scholarly journals Coordination of Tissue Cell Polarity by Auxin Transport and Signaling

2019 ◽  
Author(s):  
Carla Verna ◽  
Sree Janani Ravichandran ◽  
Megan G. Sawchuk ◽  
Nguyen Manh Linh ◽  
Enrico Scarpella
Keyword(s):  
Cell Polarity ◽  
Auxin Transport ◽  
Molecular Genetic Analysis ◽  
Cell Polarization ◽  
Tissue Cell ◽  
Auxin Signaling ◽  
Plant Signaling ◽  
Chemical Induction ◽  
Vein Formation ◽  
Vein Patterning

AbstractCoordination of polarity between cells in tissues is key to multicellular organism development. In animals, coordination of this tissue cell polarity often requires direct cell-cell interactions and cell movements, which are precluded in plants by a wall that separates cells and holds them in place; yet plants coordinate the polarity of hundreds of cells during the formation of the veins in their leaves. Overwhelming experimental evidence suggests that the plant signaling molecule auxin coordinates tissue cell polarity to induce vein formation, but how auxin does so is unclear. The prevailing hypothesis proposes that GNOM, a regulator of vesicle formation during protein trafficking, positions auxin transporters of the PIN-FORMED family to the correct side of the plasma membrane. The resulting cell-to-cell, polar transport of auxin would coordinate tissue cell polarity and would induce vein formation. Here we tested this hypothesis by means of a combination of cellular imaging, molecular genetic analysis, and chemical induction and inhibition. Contrary to predictions of the hypothesis, we find that auxin-induced vein formation occurs in the absence of PIN-FORMED proteins or any known intercellular auxin transporter, that the residual auxin-transport-independent vein-patterning activity relies on auxin signaling, and that a GNOM-dependent signal that coordinates tissue cell polarity to induce vein formation acts upstream of both auxin transport and signaling. Our results reveal synergism between auxin transport and signaling, and their unsuspected control by GNOM, in the coordination of tissue cell polarity during vein patterning, one of the most spectacular and informative expressions of tissue cell polarization in plants.

scholarly journals Coordination of tissue cell polarity by auxin transport and signaling

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Carla Verna ◽  
Sree Janani Ravichandran ◽  
Megan G Sawchuk ◽  
Nguyen Manh Linh ◽  
Enrico Scarpella
Keyword(s):  
Cell Polarity ◽  
Membrane Trafficking ◽  
Auxin Transport ◽  
Cell Polarization ◽  
Tissue Cell ◽  
Auxin Signaling ◽  
Vein Formation ◽  
Dependent Signal ◽  
Vein Patterning ◽  
Auxin Transporter

Plants coordinate the polarity of hundreds of cells during vein formation, but how they do so is unclear. The prevailing hypothesis proposes that GNOM, a regulator of membrane trafficking, positions PIN-FORMED auxin transporters to the correct side of the plasma membrane; the resulting cell-to-cell, polar transport of auxin would coordinate tissue cell polarity and induce vein formation. Contrary to predictions of the hypothesis, we find that vein formation occurs in the absence of PIN-FORMED or any other intercellular auxin-transporter; that the residual auxin-transport-independent vein-patterning activity relies on auxin signaling; and that a GNOM-dependent signal acts upstream of both auxin transport and signaling to coordinate tissue cell polarity and induce vein formation. Our results reveal synergism between auxin transport and signaling, and their unsuspected control by GNOM in the coordination of tissue cell polarity during vein patterning, one of the most informative expressions of tissue cell polarization in plants.

Cell polarity and tissue patterning in plants

Development ◽  
1991 ◽  
Vol 113 (Supplement_1) ◽  
pp. 83-93 ◽  
Author(s):  
Tsvi Sachs
Keyword(s):  
Cell Polarity ◽  
Cell Shape ◽  
Auxin Transport ◽  
Developmental Stages ◽  
Important Determinant ◽  
Genetic System ◽  
Cell Patterning ◽  
Cell Polarization ◽  
Sources And Sinks ◽  
Tissue Patterning

Cell polarization is the specialization of developmental events along one orientation or one direction. Such polarization must be an early, essential stage of tissue patterning. The specification of orientation could not occur only at the level of the genetic system and it must express a coordination of events in many cells. There is a positive feedback relation between cell polarization and the transport of the known hormone auxin: polarity determines oriented auxin transport while transport itself induces both new and continued polarization. Since cell polarization increases gradually, this feedback leads to the canalization of transport – and of the associated cell differentiation – along defined strands of specialized cells. Recent work has shown that the same canalized flow can also be an important determinant of cell shape. In primordial, embryonic regions cell growth is oriented along the flow of auxin from the shoot towards the root. In later developmental stages the cells respond to the same flow by growing in girth, presumably adjusting the capacity of the tissues to the flow of signals. Finally, disrupted flow near wounds results in the development of relatively unorganized callus. Continued callus development appears to require the participation of the cells, as sources and sinks of auxin and other signals. The overall picture to emerge suggests that cell patterning can result from competition between cells acting as preferred channels, sources and sinks for developmental signals.

Auxin biosynthesis and cellular efflux act together to regulate leaf vein patterning

2020 ◽  
Author(s):  
Irina Kneuper ◽  
William Teale ◽  
Jonathan Edward Dawson ◽  
Ryuji Tsugeki ◽  
Eleni Katifori ◽  
...  
Keyword(s):  
Plant Hormone ◽  
Auxin Transport ◽  
Auxin Biosynthesis ◽  
Mechanical Forces ◽  
Enzyme Expression ◽  
Leaf Vein ◽  
Vein Formation ◽  
Specific Accumulation ◽  
Vein Patterning ◽  
Distal Cell

Abstract Our current understanding of vein development in leaves is based on canalization of the plant hormone auxin into self-reinforcing streams which determine the sites of vascular cell differentiation. By comparison, how auxin biosynthesis affects leaf vein patterning is less well understood. Here, after observing that inhibiting polar auxin transport rescues the sparse leaf vein phenotype in auxin biosynthesis mutants, we propose that the processes of auxin biosynthesis and cellular auxin efflux work in concert during vein development. By using computational modeling, we show that localized auxin maxima are able to interact with mechanical forces generated by the morphological constraints which are imposed during early primordium development. This interaction is able to explain four fundamental characteristics of midvein morphology in a growing leaf: (i) distal cell division; (ii) coordinated cell elongation; (iii) a midvein positioned in the center of the primordium; and (iv) a midvein which is distally branched. Domains of auxin biosynthetic enzyme expression are not positioned by auxin canalization, as they are observed before auxin efflux proteins polarize. This suggests that the site-specific accumulation of auxin, as regulated by the balanced action of cellular auxin efflux and local auxin biosynthesis, is crucial for leaf vein formation.

scholarly journals Author response: Coordination of tissue cell polarity by auxin transport and signaling

2019 ◽  
Author(s):  
Carla Verna ◽  
Sree Janani Ravichandran ◽  
Megan G Sawchuk ◽  
Nguyen Manh Linh ◽  
Enrico Scarpella
Keyword(s):  
Cell Polarity ◽  
Auxin Transport ◽  
Author Response ◽  
Tissue Cell

scholarly journals Control of Leaf Vein Patterning by Regulated Plasmodesma Aperture

2021 ◽  
Author(s):  
Nguyen Manh Linh ◽  
Enrico Scarpella
Keyword(s):  
Plasma Membranes ◽  
Auxin Transport ◽  
Network Formation ◽  
Auxin Signaling ◽  
Animal Cells ◽  
Leaf Vein ◽  
Coordinated Action ◽  
Intercellular Channels ◽  
Vein Patterning ◽  
Multicellular Organisms

To form tissue networks, animal cells migrate and interact through proteins protruding from their plasma membranes. Plant cells can do neither, yet plants form vein networks. How plants do so is unclear, but veins are thought to form by the coordinated action of the polar transport and signal transduction of the plant hormone auxin. However, plants inhibited in both pathways still form veins. Patterning of vascular cells into veins is instead prevented in mutants lacking the function of the GNOM (GN) regulator of auxin transport and signaling, suggesting the existence of at least one more GN-dependent vein-patterning pathway. Here we show that pathway depends on the movement of an auxin signal through plasmodesmata (PDs) intercellular channels. PD permeability is high where veins are forming, lowers between veins and nonvascular tissues, but remains high between vein cells. Impaired ability to regulate PD aperture leads to defects in auxin transport and signaling, ultimately leading to vein patterning defects that are enhanced by inhibition of auxin transport or signaling. GN controls PD aperture regulation, and simultaneous inhibition of auxin signaling, auxin transport, and regulated PD aperture phenocopies null gn mutants. Therefore, veins are patterned by the coordinated action of three GN-dependent pathways: auxin signaling, polar auxin transport, and movement of an auxin signal through PDs. We have identified all the key vein-patterning pathways in plants and an unprecedented mechanism of tissue network formation in multicellular organisms.

scholarly journals Tissue specific auxin biosynthesis regulates leaf vein patterning

2017 ◽  
Author(s):  
Irina Kneuper ◽  
William Teale ◽  
Jonathan Edward Dawson ◽  
Ryuji Tsugeki ◽  
Klaus Palme ◽  
...  
Keyword(s):  
Auxin Transport ◽  
Spatiotemporal Analysis ◽  
Auxin Biosynthesis ◽  
Cell Stiffness ◽  
List Type ◽  
Tissue Specific ◽  
Leaf Vein ◽  
Vein Formation ◽  
Vein Patterning ◽  
Context Specific

SummaryThe plant hormone auxin (indole-3-acetic acid, IAA) has a profound influence over plant cell growth and differentiation. Current understanding of vein development in leaves is based on the canalization of auxin into self-reinforcing streams which determine the sites of vascular cell differentiation. However, the role of auxin biosynthesis during leaf development in the context of leaf vein patterning has not been much studied so far. Here we characterize the context specific importance of auxin biosynthesis, auxin transport and mechanical regulations in a growing leaf. We show that domains of auxin biosynthesis predict the positioning of vascular cells. In mutants that have reduced capacity in auxin biosynthesis, leaf vein formation is decreased. While exogenous application of auxin does not compensate the loss of vein formation in auxin biosynthesis mutants, inhibition of polar auxin transport does compensate the vein-less phenotype, suggesting that the site-specific accumulation of auxin, which is likely to be mainly caused by the local auxin biosynthesis, is important for leaf vein formation. Our computational model of midvein development brings forth the interplay of cell stiffness and auxin dependent cell division. We propose that local auxin biosynthesis has the integral role in leaf vascular development.HighlightsBuilt spatially and temporally resolved auxin biosynthesis map in growing leaf primordium of Arabidopsis.Expression domains of auxin biosynthetic enzymes within primordia strongly correlated with leaf vein initiation.Results show that domains of auxin biosynthesis within primordia drive leaf vein initiation and patterning.Highlights and eTOC BlurbUsing modelling and a spatiotemporal analysis of auxin biosynthesis and transport, Kneuper et al. show that tissue specific auxin biosynthesis defines places of vein initiation hence underlining the importance of auxin concentration in vein initiation.

Auxin-transport-dependent leaf vein formationThis paper is one of a selection published in a Special Issue comprising papers presented at the 50th Annual Meeting of the Canadian Society of Plant Physiologists (CSPP) held at the University of Ottawa, Ontario, in June 2008.

Botany ◽  
2009 ◽  
Vol 87 (7) ◽  
pp. 678-684 ◽  
Author(s):  
Tyler J. Donner ◽  
Enrico Scarpella
Keyword(s):  
Leaf Development ◽  
Auxin Transport ◽  
Plant Signaling ◽  
Canadian Society ◽  
Special Issue ◽  
Leaf Vein ◽  
Vein Formation ◽  
The University ◽  
Selection Of

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.

scholarly journals Membrane Sterol Composition in Arabidopsis thaliana Affects Root Elongation via Auxin Biosynthesis

2021 ◽  
Vol 22 (1) ◽  
pp. 437
Author(s):  
Meng Wang ◽  
Panpan Li ◽  
Yao Ma ◽  
Xiang Nie ◽  
Markus Grebe ◽  
...  
Keyword(s):  
Root Elongation ◽  
Auxin Transport ◽  
Sterol Composition ◽  
Polar Auxin Transport ◽  
Sterol Biosynthesis ◽  
Auxin Biosynthesis ◽  
Root Tip ◽  
Auxin Signaling ◽  
Auxin Response ◽  
Short Root

Plant membrane sterol composition has been reported to affect growth and gravitropism via polar auxin transport and auxin signaling. However, as to whether sterols influence auxin biosynthesis has received little attention. Here, by using the sterol biosynthesis mutant cyclopropylsterol isomerase1-1 (cpi1-1) and sterol application, we reveal that cycloeucalenol, a CPI1 substrate, and sitosterol, an end-product of sterol biosynthesis, antagonistically affect auxin biosynthesis. The short root phenotype of cpi1-1 was associated with a markedly enhanced auxin response in the root tip. Both were neither suppressed by mutations in polar auxin transport (PAT) proteins nor by treatment with a PAT inhibitor and responded to an auxin signaling inhibitor. However, expression of several auxin biosynthesis genes TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS1 (TAA1) was upregulated in cpi1-1. Functionally, TAA1 mutation reduced the auxin response in cpi1-1 and partially rescued its short root phenotype. In support of this genetic evidence, application of cycloeucalenol upregulated expression of the auxin responsive reporter DR5:GUS (β-glucuronidase) and of several auxin biosynthesis genes, while sitosterol repressed their expression. Hence, our combined genetic, pharmacological, and sterol application studies reveal a hitherto unexplored sterol-dependent modulation of auxin biosynthesis during Arabidopsis root elongation.

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