3′-Phosphoadenosine 5′-Phosphate Accumulation Delays the Circadian System

Abstract

The circadian system optimizes cellular responses to stress, but the signaling pathways that convey the metabolic consequences of stress into this molecular timekeeping mechanism remain unclear. Redox regulation of the SAL1 phosphatase during abiotic stress initiates a signaling pathway from chloroplast to nucleus by regulating the accumulation of a metabolite, 3'-phosphoadenosine 5'-phosphate (PAP). Consequently, PAP accumulates in response to redox stress and inhibits the activity of exoribonucleases (XRNs) in the nucleus and cytosol. We demonstrated that osmotic stress induces a lengthening of circadian period and that genetically inducing the SAL1-PAP-XRN pathway in plants lacking either SAL1 or XRNs similarly delays the circadian system. Exogenous application of PAP was also sufficient to extend circadian period. Thus, SAL1-PAP-XRN signaling likely regulates circadian rhythms in response to redox stress. Our findings exemplify how two central processes in plants, molecular timekeeping and responses to abiotic stress, can be interlinked to regulate gene expression.

Retrograde signalling as an informant of circadian timing

“…Loss of XRN function leads to the accumulation of uncapped RNAs, such as those generated from microRNA (miRNA) processing (Kurihara et al ., ). Interestingly, either the accumulation of PAP or the loss of XRN activity is sufficient to extend circadian period (Litthauer et al ., ). Although the mechanism underlying this phenotype remains unclear, such data are consistent with previous reports showing that gross defects in RNA processing slow circadian progression (Nolte & Staiger, ).…”

“…Tansley insight New Phytologist intermediaries that can subsequently be transported from the mitochondria or chloroplasts to the nucleus (Chan et al, 2016b;Mullineaux et al, 2018). With regard to circadian rhythmicity, high temperatures are sufficient to slow the circadian oscillator, and the circadian system is also delayed by osmotic stress (Gil et al, 2017;Litthauer et al, 2018). As with many stress responses, the question now facing the field is whether the clock is slowed under these environmental conditions as part of a generalized reaction to cellular damage, or whether specific retrograde signals delay circadian progression as part of an adaptive response.…”

Sulfation pathways from red to green

“…A common denomination, FIERY1 or FRY1, comes from a screen for mutants in abscisic acid and stress signaling, where its loss-of-function resulted in hyperinduction of the luciferase reporter gene driven by stress-responsible promoter (126). The phenotypes observed in the various alleles of sal1 mutants include cold and drought tolerance and signaling (122,127), leaf shape and venation pattern (123), RNA silencing (115), increased jasmonate levels (128), glucosinolate and sulfur accumulation (9), lateral root formation (129), increasing circadian period (130), and many others. Initially it was believed that these phenotypes are caused by defects in inositol phosphate signaling (126), but current evidence points to PAP being the main factor (8,9,131,132), thus linking sulfation pathways with a number of cellular processes.…”

Secondary sulfur metabolism in cellular signalling and oxidative stress responses

“…PAP accumulation concurrently up-regulates stress homeostasis genes and suppresses growth (Estavillo et al, 2011;Phua et al, 2018b;Rossel et al, 2006;Wilson et al, 2009). One possible mechanism by which PAP regulates growth and metabolism over short periods of drought stress is by extending the circadian period (Litthauer et al, 2018). Both sal1 and xrn mutants have extended circardian period and application of osmotic stress also prolongs the circardian clock (Litthauer et al, 2018).…”

“…One possible mechanism by which PAP regulates growth and metabolism over short periods of drought stress is by extending the circadian period (Litthauer et al, 2018). Both sal1 and xrn mutants have extended circardian period and application of osmotic stress also prolongs the circardian clock (Litthauer et al, 2018). Primary metabolism and growth are strongly associated with circadian regulation; thus PAP together with other signal(s) might contribute to the regulation of these processes during oxidative stress .…”