Uncoupling High Light Responses from Singlet Oxygen Retrograde Signaling and Spatial-Temporal Systemic Acquired Acclimation

Abstract

Distinct ROS signaling pathways initiated by singlet oxygen ( 1 O 2 ) or superoxide and hydrogen peroxide have been attributed to either cell death or acclimation, respectively. Recent studies have revealed that more complex antagonistic and synergistic relationships exist within and between these pathways. As specific chloroplastic ROS signals are difficult to study, rapid systemic signaling experiments using localized high light (HL) stress or ROS treatments were used in this study to uncouple signals required for direct HL and ROS perception and distal systemic acquired acclimation (SAA). A qPCR approach was chosen to determine local perception and distal signal reception. Analysis of a thylakoidal ascorbate peroxidase mutant (tapx), the 1 O 2 -retrograde signaling double mutant (ex1/ex2), and an apoplastic signaling double mutant (rbohD/F) revealed that tAPX and EXECUTER 1 are required for both HL and systemic acclimation stress perception. Apoplastic membrane-localized RBOHs were required for systemic spread of the signal but not for local signal induction in directly stressed tissues. Endogenous ROS treatments revealed a very strong systemic response induced by a localized 1 h induction of 1 O 2 using the conditional flu mutant. A qPCR time course of 1 O 2 induced systemic marker genes in directly and indirectly connected leaves revealed a direct vascular connection component of both immediate and longer term SAA signaling responses. These results reveal the importance of an EXECUTER-dependent 1 O 2 retrograde signal for both local and long distance RBOH-dependent acclimation signaling that is distinct from other HL signaling pathways, and that direct vascular connections have a role in spatial-temporal SAA induction.

Maintenance of pre‐existing DNA methylation states through recurring excess‐light stress

“…A simplistic model of retained alterations in leaf structure is difficult to reconcile with a leaf developed largely in the absence of stress, with newly developed chloroplasts displaying an altered requirement for NPQ. Contributions of systemic signals emanating from the exposed tissue to the newly developed or emerging tissue, such as carotenoid oxidation products, reactive oxygen species, or mobile small RNAs (Carmody et al, 2016;Lewsey et al, 2016;Ramel et al, 2012), or the direct exposure of the apical meristem to EL in this study might underpin our observations. To confirm whether this is an SAA-mediated phenomenon may involve confirming the transmission of these traits in SAA-impaired mutants such as RbohD (Miller et al, 2009 comparable with pre-existing leaves, but this was not observed.…”

“…Indeed, the spread of systemic acquired resistance to biotic stresses has been reported to be accompanied by histone modifications including methylation, acetylation, and replacement (Jaskiewicz, Conrath, & Peterhänsel, 2011;March-Díaz et al, 2008). A common output of SAA mediated EL stress priming is the pre-emptive accumulation of photoprotection associated transcripts (Carmody et al, 2016;Gordon et al, 2013;Rossel et al, 2007). Although propagation of this is often attributed to mobile signals generated at the site of EL stress (Carmody et al, 2016;Ramel et al, 2012;Suzuki et al, 2013), a hitherto untested hypothesis is the contribution of maintained chromatin variation towards sustained photoacclimation in newly developed tissue (memory).…”

“…Priming of PSII has been demonstrated in response to oxidative stress (Karpinski et al, ) and recurring EL stress, through improved photochemical efficiency and enhanced NPQ, in both exposed and newly developed tissue (Gordon et al, ; Szechyńska‐Hebda, Kruk, Górecka, Karpińska, & Karpiński, ). This occurred regardless of the area of tissue effected as targeted, or partial rosette, EL treatments still resulted in a whole rosette response and acclimation, demonstrable through enhanced induction of light‐response transcripts, and improved photoprotective capacity and photo‐oxidative tolerance (Carmody et al, ; Gordon et al, ; Karpinski et al, ; Rossel et al, ; Szechyńska‐Hebda et al, ). Indeed, using a partial rosette treatment revealed an 87% overlap in transcriptional changes between exposed and distal tissues (Rossel et al, ).…”

“…Systemic acquired acclimation (SAA) has been elucidated as a key signalling mechanism for relaying photoacclimation to a whole plant level; whereby leaves experiencing EL stress actively signal, through a variety of metabolic and oxidative molecules (Carmody et al, 2016;Gordon et al, 2013;Ramel et al, 2012;Suzuki et al, 2013), to unexposed leaves to promote a "primed" state (Conrath et al, 2006) in anticipation for incoming EL stress (Karpinski et al, 1999;Rossel et al, 2007). Priming of PSII has been demonstrated in response to oxidative stress (Karpinski et al, 1999) and recurring EL stress, through improved photochemical efficiency and enhanced NPQ, in both exposed and newly developed tissue (Gordon et al, 2013;Szechyńska-Hebda, Kruk, Górecka, Karpińska, & Karpiński, 2010).…”

FtsH2-Dependent Proteolysis of EXECUTER1 Is Essential in Mediating Singlet Oxygen-Triggered Retrograde Signaling in Arabidopsis thaliana

“…In a very recent study, however, the role of EX1 and EX2 in an acclimation response to high light-induced transcriptional reprogramming has also been demonstrated (Carmody et al, 2016). To get insight into these distinctive cascades, we compared the β-CC-induced SORGs and EX1-FtsH2-dependent ESORGs, with the aim to explain the common and distinct molecular characteristics and enlighten their coexistence.…”