Perspectives on leaf dorsoventral polarity

Szakonyi, Dóra; Moschopoulos, Alexis; Byrne, Mary E.

doi:10.1007/s10265-010-0336-3

Cited by 42 publications

(46 citation statements)

References 94 publications

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“…Apart from the genetic antagonism between KAN and class III HD-ZIP genes in the establishment of organ polarity, nothing is known about the mechanism restricting KAN function (36,37). Interestingly, our data imply that UCN acts as a direct negative regulator of a KAN transcription factor.…”

Section: Discussionmentioning

confidence: 69%

“…Class III HD-ZIP, KAN, and YABBY transcription factors play central roles in the establishment of adaxial-abaxial polarity in leaves (36,37) and ovules (38), with KAN genes promoting abaxial cell fate and lamina outgrowth in leaves (26,27). ATS is a KAN gene that regulates integument boundary formation, inner integument outgrowth, and adaxialabaxial polarity (15,28,29,38).…”

Section: Discussionmentioning

confidence: 99%

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Regulation of planar growth by the Arabidopsis AGC protein kinase UNICORN

Enugutti¹,

Kirchhelle²,

Oelschner³

et al. 2012

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

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The spatial coordination of growth is of central importance for the regulation of plant tissue architecture. Individual layers, such as the epidermis, are clonally propagated and structurally maintained by symmetric cell divisions that are oriented along the plane of the layer. The developmental control of this process is poorly understood. The simple cellular basis and sheet-like structure of Arabidopsis integuments make them an attractive model system to address planar growth. Here we report on the characterization of the Arabidopsis UNICORN (UCN) gene. Analysis of ucn integuments reveals localized distortion of planar growth, eventually resulting in an ectopic multicellular protrusion. In addition, ucn mutants exhibit ectopic growth in filaments and petals, as well as aberrant embryogenesis. We further show that UCN encodes an active AGC VIII kinase. Genetic, biochemical, and cell biological data suggest that UCN suppresses ectopic growth in integuments by directly repressing the KANADI transcription factor ABERRANT TESTA SHAPE. Our findings indicate that UCN represents a unique plant growth regulator that maintains planar growth of integuments by repressing a developmental regulator involved in the control of early integument growth and polarity.AGC protein kinase | growth suppression | floral development | ovule | signal transduction P lant tissue morphogenesis depends on the coordination of cellular behavior within tissue layers. The formation of distinct layers depends on asymmetric cell division, the developmental control of which is under intense investigation (1, 2). After initiation, individual cell layers are propagated by symmetric cell divisions (3) with division planes often oriented along the plane of the layer (planar growth). For example, the layered structure of the epidermis is maintained by anticlinal cell divisions, whereas periclinal cell divisions are usually suppressed (4). Division planes of symmetrically dividing cells can be accurately predicted by a mathematical rule linking cell geometry and cytoskeletal dynamics (5), and much progress has been made in the elucidation of the cellular machinery controlling the division plane of dividing plant cells. However, developmental controls that maintain the planar orientation of symmetrical cell divisions within a tissue layer remain poorly understood (3).Arabidopsis integuments represent an attractive model to study tissue morphogenesis. They are lateral determinate tissues of the ovule, the progenitors of the seed coat, and undergo a regular mode of development resulting in simple tissue architecture. An inner and an outer integument originate from the epidermis of the central chalaza (6, 7). They grow into laminar extensions with each integument consisting of a bilayered sheet of anticlinally dividing cells. The outer integument eventually develops into a hood-like structure that envelops the distal nucellus carrying the developing embryo sac and the inner integument.Coordination of symmetrical cell divisions along the plane of the extendi...

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Section: Discussionmentioning

confidence: 69%

Section: Discussionmentioning

confidence: 99%

Regulation of planar growth by the Arabidopsis AGC protein kinase UNICORN

Enugutti¹,

Kirchhelle²,

Oelschner³

et al. 2012

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

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“…Initially, a group of cells is patterned along the proximal-distal axis and then establishment of the adaxial-abaxial axis is crucial for further leaf development. Subsequent cell proliferation along the medial-lateral axis results in flat and mediolateral symmetric leaves (Steeves and Sussex, 1989;Waites et al, 1998;Hudson, 2000;Byrne et al, 2001;Semiarti et al, 2001;Tsukaya, 2006;Bowman and Floyd, 2008;Szakonyi et al, 2010;Nakata et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Dual regulation of ETTIN (ARF3) gene expression by AS1-AS2, which maintains the DNA methylation level, is involved in stabilization of leaf adaxial-abaxial partitioning in Arabidopsis

et al. 2013

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Leaf primordia are generated at the periphery of the shoot apex, developing into flat symmetric organs with adaxial-abaxial polarity, in which the indeterminate state is repressed. Despite the crucial role of the ASYMMETRIC LEAVES1 (AS1)-AS2 nuclear-protein complex in leaf adaxial-abaxial polarity specification, information on mechanisms controlling their downstream genes has remained elusive. We systematically analyzed transcripts by microarray and chromatin immunoprecipitation assays and performed genetic rescue of as1 and as2 phenotypic abnormalities, which identified a new target gene, ETTIN (ETT)/AUXIN RESPONSE FACTOR3 (ARF3), which encodes an abaxial factor acting downstream of the AS1-AS2 complex. While the AS1-AS2 complex represses ETT by direct binding of AS1 to the ETT promoter, it also indirectly activates miR390- and RDR6-dependent post-transcriptional gene silencing to negatively regulate both ETT and ARF4 activities. Furthermore, AS1-AS2 maintains the status of DNA methylation in the ETT coding region. In agreement, filamentous leaves formed in as1 and as2 plants treated with a DNA methylation inhibitor were rescued by loss of ETT and ARF4 activities. We suggest that negative transcriptional, post-transcriptional and epigenetic regulation of the ARFs by AS1-AS2 is important for stabilizing early leaf partitioning into abaxial and adaxial domains.

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“…During the last decade, a great number of leaf adaxial-and abaxial-promoting factors have been identified (Kidner and Timmermans, 2007;Xu et al, 2007;Bowman and Floyd, 2008;Szakonyi et al, 2010). Some leaf polarity mutants show trumpet-or lotusshaped leaves, which reflect a loss of leaf expansion in the proximal part (Waites and Hudson, 1995;McConnell and Barton, 1998;Emery et al, 2003;Xu et al, 2003).…”

mentioning

confidence: 99%

YUCCAGenes Are Expressed in Response to Leaf Adaxial-Abaxial Juxtaposition and Are Required for Leaf Margin Development

Wang

et al. 2011

Plant Physiology

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During leaf development, the formation of leaf adaxial-abaxial polarity at the primordium stage is crucial for subsequent leaf expansion. However, little is known about the genetic control from polarity establishment to blade outgrowth. The leaf margin, comprising elongated margin cells and hydathodes, is thought to affect leaf expansion. Here, we show that mutants with defective leaf polarity or with loss of function in the multiple auxin-biosynthetic YUCCA (YUC) genes exhibited a similar abnormal leaf margin and less-expanded leaves. Leaf margins of these mutants contained fewer hydathodes and an increased number of cell patches in which the patterns of epidermal cells resembled those of hydathodes. The previously characterized leafabaxialized asymmetric leaves2 (as2) revoluta (rev) and leaf-adaxialized kanadi1 (kan1) kan2 double mutants both produce fingershaped, hydathode-like protrusions on adaxial and abaxial leaf surfaces, respectively. YUCs are required for formation of the protrusions, as those produced by as2 rev and kan1 kan2 were absent in the yuc1 yuc2 yuc4 triple mutant background. Expressions of YUC1, YUC2, and YUC4 were spatially regulated in the leaf, being associated with hydathodes in wild-type leaves and protrusions on as2 rev and kan1 kan2 leaves. In addition, inhibition of auxin transport by treatment of seedlings with N-(1-naphtyl) phtalamic acid or disruption of the auxin gradient by transforming plants with the 35S:YUC1 construct also blocked leaf margin development. Collectively, our data show that expressions of YUCs in the leaf respond to the adaxial-abaxial juxtaposition, and that the activities of auxin mediate leaf margin development, which subsequently promotes blade outgrowth.

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Perspectives on leaf dorsoventral polarity

Cited by 42 publications

References 94 publications

Regulation of planar growth by the Arabidopsis AGC protein kinase UNICORN

Regulation of planar growth by the Arabidopsis AGC protein kinase UNICORN

Dual regulation of ETTIN (ARF3) gene expression by AS1-AS2, which maintains the DNA methylation level, is involved in stabilization of leaf adaxial-abaxial partitioning in Arabidopsis

YUCCAGenes Are Expressed in Response to Leaf Adaxial-Abaxial Juxtaposition and Are Required for Leaf Margin Development

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