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Functional analysis of a putative master regulator of plant development, the Translationally-Controlled Tumour Protein

Branco, Remi

Description

Being sessile, plants need to accurately coordinate leaf and root growth to adapt to changing environmental conditions. TCTP (Translationally Controlled Tumour Protein) belongs to a conserved gene family, present in all eukaryotes. In animals, TCTP controls several core cellular processes including apoptosis, cellular proliferation and growth, tissue patterning, and is thought to interact with the TOR (Target Of Rapamycin) pathway. Plant TCTPs are little known, however, but recent studies...[Show more]

dc.contributor.authorBranco, Remi
dc.date.accessioned2020-09-10T04:32:28Z
dc.date.available2020-09-10T04:32:28Z
dc.identifier.urihttp://hdl.handle.net/1885/209920
dc.description.abstractBeing sessile, plants need to accurately coordinate leaf and root growth to adapt to changing environmental conditions. TCTP (Translationally Controlled Tumour Protein) belongs to a conserved gene family, present in all eukaryotes. In animals, TCTP controls several core cellular processes including apoptosis, cellular proliferation and growth, tissue patterning, and is thought to interact with the TOR (Target Of Rapamycin) pathway. Plant TCTPs are little known, however, but recent studies suggest functional similarities with animal TCTPs. What functions they assume is still a matter of debate and how they promote organ and whole organism growth is controversial, although they are widely described as mitotic activators, but with no role in cellular growth. In addition, plant TCTPs have never been shown to have extracellular functions and act as signalling molecules as known of animal TCTPs. This Thesis investigates TCTP function in plant development. Using Arabidopsis as a model plant species, and focusing on AtTCTP1, I probe the role of AtTCTP1 in the expansive growth of non-proliferative cells; I explore the AtTCTP1 molecular pathway in the control of root elongation and embryogenesis; and I investigate the physiological relevance to root development of AtTCTP1 mRNA and protein mobility. To fulfil these aims I carried out a kinematics analysis of primary root and hypocotyl development. This included the development of a custom imaging and bioinformatic pipeline for in situ, high throughput acquisition of spatial profiles of cell sizes and expansion rates. The results demonstrate that AtTCTP1 acts in the positioning of frontiers between proliferating, expanding only, and maturing cells in roots; controls cell size at division, hence the balance between expansion and partitioning rates in meristematic cells; and promotes the growth and final size of non-proliferative cells, in the root elongation zone and also the hypocotyl, indicating this is a likely a general function. Supporting this, TCTP1 also promotes tip growth in root hairs. Taken together, these results demonstrate that, similar to animal TCTP, plant TCTP is a pivotal cell and organ growth controller. Combining genetic, microscopy and pharmacological approaches I next demonstrate that TCTP1 constitutes an upstream component of the core TOR pathway, and is crucial to its activation. Moreover, I establish the function in root development of a small GTPase as an effector of TCTP-mediated activation of the TOR pathway. To investigate the possibility that plant TCTPs may also have a signalling role in root development, I used a micrografting technique to generate heterografts between Arabidopsis TCTP1 transgenic and wild type seedlings, including seedlings expressing a TCTP1::GFP fusion protein. I monitored rootstock elongation and branching in relation to the patterns of GFP signal and the respective genotypes of root-stock and scion. These experiments demonstrated the existence of bi-directional movement of AtTCTP1 mRNA between scion and rootstock, and an active, destination-controlled accumulation of shoot-derived TCTP1 protein at sites of lateral root initiation. Long-distance mobility of shoot TCTP1 mRNA promotes lateral root initiation and emergence, and appears as one of the elusive controllers of the spatial patterning of lateral roots along the primary root. Remarkably, TCTP1 rootward mobility modulated root system architecture without impacting the overall length of root produced. This points to a role of AtTCTP1 gene products in the regulation of the trade-off for a root between branching or elongating more, to greater depth. These findings provide the first evidence of an extracellular function of TCTPs in plants. Altogether, this work introduces a new paradigm for the physiological roles of plant TCTPs, positioning them as agents of systemic signalling between leaves and roots, and essential coordinators of cell proliferation and growth, upstream of TOR.
dc.language.isoen_AU
dc.titleFunctional analysis of a putative master regulator of plant development, the Translationally-Controlled Tumour Protein
dc.typeThesis (PhD)
local.contributor.supervisorMasle, Josette
local.contributor.supervisorcontactu8805691@anu.edu.au
dc.date.issued2020
local.contributor.affiliationResearch School of Biology, ANU College of Science, The Australian National University
local.identifier.doi10.25911/5f6b247368978
local.identifier.proquestNo
local.identifier.researcherIDAAE-1882-2020
local.thesisANUonly.author858642f1-6510-4fef-bf47-61bab8b0f498
local.thesisANUonly.title000000014502_TC_1
local.thesisANUonly.key0446cee0-d3d5-14fc-e297-33658da9cf55
local.mintdoimint
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