Long‐distance communication in Arabidopsis involving a self‐activating G protein

Abstract

In plant cells, heterotrimeric G protein signaling mediates development, biotic/abiotic stress responsiveness, hormone signaling, and extracellular sugar sensing. The amount of sugar in plant cells fluctuates from nanomolar to high millimolar concentrations over time depending on changes in the light environment. Arabidopsis thaliana Regulator of G Signaling protein 1 (AtRGS1) modulates G protein activation and detects the concentration and the exposure time of sugars. This is called dose–duration reciprocity in sugar sensing and occurs through AtRGS1 internalization which is directly proportional to G protein activation. One source of sugars is from CO2 fixation by photosynthesis. Through a simple set of experiments, we show that sugars made in cotyledons that are undergoing photomorphogenesis activate G signaling in cells distal to the nascent photosynthesis center. This occurs with sufficient speed to enable distal cells to monitor changes in photosynthetic activity in the leaves.

Differential regulation of G protein signaling in Arabidopsis through two distinct pathways that internalize AtRGS1

“…Therefore, an extracellular glucose/metabolite detection system may be more appropriate for monitoring sugars produced by photosynthesis for real-time information. This is consistent with the finding that AtRGS1 is important for detecting fluctuations in CO 2 -fixed sugar in the minute time range over the diel cycle ( 15 , 61 ).…”

“…It is already established that flg22 is perceived extracellularly ( 12 ) by the co-receptors BRASSINOSTEROID INSENSITIVE 1 (BAK1) and FLAGELLIN-SENSITIVE 2 (FLS2), both receptor-like kinases (RLK), as part of a larger G protein complex ( 13 , 14 ). Another signal is glucose or a glucose metabolite, which are products of photosynthesis ( 15 ) and metabolism of starch stores ( 16 ).…”

Light regulates alternative splicing outcomes via the TOR kinase pathway

“…Sugars have been shown to repress SnRK1.1 (AT3G01090) ( Baena-González et al, 2007 ) and to activate TOR kinase (AT1G50030) ( Dobrenel et al, 2016a ). Moreover, it was previously shown that sugars derived from photosynthesis activate the root meristem through TOR ( Xiong et al, 2013 ), modulate G protein activity in a long-distance communication pathway ( Tunc-Ozdemir et al, 2018 ), and regulate alternative splicing in etiolated seedlings ( Hartmann et al, 2016 ). Here, we show that by activating the TOR pathway in roots, sugars act as mobile signals to coordinate alternative splicing responses to light throughout the whole plant.…”

Nudge‐nudge, WNK‐WNK (kinases), say no more?

“…Less substrate projects a high proportion of phosphorylated AtRGS1, while a high number of AtRGS1 projects a low proportion of phosphorylated AtRGS1 (Liao et al, 2017a,b). From a physiological perspective, this complex dynamics of AtRGS1 pool sizes imparts upon the plant the ability to distinguish shadows from flickers and from the end of day (Liao et al, 2017a) and for cells distal to the photosynthetic centers, such as roots, to receive information of the state of autotrophy (Tunc-Ozdemir et al, 2018).…”