Enrico Scarpella

University of Alberta, Edmonton, Alberta, Canada

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Publications (30)157.24 Total impact

  • Megan Sawchuk, Enrico Scarpella
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    ABSTRACT: The vein networks of plant leaves are among the most spectacular expressions of biological pattern, and the principles controlling their formation have continually inspired artists and scientists. Control of vein patterning by the polar, cell-to-cell transport of the plant signaling molecule auxin-mediated in Arabidopsis primarily by the plasma-membrane-localized PIN1-has long been known. By contrast, the existence of intracellular auxin transport and its contribution to vein patterning are recent discoveries. The endoplasmic-reticulum-localized PIN5, PIN6, and PIN8 of Arabidopsis define an intracellular auxin-transport pathway whose functions in vein patterning overlap with those of PIN1-mediated intercellular auxin transport. The genetic interaction between the components of the intracellular auxin-transport pathway is far from having been resolved. The study of vein patterning provides experimental access to gain such a resolution-a resolution that in turn holds the promise to improve our understanding of one of the most fascinating examples of biological pattern formation.
    Plant signaling & behavior 12/2013; 8(11).
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    ABSTRACT: Patterning of numerous features of plants depends on transduction of the auxin signal. Auxin signaling is mediated by several pathways, the best understood of which relies on the function of the MONOPTEROS (MP) gene. Seven mp mutant alleles have been described in the widely used Columbia background of Arabidopsis: two extensively characterized and five only partially characterized. One of these five mp alleles appears to be extinct and thus unavailable for analysis. We show that two of the four remaining, partially characterized mp alleles reported to be in the Columbia background are in fact not in this background. We extend characterization of the remaining two Columbia alleles of mp, and we identify and characterize four new alleles of mp in the Columbia background, among which the first low-expression allele of mp and the strongest Columbia allele of mp. These genetic resources provide the research community with new experimental opportunities for insight into the function of MP-dependent auxin signaling in plant development. © 2013 Wiley Periodicals, Inc.
    genesis 11/2013; · 2.58 Impact Factor
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    Megan G Sawchuk, Enrico Scarpella
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    ABSTRACT: Plant vascular cells are joined end to end along uninterrupted lines to connect shoot organs with roots; vascular strands are thus polar, continuous and internally aligned. What controls the formation of vascular strands with these properties? The "auxin canalization hypothesis"-based on positive feedback between auxin flow through a cell and the cell's capacity for auxin transport-predicts the selection of continuous files of cells that transport auxin polarly, thus accounting for the polarity and continuity of vascular strands. By contrast, polar, continuous auxin transport-though required-is insufficient to promote internal alignment of vascular strands, implicating additional factors. The auxin canalization hypothesis was derived from the response of mature tissue to auxin application but is consistent with molecular and cellular events in embryo axis formation and shoot organ development. Objections to the hypothesis have been raised based on vascular organizations in callus tissue and shoot organs but seem unsupported by available evidence. Other objections call instead for further research; yet the inductive and orienting influence of auxin on continuous vascular differentiation remains unique.
    Journal of Integrative Plant Biology 06/2013; · 3.75 Impact Factor
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    Megan G Sawchuk, Alexander Edgar, Enrico Scarpella
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    ABSTRACT: The formation of leaf vein patterns has fascinated biologists for centuries. Transport of the plant signal auxin has long been implicated in vein patterning, but molecular details have remained unclear. Varied evidence suggests a central role for the plasma-membrane (PM)-localized PIN-FORMED1 (PIN1) intercellular auxin transporter of Arabidopsis thaliana in auxin-transport-dependent vein patterning. However, in contrast to the severe vein-pattern defects induced by auxin transport inhibitors, pin1 mutant leaves have only mild vein-pattern defects. These defects have been interpreted as evidence of redundancy between PIN1 and the other four PM-localized PIN proteins in vein patterning, redundancy that underlies many developmental processes. By contrast, we show here that vein patterning in the Arabidopsis leaf is controlled by two distinct and convergent auxin-transport pathways: intercellular auxin transport mediated by PM-localized PIN1 and intracellular auxin transport mediated by the evolutionarily older, endoplasmic-reticulum-localized PIN6, PIN8, and PIN5. PIN6 and PIN8 are expressed, as PIN1 and PIN5, at sites of vein formation. pin6 synthetically enhances pin1 vein-pattern defects, and pin8 quantitatively enhances pin1pin6 vein-pattern defects. Function of PIN6 is necessary, redundantly with that of PIN8, and sufficient to control auxin response levels, PIN1 expression, and vein network formation; and the vein pattern defects induced by ectopic PIN6 expression are mimicked by ectopic PIN8 expression. Finally, vein patterning functions of PIN6 and PIN8 are antagonized by PIN5 function. Our data define a new level of control of vein patterning, one with repercussions on other patterning processes in the plant, and suggest a mechanism to select cell files specialized for vascular function that predates evolution of PM-localized PIN proteins.
    PLoS Genetics 02/2013; 9(2):e1003294. · 8.52 Impact Factor
  • Tyler J Donner, Enrico Scarpella
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    ABSTRACT: Unlike most animal tissue networks, the patterns of vein networks in plant leaves are variable and plastic, suggesting distinct control mechanisms. Thus, knowledge of the gene regulatory circuits that pattern leaf vein networks could suggest new control mechanisms of tissue network formation. However, the cis-regulatory elements required for expression at early stages of vein development are largely unknown. Here we show that the Arabidopsis genes CYCLIN A2;1 (CYCA2;1) and CYCLIN A2;4 (CYCA2;4), previously shown to act redundantly in vein cell proliferation, are expressed at early stages of vein development. We show that stage-specific expression of CYCA2;1 and CYCA2;4 in vein development depends on regulatory elements containing, respectively, one and three evolutionarily conserved transcription-factor binding sites. Our data suggest that early vein expression is encoded in regulatory elements of different structures.
    Mechanisms of development 07/2012; · 2.83 Impact Factor
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    ABSTRACT: Genes expressed in vascular tissues have been identified by several strategies, usually with a focus on mature vascular cells. In this study, we explored the possibility of using two opposite types of altered tissue compositions in combination with a double-filter selection to identify genes with a high probability of vascular expression in early organ primordia. Specifically, we generated full-transcriptome microarray profiles of plants with (a) genetically strongly reduced and (b) pharmacologically vastly increased vascular tissues and identified a reproducible cohort of 158 transcripts that fulfilled the dual requirement of being underrepresented in (a) and overrepresented in (b). In order to assess the predictive value of our identification scheme for vascular gene expression, we determined the expression patterns of genes in two unbiased subsamples. First, we assessed the expression patterns of all twenty annotated transcription factor genes from the cohort of 158 genes and found that seventeen of the twenty genes were preferentially expressed in leaf vascular cells. Remarkably, fifteen of these seventeen vascular genes were clearly expressed already very early in leaf vein development. Twelve genes with published leaf expression patterns served as a second subsample to monitor the representation of vascular genes in our cohort. Of those twelve genes, eleven were preferentially expressed in leaf vascular tissues. Based on these results we propose that our compendium of 158 genes represents a sample that is highly enriched for genes expressed in vascular tissues and that our approach is particularly suited to detect genes expressed in vascular cell lineages at early stages of their inception.
    Plant Science 08/2011; 181(2):96-104. · 4.11 Impact Factor
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    Jason Gardiner, Tyler J Donner, Enrico Scarpella
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    ABSTRACT: The processes underlying the formation of leaf vascular networks have long captured the attention of developmental biologists, especially because files of elongated vascular-precursor procambial cells seem to differentiate from apparently equivalent, isodiametric ground cells. In Arabidopsis leaves, ground cells that have been specified to vascular fate engage expression of ARABIDOPSIS THALIANA HOMEOBOX8 (ATHB8). While definition of the transcriptional state of ATHB8-expressing ground cells would be particularly informative, no other genes have been identified whose expression is initiated at this stage. Here we show that expression of SHORT-ROOT (SHR) is activated simultaneously with that of ATHB8 in leaf development. Congruence between SHR and ATHB8 expression domains persists under conditions of manipulated vein patterning, suggesting that inception of expression of SHR and ATHB8 identifies transition to a preprocambial cell state that presages vein formation. Our observations further characterize the molecular identity of cells at anatomically inconspicuous stages of leaf vein development.
    Developmental Dynamics 01/2011; 240(1):261-70. · 2.59 Impact Factor
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    ABSTRACT: In multicellular organisms, morphogenesis relies on a strict coordination in time and space of cell proliferation and differentiation. In contrast to animals, plant development displays continuous organ formation and adaptive growth responses during their lifespan relying on a tight coordination of cell proliferation. How developmental signals interact with the plant cell-cycle machinery is largely unknown. Here, we characterize plant A2-type cyclins, a small gene family of mitotic cyclins, and show how they contribute to the fine-tuning of local proliferation during plant development. Moreover, the timely repression of CYCA2;3 expression in newly formed guard cells is shown to require the stomatal transcription factors FOUR LIPS/MYB124 and MYB88, providing a direct link between developmental programming and cell-cycle exit in plants. Thus, transcriptional downregulation of CYCA2s represents a critical mechanism to coordinate proliferation during plant development.
    The EMBO Journal 01/2011; 30(16):3430-41. · 9.82 Impact Factor
  • Enrico Scarpella, Ykä Helariutta
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    ABSTRACT: Reticulate tissue systems exist in most multicellular organisms, and the principles underlying the formation of cellular networks have fascinated philosophers, mathematicians, and biologists for centuries. In particular, the beautiful and varied arrangements of vascular tissues in plants have intrigued mankind since antiquity, yet the organizing signals have remained elusive. Plant vascular tissues form systems of interconnected cell files throughout the plant body. Vascular cells are aligned with one another along continuous lines, and vascular tissues differentiate at reproducible positions within organ environments. However, neither the precise path of vascular differentiation nor the exact geometry of vascular networks is fixed or immutable. Several recent advances converge to reconcile the seemingly conflicting predictability and plasticity of vascular tissue patterns. A control mechanism in which an apical-basal flow of signal establishes a basic coordinate system for body axis formation and vascular strand differentiation, and in which a superimposed level of radial organizing cues elaborates cell patterns, would generate a reproducible tissue configuration in the context of an underlying robust, self-organizing structure, and account for the simultaneous regularity and flexibility of vascular tissue patterns.
    Current Topics in Developmental Biology 01/2010; 91:221-65. · 6.91 Impact Factor
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    Tyler J Donner, Ira Sherr, Enrico Scarpella
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    ABSTRACT: The plant signaling molecule auxin has been implicated in the control of a confounding multitude of diverse processes in plants, including leaf vascular patterning. In Arabidopsis leaves, expression of the HD-ZIP III gene ATHB8 is initiated in files of isodiametric subepidermal cells that will elongate into vein-forming procambium. We have recently shown that ATHB8 is transiently required for preprocambial development and procambium differentiation, and that permanence of the effects of loss of ATHB8 function on vein formation depends on the activity of the auxin response factor MONOPTEROS (MP). Further, we have shown that the onset of ATHB8 expression is directly and positively regulated by MP through an auxin-response element in the ATHB8 promoter, suggesting a molecular path by which auxin signals are translated into vein patterning inputs. Within broad fields of MP expression, however, only a subset of cells initiates expression of ATHB8. Here we discuss putative mechanisms by which wide domains of MP expression could activate ATHB8 transcription in single cell files.
    Plant signaling & behavior 01/2010; 5(1):70-2.
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    Enrico Scarpella, Michalis Barkoulas, Miltos Tsiantis
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    ABSTRACT: Leaves are the main photosynthetic organs of vascular plants and show considerable diversity in their geometries, ranging from simple spoon-like forms to complex shapes with individual leaflets, as in compound leaves. Leaf vascular tissues, which act as conduits of both nutrients and signaling information, are organized in networks of different architectures that usually mirror the surrounding leaf shape. Understanding the processes that endow leaves and vein networks with ordered and closely aligned shapes has captured the attention of biologists and mathematicians since antiquity. Recent work has suggested that the growth regulator auxin has a key role in both initiation and elaboration of final morphology of both leaves and vascular networks. A key feature of auxin action is the existence of feedback loops through which auxin regulates its own transport. These feedbacks may facilitate the iterative generation of basic modules that underlies morphogenesis of both leaves and vasculature.
    Cold Spring Harbor perspectives in biology 01/2010; 2(1):a001511. · 9.63 Impact Factor
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    Jason Gardiner, Ira Sherr, Enrico Scarpella
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    ABSTRACT: The sequence of events underlying the formation of vascular networks in the leaf has long fascinated developmental biologists. In Arabidopsis leaves, vascular-precursor procambial cells derive from the elongation of morphologically inconspicuous ground cells that selectively activate expression of the HD-ZIP III gene ATHB8. Inception of ATHB8 expression operationally defines acquisition of a typically irreversible preprocambial cell state that preludes to vein formation. A view of the constellation of genes whose expression is activated at preprocambial stages would therefore be particularly desirable; however, very few preprocambial gene expression profiles have been identified. Here, we show that expression of three genes encoding members of the DOF family of plant-specific transcription factors is activated at stages overlapping onset of ATHB8 expression. Expression of DOF genes is initiated in wide domains that become confined to sites of vein development. Congruence between DOF expression fields and zones of vein formation persists upon experimental manipulation of leaf vascular patterning, suggesting that DOF expression identifies consistently recurring steps in vein ontogeny. Our results contribute to defining preprocambial cell identity at the molecular level.
    The International journal of developmental biology 01/2010; 54(8-9):1389-96. · 2.16 Impact Factor
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    Tyler J Donner, Ira Sherr, Enrico Scarpella
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    ABSTRACT: The principles underlying the formation of veins in the leaf have long intrigued developmental biologists. In Arabidopsis leaves, files of anatomically inconspicuous subepidermal cells that will elongate into vein-forming procambial cells selectively activate ATHB8 gene expression. The biological role of ATHB8 in vein formation and the molecular events that culminate in acquisition of the ATHB8 preprocambial cell state are unknown, but intertwined pathways of auxin transport and signal transduction have been implicated in defining paths of vascular strand differentiation. Here we show that ATHB8 is required to stabilize preprocambial cell specification against auxin transport perturbations, to restrict preprocambial cell state acquisition to narrow fields and to coordinate procambium formation within and between veins. We further show that ATHB8 expression at preprocambial stages is directly and positively controlled by the auxin-response transcription factor MONOPTEROS (MP) through an auxin-response element in the ATHB8 promoter. We finally show that the consequences of loss of ATHB8 function for vein formation are masked by MP activity. Our observations define, at the molecular level, patterning inputs of auxin signaling in vein formation.
    Development 09/2009; 136(19):3235-46. · 6.60 Impact Factor
  • Tyler J. Donner, Enrico Scarpella
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    ABSTRACT: The formation of vein patterns in leaves has captivated biologists, mathematicians, and philosophers. In leaf development, files of vein-forming procambial cells emerge from within a seemingly homogeneous subepidermal tissue through the selection of anatomically inconspicuous preprocambial cells. Although the molecular details underlying the orderly formation of veins in the leaf remain elusive, gradually restricted transport paths of the plant signaling molecule auxin have long been implicated in defining sites of vein differentiation. Several recent advances converge to more precisely define the role of auxin flow at successive stages of vascular development. The picture that emerges is that of vein formation as a self-organizing, reiterative, auxin-transport-dependent process.La formation des patrons des nervures foliaires a captivé les biologistes, les mathématiciens et les philosophes. Au cours du développement foliaire, des files de cellules procambiales forment des veines émergentes au sein de ce qui semble un tissus sub épidermique homogène, via la sélection de cellules procambiales anatomiquement invisibles. Bien que les détails moléculaires sous-jacents à la formation ordonnée des nervures dans la feuille demeurent insaisissables, on a depuis longtemps impliqué le transport graduellement restreint de la molécule d'auxine responsable de signaux végétaux, dans la définition des sites de différenciation des nervures. Plusieurs percées récentes convergent vers une définition plus précise du rôle du flux d'auxine à différents stades du développement vasculaire. Le tableau qui émerge est celui de la formation des nervures comme un processus auto organisé, réitératif et dépendant de l'auxine.
    Botany 07/2009; 87(7):678-684. · 1.23 Impact Factor
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    ABSTRACT: Light provides crucial positional information in plant development, and the morphogenetic processes that are orchestrated by light signals are triggered by changes of gene expression in response to variations in light parameters. Control of expression of members of the RbcS and Lhc families of photosynthesis-associated nuclear genes by light cues is a paradigm for light-regulated gene transcription, but high-resolution expression profiles for these gene families are lacking. In this study, we have investigated expression patterns of members of the RbcS and Lhc gene families in Arabidopsis (Arabidopsis thaliana) at the cellular level during undisturbed development and upon controlled interference of the light environment. Members of the RbcS and Lhc gene families are expressed in specialized territories, including root tip, leaf adaxial, abaxial, and epidermal domains, and with distinct chronologies, identifying successive stages of leaf mesophyll ontogeny. Defined spatial and temporal overlap of gene expression fields suggest that the light-harvesting and photosynthetic apparatus may have a different polypeptide composition in different cells and that such composition could change over time even within the same cell.
    Plant physiology 10/2008; 148(4):1908-24. · 6.56 Impact Factor
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    Megan G Sawchuk, Tyler J Donner, Enrico Scarpella
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    ABSTRACT: For centuries, the formation of vein patterns in the leaf has intrigued biologists, mathematicians and philosophers. In leaf development, files of vein-forming procambial cells emerge from seemingly homogeneous subepidermal tissue through the selection of anatomically inconspicuous preprocambial cells. Although the molecular details underlying the orderly differentiation of veins in the leaf remain elusive, gradually restricted transport paths of the plant hormone auxin have long been implicated in defining sites of vein formation. Several recent advances now appear to converge on a more precise definition of the role of auxin flow at different stages of vascular development. The picture that emerges is that of vein formation as a self-organizing, reiterative, auxin transport-dependent process.
    Plant signaling & behavior 06/2008; 3(5):286-9.
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    ABSTRACT: Polar auxin transport intimately connects plant cell polarity and multicellular patterning. Through the transport of the small molecule indole-3-acetic acid, plant cells integrate their polarities and communicate the degree of their polarization. In this way, they generate an apical-basal axis that serves as a positional reference anchoring subsequent patterning events. Research in recent years has brought the molecular mechanisms underlying auxin perception and auxin transport to light. This knowledge has been used to derive spectacular molecular visualization tools and animated computer simulations, which are now allied in a joint systems biology effort towards a mathematical description of auxin-transport-mediated patterning processes.
    Trends in Plant Science 05/2007; 12(4):151-9. · 11.81 Impact Factor
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    ABSTRACT: The principles underlying the formation of leaf veins have long intrigued developmental biologists. In leaves, networks of vascular precursor procambial cells emerge from seemingly homogeneous subepidermal tissue through the selection of anatomically inconspicuous preprocambial cells. Understanding dynamics of procambium formation has been hampered by the difficulty of observing the process in vivo. Here we present a live-imaging technique that allows visual access to complex events occurring in developing leaves. We combined this method with stage-specific fluorescent markers in Arabidopsis (Arabidopsis thaliana) to visualize preprocambial strand formation and procambium differentiation during the undisturbed course of development and upon defined perturbations of vein ontogeny. Under all experimental conditions, we observed extension, termination and fusion of preprocambial strands and simultaneous initiation of procambium differentiation along entire individual veins. Our findings strongly suggest that progressiveness of preprocambial strand formation and simultaneity of procambium differentiation represent inherent properties of the mechanism underlying vein formation.
    New Phytologist 02/2007; 176(3):560-71. · 6.74 Impact Factor
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    ABSTRACT: The formation of the leaf vascular pattern has fascinated biologists for centuries. In the early leaf primordium, complex networks of procambial cells emerge from homogeneous subepidermal tissue. The molecular nature of the underlying positional information is unknown, but various lines of evidence implicate gradually restricted transport routes of the plant hormone auxin in defining sites of procambium formation. Here we show that a crucial member of the AtPIN family of auxin-efflux-associated proteins, AtPIN1, is expressed prior to pre-procambial and procambial cell fate markers in domains that become restricted toward sites of procambium formation. Subcellular AtPIN1 polarity indicates that auxin is directed to distinct "convergence points" in the epidermis, from where it defines the positions of major veins. Integrated polarities in all emerging veins indicate auxin drainage toward pre-existing veins, but veins display divergent polarities as they become connected at both ends. Auxin application and transport inhibition reveal that convergence point positioning and AtPIN1 expression domain dynamics are self-organizing, auxin-transport-dependent processes. We derive a model for self-regulated, reiterative patterning of all vein orders and postulate at its onset a common epidermal auxin-focusing mechanism for major-vein positioning and phyllotactic patterning.
    Genes & Development 05/2006; 20(8):1015-27. · 12.44 Impact Factor
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    Enrico Scarpella, Erik J Simons, Annemarie H Meijer
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    ABSTRACT: The primary vascular tissues of plants differentiate from a single precursor tissue, the procambium. The role of upstream regulatory sequences in the transcriptional control of early vascular-specific gene expression is largely unknown. The onset of expression of the rice homeodomain-leucine zipper (HD-Zip) gene Oshox1 marks procambial cells that have acquired their distinctive anatomical features but do not yet display any overt signs of terminal vascular differentiation. The expression pattern of Oshox1 in rice appears to be mainly controlled by the activity of the 1.6 kb upstream promoter region. Here, we show that the Oshox1 promoter directs vascular, auxin- and sucrose-responsive reporter gene expression in Arabidopsis plants in a fashion comparable with that in rice. This is the case not only during normal development but also upon experimental manipulation, suggesting that the cis-acting regulatory elements that are instrumental in Oshox1 expression pattern are conserved between rice and Arabidopsis. Finally, through analysis of reporter gene expression profiles conferred by progressive 5' deletions of the Oshox1 promoter in transgenic Arabidopsis, we have identified upstream regulatory regions required for auxin and sucrose inducibility, and for cell type-, tissue- and organ-specific aspects of Oshox1 expression. Our study suggests that Oshox1 embryonic vascular expression is mainly achieved through suppression of expression in non-vascular tissues.
    Plant and Cell Physiology 09/2005; 46(8):1400-10. · 4.98 Impact Factor

Publication Stats

1k Citations
157.24 Total Impact Points

Institutions

  • 2004–2013
    • University of Alberta
      • Department of Biological Sciences
      Edmonton, Alberta, Canada
  • 2004–2011
    • University of Toronto
      • Department of Cell and Systems Biology
      Toronto, Ontario, Canada
  • 2000–2005
    • Leiden University
      • Institute of Biology Leiden
      Leiden, South Holland, Netherlands