Control of vein network topology by auxin transport

Verna, Carla; Sawchuk, Megan G.; Linh, Nguyễn Mạnh; Scarpella, Enrico

doi:10.1186/s12915-015-0208-3

Cited by 50 publications

(84 citation statements)

References 95 publications

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“…5a,b) (Benkova et al, 2003;Reinhardt et al, 2003;Carraro et al, 2006;Gallavotti et al, 2008;Bayer et al, 2009). Subsequent analyses performed in Arabidopsis suggest that the convergence of PIN1-mediated auxin transport likewise controls the initiation of lateral veins (Scarpella et al, 2006;Sawchuk et al, 2013;Verna et al, 2015). In this way, a single mechanism is proposed to pattern leaf initiation, midvein formation and lateral vein development in the eudicot leaf (reviewed in (Linh et al, 2018).…”

Section: Reticulate and Parallel Venation: Extending The Model?mentioning

confidence: 99%

On the mechanisms of development in monocot and eudicot leaves

Conklin

Strable

et al. 2018

New Phytologist

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Contents Summary I. Introduction II. Leaf zones in monocot and eudicot leaves III. Monocot and eudicot leaf initiation: differences in degree and timing, but not kind IV. Reticulate and parallel venation: extending the model? V. Flat laminar growth: patterning and coordination of adaxial-abaxial and mediolateral axes VI. Stipules and ligules: ontogeny of primordial elaborations VII. Leaf architecture VIII. Stomatal development: shared and diverged mechanisms for making epidermal pores IX. Conclusion Acknowledgements References SUMMARY: Comparisons of concepts in monocot and eudicot leaf development are presented, with attention to the morphologies and mechanisms separating these angiosperm lineages. Monocot and eudicot leaves are distinguished by the differential elaborations of upper and lower leaf zones, the formation of sheathing/nonsheathing leaf bases and vasculature patterning. We propose that monocot and eudicot leaves undergo expansion of mediolateral domains at different times in ontogeny, directly impacting features such as venation and leaf bases. Furthermore, lineage-specific mechanisms in compound leaf development are discussed. Although models for the homologies of enigmatic tissues, such as ligules and stipules, are proposed, tests of these hypotheses are rare. Likewise, comparisons of stomatal development are limited to Arabidopsis and a few grasses. Future studies may investigate correlations in the ontogenies of parallel venation and linear stomatal files in monocots, and the reticulate patterning of veins and dispersed stoma in eudicots. Although many fundamental mechanisms of leaf development are shared in eudicots and monocots, variations in the timing, degree and duration of these ontogenetic events may contribute to key differences in morphology. We anticipate that the incorporation of an ever-expanding number of sequenced genomes will enrich our understanding of the developmental mechanisms generating eudicot and monocot leaves.

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Section: Reticulate and Parallel Venation: Extending The Model?mentioning

confidence: 99%

On the mechanisms of development in monocot and eudicot leaves

Conklin

Strable

et al. 2018

New Phytologist

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“…Consider, for example, the formation of the midvein at the center of the cylindrical leaf primordium. Initially, the plasma-membrane (PM)-localized PIN-FORMED1 (PIN1) protein of Arabidopsis (Galweiler et al, 1998), which catalyzes cellular efflux of the plant signal auxin (Petrasek et al, 2006), is expressed in all the inner cells of the leaf primordium (Benkova et al, 2003; Reinhardt et al, 2003; Heisler et al, 2005; Scarpella et al, 2006; Wenzel et al, 2007; Bayer et al, 2009; Verna et al, 2015); over time, however, PIN1 expression becomes gradually restricted to the file of cells that will form the midvein. PIN1 localization at the PM of the inner cells is initially isotropic, or nearly so, but as PIN1 expression becomes restricted to the site of midvein formation, PIN1 localization becomes polarized: in the cells surrounding the developing midvein, PIN1 localization gradually changes from isotropic to medial, i.e.…”

Section: Introductionmentioning

confidence: 99%

Coordination of Tissue Cell Polarity by Auxin Transport and Signaling

Verna

Ravichandran

Sawchuk

et al. 2019

Preprint

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Coordination of polarity between cells in tissues is key to multicellular organism development. In animals, coordination of this tissue cell polarity often requires direct cellcell 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 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 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 a synergism between auxin transport and signaling and their unsuspected control by GNOM in the coordination of cell polarity during vein patterning, one of the most spectacular and informative expressions of tissue cell polarization in plants.

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“…Here we use the powerful tool of physiological genetics to address the relationships between venation, water transport, and A. A number of mutants, particularly those related to auxin biosynthesis or signaling, have reduced vein densities, aberrant vein topologies, or defective vein formation (Tobeña-Santamaria et al, 2002;Scarpella and Meijer, 2004;Cheng et al, 2006Cheng et al, , 2007Verna et al, 2015). Indeed, the auxin canalization theory, based on observations of a self-organizing flux of auxin that initiates a vascular cambium, effectively predicts the formation and development of leaf vein networks (Sachs 1981;Lee et al, 2014;Rolland-Lagan and Prusinkiewicz, 2005).…”

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confidence: 99%

Linking Auxin with Photosynthetic Rate via Leaf Venation

McAdam

Eléouët

Best³

et al. 2017

Plant Physiol.

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Land plants lose vast quantities of water to the atmosphere during photosynthetic gas exchange. In angiosperms, a complex network of veins irrigates the leaf, and it is widely held that the density and placement of these veins determines maximum leaf hydraulic capacity and thus maximum photosynthetic rate. This theory is largely based on interspecific comparisons and has never been tested using vein mutants to examine the specific impact of leaf vein morphology on plant water relations. Here we characterize mutants at the Crispoid (Crd) locus in pea (Pisum sativum), which have altered auxin homeostasis and activity in developing leaves, as well as reduced leaf vein density and aberrant placement of free-ending veinlets. This altered vein phenotype in crd mutant plants results in a significant reduction in leaf hydraulic conductance and leaf gas exchange. We find Crispoid to be a member of the YUCCA family of auxin biosynthetic genes. Our results link auxin biosynthesis with maximum photosynthetic rate through leaf venation and substantiate the theory that an increase in the density of leaf veins coupled with their efficient placement can drive increases in leaf photosynthetic capacity.

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Control of vein network topology by auxin transport

Cited by 50 publications

References 95 publications

On the mechanisms of development in monocot and eudicot leaves

On the mechanisms of development in monocot and eudicot leaves

Coordination of Tissue Cell Polarity by Auxin Transport and Signaling

Linking Auxin with Photosynthetic Rate via Leaf Venation

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