Control of stem cell homeostasis via interlocking microRNA and microProtein feedback loops

Brandt, Ronny; Xie, Yakun; Musielak, Thomas J.; Graeff, Moritz; Stierhof, York‐Dieter; Huang, Hai; Liu, Chunming; Wenkel, Stephan

doi:10.1016/j.mod.2012.06.007

Cited by 26 publications

(18 citation statements)

References 31 publications

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“…5F, region III), relative to surrounding locations. ACT2 and ZPR3 were also tested as negative and positive controls, respectively (26,27), and validated our results. Together these data demonstrate that REV represses MIR165/166 directly via a previously characterized conserved cis-element (25).…”

Section: Hd-zipiis and Hd-zipiiis Repress Mir165/166 Expression Via Asupporting

confidence: 73%

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Regulation of MIR165/166 by class II and class III homeodomain leucine zipper proteins establishes leaf polarity

Merelo

Ram

Caggiano

et al. 2016

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

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109

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A defining feature of plant leaves is their flattened shape. This shape depends on an antagonism between the genes that specify adaxial (top) and abaxial (bottom) tissue identity; however, the molecular nature of this antagonism remains poorly understood. Class III homeodomain leucine zipper (HD-ZIP) transcription factors are key mediators in the regulation of adaxial-abaxial patterning. Their expression is restricted adaxially during early development by the abaxially expressed microRNA (MIR)165/166, yet the mechanism that restricts MIR165/166 expression to abaxial leaf tissues remains unknown. Here, we show that class III and class II HD-ZIP proteins act together to repress MIR165/166 via a conserved cis-element in their promoters. Organ morphology and tissue patterning in plants, therefore, depend on a bidirectional repressive circuit involving a set of miRNAs and its targets. T he morphogenesis of lateral organs in plants and animals is dependent on the specification of distinct cell types early in development. In particular, the correct patterning of adaxialabaxial tissues in plant organs such as leaves is critical for the generation of a lamina shape and the formation of a polar vascular system (1-4). Adaxial-abaxial cell-type patterning in turn depends on the restricted expression of several genes known to specify these cell types, including the class III homeodomain leucine zipper genes (HD-ZIPIIIs), KANADI genes, HD-ZIPIIs, and microRNA (MIR)165/166 (1, 2, 4-11). In general, genetic analyses have indicated that adaxial and abaxial factors act oppositely in organ patterning (1,2,4,(8)(9)(10)(11). Hence, loss-of-function mutations in genes promoting adaxial cell identity typically cause an abaxialized phenotype that correlates with the ectopic expression of abaxial genes, whereas loss-of-function mutations in abaxial genes produce an adaxialized phenotype that is accompanied by the expanded expression of adaxial genes. This antagonistic interaction between adaxial and abaxial factors may be mediated by mutually antagonistic regulation (12) or through opposing regulation of common targets (9, 13-16).A key set of transcription factors involved in plant organ polarity are the HD-ZIPIII proteins, such as REVOLUTA (REV), which specify adaxial cell fate (1, 2, 4, 17). The expression of these genes is restricted specifically to adaxial tissues via the action of two miRNA families, MIR165 and MIR166 (2, 7). In turn, the expression of these miRNAs is restricted to abaxial tissues and this restriction is essential for maintaining proper organ polarity (18).Here, we address the question of how MIR165/166 are regulated. We show that the HD-ZIPII proteins HAT3 and ATHB4 physically interact with HD-ZIPIII proteins and directly repress MIR165/166 expression via a conserved cis-element located in their promoters. This regulatory interaction largely accounts for HAT3 and ATHB4 function and reveals the molecular nature of a bidirectional repressive circuit essential to maintain balance between adaxial and abaxial tissue sp...

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Section: Hd-zipiis and Hd-zipiiis Repress Mir165/166 Expression Via Asupporting

confidence: 73%

“…Error bars show means ± SD of three biological replicates treated with 10 μM DEX (+DEX; yellow and blue bars) or mock (0.1% ethanol; −DEX; gray bars). ACT2 and ZPR3 were also tested as negative and positive controls, respectively (26,27). *P ≤ 0.05; **P ≤ 0.01.…”

Section: Hd-zipiis and Hd-zipiiis Repress Mir165/166 Expression Via Amentioning

confidence: 99%

Regulation of MIR165/166 by class II and class III homeodomain leucine zipper proteins establishes leaf polarity

Merelo

Ram

Caggiano

et al. 2016

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

Self Cite

109

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“…Accordingly, a mutual repressive relationship is known at least between PHB -like genes and miR165/166 whereas the regulatory relationship between PHB -like genes and FIL is yet to be elucidated. PHB -like genes repress miR165/166 activity by positively regulating AGO10 / PINHEAD [77], [78], by decreasing miR165/166 expression level via cytokinin signal [79] and possibly by activating tasiR-ARFs [25]. The activity of miR165/166 in turn represses the expression of PHB -like genes through mRNA cleavage [80] and DNA methylation [81].…”

Section: Discussionmentioning

confidence: 99%

Pattern Dynamics in Adaxial-Abaxial Specific Gene Expression Are Modulated by a Plastid Retrograde Signal during Arabidopsis thaliana Leaf Development

et al. 2013

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The maintenance and reformation of gene expression domains are the basis for the morphogenic processes of multicellular systems. In a leaf primordium of Arabidopsis thaliana, the expression of FILAMENTOUS FLOWER (FIL) and the activity of the microRNA miR165/166 are specific to the abaxial side. This miR165/166 activity restricts the target gene expression to the adaxial side. The adaxial and abaxial specific gene expressions are crucial for the wide expansion of leaf lamina. The FIL-expression and the miR165/166-free domains are almost mutually exclusive, and they have been considered to be maintained during leaf development. However, we found here that the position of the boundary between the two domains gradually shifts from the adaxial side to the abaxial side. The cell lineage analysis revealed that this boundary shifting was associated with a sequential gene expression switch from the FIL-expressing (miR165/166 active) to the miR165/166-free (non-FIL-expressing) states. Our genetic analyses using the enlarged fil expression domain2 (enf2) mutant and chemical treatment experiments revealed that impairment in the plastid (chloroplast) gene expression machinery retards this boundary shifting and inhibits the lamina expansion. Furthermore, these developmental effects caused by the abnormal plastids were not observed in the genomes uncoupled1 (gun1) mutant background. This study characterizes the dynamic nature of the adaxial-abaxial specification process in leaf primordia and reveals that the dynamic process is affected by the GUN1-dependent retrograde signal in response to the failure of plastid gene expression. These findings advance our understanding on the molecular mechanism linking the plastid function to the leaf morphogenic processes.

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“…The YABBY1/FILAMENTOUS FLOWER gene is one promising candidate because of its well-known role in polarity (Sarojam et al, 2010;Siegfried et al, 1999): as documented in Supporting Information Data S1, YAB1 is predicted to have high affinity for a site in the AGO7 proximal promoter but did not emerge as a hit from the Y1H screens. Surprisingly, we also did not recover the polarity factor REVOLUTA for the AGO10 promoter (Brandt et al, 2013); this likely represents a biological false negative. AGO1 is ubiquitously expressed (Lynn et al, 1999), and therefore expected to be under very robust transcriptional control which may be difficult to dissect.…”

Section: Discussionmentioning

confidence: 63%

Functional dissection of the ARGONAUTE7 promoter

et al. 2019

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ARGONAUTES are the central effector proteins of RNA silencing which bind target transcripts in a small RNA ‐guided manner. Arabidopsis thaliana has 10 ARGONAUTE ( AGO ) genes, with specialized roles in RNA ‐directed DNA methylation, post‐transcriptional gene silencing, and antiviral defense. To better understand specialization among AGO genes at the level of transcriptional regulation we tested a library of 1497 transcription factors for binding to the promoters of AGO 1 , AGO 10 , and AGO 7 using yeast 1‐hybrid assays. A ranked list of candidate DNA ‐binding TF s revealed binding of the AGO 7 promoter by a number of proteins in two families: the miR156‐regulated SPL family and the miR319‐regulated TCP family, both of which have roles in developmental timing and leaf morphology. Possible functions for SPL and TCP binding are unclear: we showed that these binding sites are not required for the polar expression pattern of AGO 7 , nor for the function of AGO 7 in leaf shape. Normal AGO 7 transcription levels and function appear to depend instead on an adjacent 124‐bp region. Progress in understanding the structure of this promoter may aid efforts to understand how the conserved AGO 7‐triggered TAS 3 pathway functions in timing and polarity.

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Control of stem cell homeostasis via interlocking microRNA and microProtein feedback loops

Cited by 26 publications

References 31 publications

Regulation of MIR165/166 by class II and class III homeodomain leucine zipper proteins establishes leaf polarity

Regulation of MIR165/166 by class II and class III homeodomain leucine zipper proteins establishes leaf polarity

Pattern Dynamics in Adaxial-Abaxial Specific Gene Expression Are Modulated by a Plastid Retrograde Signal during Arabidopsis thaliana Leaf Development

Functional dissection of the ARGONAUTE7 promoter

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