS) and CLAVATA3 (CLV3), two central players in the establishment and maintenance of meristems, are epistatic to FHY3. Using genome-wide ChIP-seq and RNA-seq data, we identify hundreds of FHY3 target genes in flowers and find that FHY3 mainly acts as a transcriptional repressor in flower development, in contrast to its transcriptional activator role in seedlings. Binding motif-enrichment analyses indicate that FHY3 may coregulate flower development with three flowerspecific MADS-domain TFs and four basic helix-loop-helix TFs that are involved in photomorphogenesis. We further demonstrate that CLV3, SEPALLATA1 (SEP1), and SEP2 are FHY3 target genes. In shoot apical meristem, FHY3 directly represses CLV3, which consequently regulates WUS to maintain the stem cell pool. Intriguingly, CLV3 expression did not change significantly in fhy3 and phytochrome B mutants before and after light treatment, indicating that FHY3 and phytochrome B are involved in light-regulated meristem activity. In FM, FHY3 directly represses CLV3, but activates SEP2, to ultimately promote FM determinacy. Taken together, our results reveal insights into the mechanisms of meristem maintenance and determinacy, and illustrate how the roles of a single TF may vary in different organs and developmental stages. meristem maintenance | meristem determinacy | FHY3 | CLV3 | SEP2 P lant meristems are responsible for the generation of all plant tissues and organs. Unlike the shoot apical meristem (SAM), whose activity is maintained throughout the life of plants, the floral meristem (FM) is precisely programmed to terminate in a process known as FM determinacy (1). WUSCHEL (WUS) plays a central role in the establishment and maintenance of SAM, inflorescence meristem, and FM, as well as in FM determinacy (2-4). WUS is expressed in the organizing center located beneath the stem cells in the meristem to promote cell proliferation by maintaining stem cell potential (2). The WUS/CLAVATA3 (CLV3) signaling pathway maintains the stabilization of meristem size and the stem cell pool (3, 5). Consistent with WUS overactivation, clv3 mutants have an enlarged SAM and increased numbers of floral organs and whorls (5). In addition to the WUS/CLV3 loop, several other pathways are known to regulate FM determinacy (4). AGAMOUS (AG) encodes a MADS-box transcription factor (TF) and is the lynchpin of the FM determinacy network (4, 6, 7). In the null ag-1 mutant, FM determinacy is severely impaired, resulting in a flower-in-flower phenotype (6). AG inhibits WUS expression through both indirect and direct means (8, 9). A number of other gene...

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Section: Discussionmentioning

confidence: 99%

FAR-RED ELONGATED HYPOCOTYL3 activates SEPALLATA2 but inhibits CLAVATA3 to regulate meristem determinacy and maintenance in Arabidopsis

Guo

et al. 2016

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

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“…Furthermore, KAN proteins are excluded from the P0, which is defined by high levels of the KAN1-repressed target PIN1, and instead accumulate in a ring below initiating organs (Merelo et al, 2013;Yadav et al, 2014).…”

Section: Further Roles For As1-as2 In Adaxial-abaxial Patterningmentioning

confidence: 99%

“…The exclusion of KAN proteins from the P0 allows the nonpolar accumulation of AS1-AS2 and the initial nucleation of PRC2-mediated H3K27me3 at the promoter of MIR166A on both sides of the primordium. As the primordium develops, KAN expression extends into its abaxial side (Yadav et al, 2014), directly repressing AS2 expression and restricting further deposition of H3K27me3 at MIR166A solely to the adaxial side. This polarizes the production of mature miR166 and consequently limits HD-ZIPIII accumulation to the adaxial side.…”

Section: Further Roles For As1-as2 In Adaxial-abaxial Patterningmentioning

confidence: 99%

The ASYMMETRIC LEAVES Complex Employs Multiple Modes of Regulation to Affect Adaxial-Abaxial Patterning and Leaf Complexity

et al. 2015

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Flattened leaf architecture is not a default state but depends on positional information to precisely coordinate patterns of cell division in the growing primordium. This information is provided, in part, by the boundary between the adaxial (top) and abaxial (bottom) domains of the leaf, which are specified via an intricate gene regulatory network whose precise circuitry remains poorly defined. Here, we examined the contribution of the ASYMMETRIC LEAVES (AS) pathway to adaxial-abaxial patterning in Arabidopsis thaliana and demonstrate that AS1-AS2 affects this process via multiple, distinct regulatory mechanisms. AS1-AS2 uses Polycomb-dependent and -independent mechanisms to directly repress the abaxial determinants MIR166A, YABBY5, and AUXIN RESPONSE FACTOR3 (ARF3), as well as a nonrepressive mechanism in the regulation of the adaxial determinant TAS3A. These regulatory interactions, together with data from prior studies, lead to a model in which the sequential polarization of determinants, including AS1-AS2, explains the establishment and maintenance of adaxial-abaxial leaf polarity. Moreover, our analyses show that the shared repression of ARF3 by the AS and trans-acting small interfering RNA (ta-siRNA) pathways intersects with additional AS1-AS2 targets to affect multiple nodes in leaf development, impacting polarity as well as leaf complexity. These data illustrate the surprisingly multifaceted contribution of AS1-AS2 to leaf development showing that, in conjunction with the ta-siRNA pathway, AS1-AS2 keeps the Arabidopsis leaf both flat and simple.

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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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confidence: 99%

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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A high-resolution gene expression map of theArabidopsisshoot meristem stem cell niche

Cited by 113 publications

References 85 publications

FAR-RED ELONGATED HYPOCOTYL3 activates SEPALLATA2 but inhibits CLAVATA3 to regulate meristem determinacy and maintenance in Arabidopsis

FAR-RED ELONGATED HYPOCOTYL3 activates SEPALLATA2 but inhibits CLAVATA3 to regulate meristem determinacy and maintenance in Arabidopsis

The ASYMMETRIC LEAVES Complex Employs Multiple Modes of Regulation to Affect Adaxial-Abaxial Patterning and Leaf Complexity

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

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