TOR dynamically regulates plant cell–cell transport

Abstract

The coordinated redistribution of sugars from mature “source” leaves to developing “sink” leaves requires tight regulation of sugar transport between cells via plasmodesmata (PD). Although fundamental to plant physiology, the mechanisms that control PD transport and thereby support development of new leaves have remained elusive. From a forward genetic screen for altered PD transport, we discovered that the conserved eukaryotic glucose-TOR (TARGET OF RAPAMYCIN) metabolic signaling network restricts PD transport in leaves. Genetic approaches and chemical or physiological treatments to either promote or disrupt TOR activity demonstrate that glucose-activated TOR decreases PD transport in leaves. We further found that TOR is significantly more active in mature leaves photosynthesizing excess sugars than in young, growing leaves, and that this increase in TOR activity correlates with decreased rates of PD transport. We conclude that leaf cells regulate PD trafficking in response to changing carbohydrate availability monitored by the TOR pathway.

Parallel global profiling of plant TOR dynamics reveals a conserved role for LARP1 in translation

“…TOR and several of its interactors are conserved across eukaryotes, but many distinct upstream regulators and downstream effectors of TOR have evolved in different lineages ( Brunkard et al, 2020 ; Chantranupong et al, 2015 ; Shi et al, 2018 ). Using parallel global profiling methods for unbiased screening, we sought to uncover both new and conserved components of the TOR signaling network in Arabidopsis thaliana seedlings.…”

“…Recently, we proposed that the TOR metabolic signaling network evolves through exaptation by coopting existing pathways to serve new functions relevant to specific lineages ( Brunkard, 2020 ). For example, TOR gained new functions when eukaryotic lineages evolved multicellularity, such as coordinating plasmodesmatal (intercellular) transport in plants ( Brunkard et al, 2020 ) or regulating cellular differentiation and cell type-specific metabolisms in humans ( Brunkard, 2020 ; Kosillo et al, 2019 ), as examples. Similarly, here, we provide evidence that plants exapted the TOR-LARP1-5′TOP signaling axis to regulate translation of proteins involved in developmental patterning and auxin signaling ( Figure 5G ), pathways that did not exist in the unicellular ancestor of plants and animals that first evolved TOR-LARP1-5′TOP signaling.…”

The Morphoregulatory Role of Thidiazuron: Metabolomics-Guided Hypothesis Generation for Mechanisms of Activity

“…One of the first hypotheses for induction of regeneration was control of the uptake of nutrients from the culture media and maintenance of osmotic turgor in the isolated cells [ 50 ]. Sugar source-sink relationships are dependent on both passive and active transport across cell membranes and through plasmodesmata [ 51 , 52 , 53 ]. Our data suggest that TDZ may interact with one of the active sugar transporters to modulate uptake of 5C and 6C sugars from the culture media, with our results suggesting that it may favor uptake of 6C sugars.…”

“…TDZ is a particularly effective PGR that can fulfill the role of the inductive signal of both auxins and cytokinins in many recalcitrant species [ 2 ]. Cells must be competent to accept the inductive signal and initiate a developmental pathway toward regeneration via organogenesis or embryogenesis ( Figure 10 ) [ 51 , 73 , 74 ]. In diverse species such as geraniums, African violet and peanut ( Arachis hypogea ), TDZ induces somatic embryogenesis alone or in addition to shoot organogenesis [ 24 , 33 , 75 , 76 , 77 ].…”

Target of Rapamycin in Control of Autophagy: Puppet Master and Signal Integrator

“…However, in mammals and flies the TEL2–TTI1–TTI2 (TTT)–RUVBL1/2 complex causes TORC1 dimerization, which is necessary for its translocation to the lysosomal membrane and activation in response to glucose/energy availability [ 161 , 162 , 163 ]. Since the Arabidopsis genome contains putative orthologous genes encoding TEL2–TTI1–TTI2 and RUVBLs [ 164 ], a similar mechanism may exist in plants, although this awaits experimental evidence. Glucose activation of TOR could also be mediated by inactivation of SnRK1, which is an ortholog of mammalian AMPK and is a major energy sensor [ 163 , 165 ].…”