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 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.

scholarly journals Auxin transport-dependent, stage-specific dynamics of leaf vein formation

2008 ◽  
Vol 3 (5) ◽  
pp. 286-289 ◽  
Author(s):  
Megan G. Sawchuk ◽  
Tyler J. Donner ◽  
Enrico Scarpella
Keyword(s):  
Auxin Transport ◽  
Leaf Vein ◽  
Vein Formation

Vein patterning and evolution in C4 plants

Botany ◽  
2010 ◽  
Vol 88 (9) ◽  
pp. 775-786 ◽  
Author(s):  
Athena D. McKown ◽  
Nancy G. Dengler
Keyword(s):  
Molecular Mechanisms ◽  
Vascular System ◽  
Leaf Ontogeny ◽  
Vascular Patterning ◽  
Leaf Venation ◽  
Evolutionary Selection ◽  
Leaf Vein ◽  
Auxin Production ◽  
Vein Formation ◽  
Vein Patterning

The C4 photosynthetic pathway provides a platform to gain insight into the formation, regulation, and biological consequences of leaf vein pattern modification. This review examines the functional role of the vascular system in C4 photosynthesis and the development of veins in C3 and C4 plants, highlighting the contribution of vasculature in the evolution of the C4 pathway. With interest in developing C3 plant crops into C4 systems, it is essential to understand vascular patterning as a necessary element for C4 functioning. Leaf venation in C4 plants generally shows a higher vein density through a greater network complexity (more veins) compared with the ancestral C3 condition. Thus, C4 plants can provide a model that links the development of vein patterning with evolutionary selection pressures and molecular mechanisms (i.e., modifications of different components of vascular development). Numerous studies, including a comparative C3 and C4 Flaveria case study, highlight that the overall process of vein formation and patterning is complex, involving interactions between procambium and ground meristem during leaf ontogeny, and points to potential roles of changes in auxin production, transport, and perception.

scholarly journals Polar auxin transport dynamics of primary and secondary vein patterning in dicot leaves

2021 ◽  
Author(s):  
David M Holloway ◽  
Carol L Wenzel
Keyword(s):  
Auxin Transport ◽  
Leaf Growth ◽  
Cellular Level ◽  
Polar Auxin Transport ◽  
Secondary Vein ◽  
Neighbouring Cell ◽  
Transport Dynamics ◽  
Leaf Vein ◽  
Auxin Flux ◽  
Vein Patterning

Abstract The growth regulator auxin plays a central role in the phyllotaxy, shape, and venation patterns of leaves. The auxin spatial localization underlying these phenomena involves polar auxin transport (PAT) at the cellular level, particularly the preferential allocation of PIN efflux proteins to certain areas of the plasma membrane. Two general mechanisms have been studied: an up-the-gradient (UTG) allocation dependent on neighbouring-cell auxin concentrations, and a with-the-flux (WTF) allocation dependent on the flow of auxin across walls. We have developed a combined UTG+WTF model to quantify the observed auxin flows both towards (UTG) and away from (WTF) auxin maxima during primary and secondary vein patterning in leaves. The model simulates intracellular and membrane kinetics and intercellular transport, and is solved for a 2D leaf of several hundred cells. In addition to normal development, modelling of increasing PAT inhibition generates, as observed experimentally: a switch from several distinct vein initiation sites to many less-distinct sites; a delay in vein canalization; inhibited connection of new veins to old; and finally loss of patterning in the margin, loss of vein extension, and confinement of auxin to the margin. The model generates the observed formation of discrete auxin maxima at leaf vein sources and shows the dependence of secondary vein patterning on the efficacy of auxin flux through cells. Simulations of vein patterning and leaf growth further indicate that growth itself may bridge the spatial scale from the cell-cell resolution of the PIN-auxin dynamics to vein patterns on the whole-leaf scale.

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.

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.

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 Elevated auxin biosynthesis and transport underlie high vein density in C4 leaves

2017 ◽  
Vol 114 (33) ◽  
pp. E6884-E6891 ◽  
Author(s):  
Chi-Fa Huang ◽  
Chun-Ping Yu ◽  
Yeh-Hua Wu ◽  
Mei-Yeh Jade Lu ◽  
Shih-Long Tu ◽  
...  
Keyword(s):  
Auxin Transport ◽  
Auxin Biosynthesis ◽  
Efflux Transporter ◽  
Loss Of Function ◽  
Leaf Vein ◽  
Vein Density ◽  
Transport Inhibitor ◽  
Auxin Content ◽  
Auxin Transport Inhibitor ◽  
Leaf Vein Density

High vein density, a distinctive trait of C4 leaves, is central to both C3-to-C4 evolution and conversion of C3 to C4-like crops. We tested the hypothesis that high vein density in C4 leaves is due to elevated auxin biosynthesis and transport in developing leaves. Up-regulation of genes in auxin biosynthesis pathways and higher auxin content were found in developing C4 leaves compared with developing C3 leaves. The same observation held for maize foliar (C4) and husk (C3) leaf primordia. Moreover, auxin content and vein density were increased in loss-of-function mutants of Arabidopsis MYC2, a suppressor of auxin biosynthesis. Treatment with an auxin biosynthesis inhibitor or an auxin transport inhibitor led to much fewer veins in new leaves. Finally, both Arabidopsis thaliana auxin efflux transporter pin1 and influx transporter lax2 mutants showed reduced vein numbers. Thus, development of high leaf vein density requires elevated auxin biosynthesis and transport.

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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