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

Husbands, Aman Y.; Benkovics, Anna Hangyáné; Nogueira, Fábio Tebaldi Silveira; Lodha, Mukesh; Timmermans, Marja C.P.

doi:10.1105/tpc.15.00454

Cited by 74 publications

(75 citation statements)

References 65 publications

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“…In addition to REV, HAT3, and ATHB4, another factor recently shown to repress MIR166a is the adaxial transcription factor ASSYMETRIC LEAVES 2 (AS2). However, this regulation occurs at later stages of leaf development via a binding site located further upstream of the cis-element reported here (28). In turn, AS2 is directly repressed by the abaxial factor KANADI1 (12), and KAN1 together with KAN2 help repress HD-ZIPIII expression (1).…”

Section: Combinations (Simentioning

confidence: 84%

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.

103

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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: Combinations (Simentioning

confidence: 84%

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.

103

View full text Add to dashboard Cite

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“…This regulatory interaction can explain the dynamic pattern of AS2 expression, which transitions from uniform to adaxialized as the incipient leaf grows out ( Fig. 6; Iwakawa et al, 2007;Husbands et al, 2015). The interaction between KAN1 and AS2 thus .…”

Section: Cellular Properties Of the Adaxial-abaxial Polarity Networkmentioning

confidence: 91%

“…5; see Husbands et al, 2009 for more details on individual polarity determinants). In Arabidopsis, the LOB domain transcription factor ASYMMETRIC LEAVES2 (AS2) acts in a complex with the PHAN ortholog AS1 to promote adaxial identity (Lin et al, 2003;Iwakawa et al, 2007;Husbands et al, 2015). In addition, members of the CLASS III HOMEODOMAIN-LEUCINE ZIPPER (HD-ZIPIII) family, which in Arabidopsis includes PHABULOSA (PHB), PHAVOLUTA (PHV) and REVOLUTA (REV), specify adaxial fate (McConnell et al, 2001;Emery et al, 2003;Juarez et al, 2004a;Itoh et al, 2008).…”

Section: The Molecular Genetics Of Leaf Polaritymentioning

confidence: 99%

“…AS1-AS2 also binds the promoters of ARF3 and the tasiARF precursor TAS3A. Interestingly, at TAS3A, AS1-AS2 appears to use a 'protective mechanism' to prevent downregulation of TAS3A expression by abaxial determinants, most likely ARF3 and KAN1 (Husbands et al, 2015). Indeed, to attain a clean separation of adaxial and abaxial fates, the polarity network must also include positive regulatory interactions that reinforce cell identity (Fig.…”

Section: Cellular Properties Of the Adaxial-abaxial Polarity Networkmentioning

confidence: 99%

“…The dumbbell denotes protein-protein interaction. Reprinted with permission from Husbands et al (2015).…”

Section: Hierarchical and Sequential Signaling Characterizes Adaxialamentioning

confidence: 99%

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The differentiation of a leaf -from its inception as a semicircular bulge on the surface of the shoot apical meristem into a flattened structure with specialized upper and lower surfaces -is one of the most intensely studied processes in plant developmental biology. The large body of contemporary data on leaf dorsiventrality has its origin in the pioneering experiments of Ian Sussex, who carried out these studies as a PhD student in the early 1950s. Here, we review his original experiments in their historical context and describe our current understanding of this surprisingly complex process. Finally, we postulate possible candidates for the 'Sussex signal' -the elusive meristem-derived factor that first ignited interest in this important developmental problem.

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Development in plants is a continuous process during which new tissues and organs are formed all along its life cycle. Development involves the coordination of both time and space of complex cellular processes such as proliferation, expansion and differentiation following endogenous programmes and in response to environmental signals. Since their discovery in 2002, plant microRNAs (miRNAs), a class of small single‐stranded regulatory ribonucleic acids (RNAs) have emerged as important nodes in regulatory networks controlling plant development. For instance, miRNAs play important roles for cell fate determination during the patterning of organs and contribute to the regulation of their growth. In addition, miRNAs integrate different signals to regulate the life cycle of plants. Finally, miRNAs appear as molecular links between environmental signals and plant development and may constitute levers to modify plant development in crops. Key Concepts miRNAs are essential for plant development as mutants affecting miRNA biogenesis or function are embryo lethal or show severe pleiotropic defects. miRNA precursors are mostly produced from independent genetic units and are processed into mature miRNAs via a complex core machinery. miRNAs can have different effects on the expression of their target genes, controlling their spatial pattern, their level of expression or the timing of their expression. miRNAs are regulating many different developmental processes, including pattern formation, morphogenesis and differentiation at all stages of a plant's life. Most of the miRNAs regulating plant development are evolutionary conserved and target evolutionary conserved transcription factors. miRNAs can act non‐cell‐autonomously, generating a mobile signal that contributes to pattern formation through the regulation of the expression pattern of their targets. miRNAs are integrated into complex regulatory networks and their expression is regulated by both endogenous and exogenous signals.

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

Cited by 74 publications

References 65 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

The Sussex signal: insights into leaf dorsiventrality

MicroRNAs ( miRNAs ) and Plant Development

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