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Permanent link (DOI): https://doi.org/10.7939/R3K931H4F

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Control of Arabidopsis vein-network formation by auxin transport Open Access

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Other title
Subject/Keyword
Arabidopsis
vein-network formation
auxin transport
Type of item
Thesis
Degree grantor
University of Alberta
Author or creator
Sawchuk, Megan G
Supervisor and department
Scarpella, Enrico (Department of Biological Sciences)
Examining committee member and department
Kav, Nat (Agricultural, Food & Nutritional Science)
Deyholos, Michael (Department of Biological Sciences)
Hacke, Uwe (Renewable Resources)
Prusinkiewicz, Przemyslaw (University of Calgary)
Department
Department of Biological Sciences
Specialization
Plant Biology
Date accepted
2014-06-03T10:53:21Z
Graduation date
2014-11
Degree
Doctor of Philosophy
Degree level
Doctoral
Abstract
Most multicellular organisms form tissue networks for transport function. What controls the formation of tissue networks is thus a central question in biology. In animals, the formation of these networks often involves extensive cell movements—movements that are instead prevented in plants by a wall that holds cells in place; thus plants are a simplified system in which to address the question of tissue network formation. The vein networks of plant leaves are among the most spectacular examples of tissue networks, and as such the principles controlling their formation have inspired artists and scientists since time immemorial. From a developmental standpoint, this interest seems justified, as vein networks are formed progressively during leaf development by the iteration of initiation, continuation and termination of vein formation. An additional, equally intriguing feature of vein networks is that they are both reproducible and variable. Consider, for example, the vein networks in leaves of Arabidopsis thaliana: lateral veins branch off from a central midvein and join distal veins to form closed loops, and minor veins branch off from midvein and loops to end freely in the leaf or join other veins. Whereas these pattern features of vein networks are reproducible, other features of vein networks, such as the number of veins and the extent of their interconnectedness, are variable. Such coexisting reproducibility and variability argue against a tight specification of vein networks and instead suggest an iterative, self-organizing vein-formation mechanism that functionally integrates vein network formation with leaf growth. Varied evidence implicates the plant signalling molecule auxin and its polar transport through plant tissues in the control of vein network formation: (i) Expression of the PIN-FORMED1 (PIN1) auxin effluxer of Arabidopsis is iteratively initiated in broad domains of leaf inner cells that become gradually restricted to files of vascular precursor cells in contact with pre-existing, narrow PIN1 expression domains. Within broad expression domains, PIN1 is localized isotropically—or nearly so—at the plasma membrane of leaf inner cells. As expression of PIN1 becomes gradually restricted to files of vascular precursor cells, PIN1 localization becomes polarized to the side of the plasma membrane facing the pre-existing, narrow PIN1 expression domains with which the narrowing domains are in contact. (ii) Auxin application to developing leaves induces formation of broad expression domains of isotropically localized PIN1; such domains become restricted to the sites of auxin-induced vein formation, and PIN1 localization becomes polarized toward the pre-existing vasculature. (iii) Both the restriction of PIN1 expression and the polarization of PIN1 localization that occur during normal leaf development are slowed down by chemical inhibition of auxin transport. (iv) Auxin transport inhibitors induce characteristic and reproducible vein-pattern defects, similar to—though stronger than—those of pin1 mutants. Thus available evidence suggests that auxin induces the polar formation of vein networks, and that such inductive and orienting property of auxin strictly depends on the function of PIN1 and possibly of the other seven PIN genes. Here I tested this hypothesis. My results suggest that: (i) PIN1 is the only PIN gene with non-redundant functions in vein patterning; PIN3, PIN4 and PIN7 act redundantly with PIN1 in vein patterning; and PIN6 and PIN8 inhibit the negative function of PIN5 in PIN1-dependent vein patterning. Further, PIN1 non-redundantly inhibits vein network formation; PIN6 acts redundantly with PIN1 in inhibition of vein network formation; PIN8 acts redundantly with PIN6 in PIN1-dependent inhibition of vein network formation; and PIN6 and PIN8 redundantly inhibit—independently of PIN1—the positive function of PIN5 in vein network formation. (ii) Auxin-induced polar vein formation occurs in the absence of the function of PIN proteins or of any known intercellular auxin transporter. (iii) The vein-forming and -patterning activity independent of carrier-mediated auxin transport relies, at least in part, on the auxin signal transduction mediated by the TRANSPORT INHIBITOR RESPONSE1/AUXIN SIGNALLING F-BOX (TIR1/AFB) auxin receptors and the MONOPTEROS (MP) auxin-responsive transcription factor. (iv) A polarizing signal that depends on the function of the GNOM guanine-nucleotide exchange factor for ADP-rybosilation-factor GTPases acts upstream of carrier-mediated auxin transport and TIR1/AFB/MP-mediated auxin signalling in vein formation and patterning. My results define genetic interaction networks controlling vein patterning and network formation.
Language
English
DOI
doi:10.7939/R3K931H4F
Rights
This thesis is made available by the University of Alberta Libraries with permission of the copyright owner solely for the purpose of private, scholarly or scientific research. This thesis, or any portion thereof, may not otherwise be copied or reproduced without the written consent of the copyright owner, except to the extent permitted by Canadian copyright law.
Citation for previous publication
MG Sawchuk and E Scarpella, “Polarity, Continuity, and Alignment in Plant Vascular Strands,” Journal of Integrative Plant Biology, volume 55, issue 9, 824-834.MG Sawchuk, A Edgar and E Scarpella, “Patterning of Leaf Vein Networks by Convergent Auxin Transport Pathways,” PLoS Genetics, volume 9, issue 2, e1003294.O Odat, J Gardiner, MG Sawchuk, C Verna, TJ Donner and E Scarpella, “Characterization of an allelic series in the MONOPTEROS gene of Arabidopsis,” genesis, volume 52, issue 2, 127-133.

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