Evidence for a SAL1-PAP Chloroplast Retrograde Pathway That Functions in Drought and High Light Signaling in Arabidopsis      

Abstract

Compartmentation of the eukaryotic cell requires a complex set of subcellular messages, including multiple retrograde signals from the chloroplast and mitochondria to the nucleus, to regulate gene expression. Here, we propose that one such signal is a phosphonucleotide (39-phosphoadenosine 59-phosphate [PAP]), which accumulates in Arabidopsis thaliana in response to drought and high light (HL) stress and that the enzyme SAL1 regulates its levels by dephosphorylating PAP to AMP. SAL1 accumulates in chloroplasts and mitochondria but not in the cytosol. sal1 mutants accumulate 20-fold more PAP without a marked change in inositol phosphate levels, demonstrating that PAP is a primary in vivo substrate. Significantly, transgenic targeting of SAL1 to either the nucleus or chloroplast of sal1 mutants lowers the total PAP levels and expression of the HL-inducible ASCORBATE PEROXIDASE2 gene. This indicates that PAP must be able to move between cellular compartments. The mode of action for PAP could be inhibition of 59 to 39 exoribonucleases (XRNs), as SAL1 and the nuclear XRNs modulate the expression of a similar subset of HL and drought-inducible genes, sal1 mutants accumulate XRN substrates, and PAP can inhibit yeast (Saccharomyces cerevisiae) XRNs. We propose a SAL1-PAP retrograde pathway that can alter nuclear gene expression during HL and drought stress.

The Arabidopsis Thylakoid ADP/ATP Carrier TAAC Has an Additional Role in Supplying Plastidic Phosphoadenosine 5′-Phosphosulfate to the Cytosol

“…The 59-phosphoadenosine 39-phosphate (PAP) formed from PAPS after transfer of the sulfate group is a potent inhibitor of sulfotransferases and RNases, and its accumulation leads to large changes in gene expression, metabolite accumulation, plant morphology, and stress resistance (Estavillo et al, 2011;Lee et al, 2012). PAP is degraded to AMP and Pi by the phosphatase FIERY/Increased Salt Tolerance (FRY1/SAL1) localized in plastids, indicating again a need for a PAP transporter in plastidic membranes (Figure 1).…”

Molecular components of stress-responsive plastid retrograde signaling networks and their involvement in ammonium stress

“…[20][21][22][23][24][25] Two new plastid retrograde signals (PAP and MEcPP) during drought, high light and wounding stress responses have been revealed by two research teams, involving the analysis of the Arabidopsis mutants sal1 and ceh1, which encode the plastid nucleotidase/phosphatase SAL1 and hydroxyl-2-methyl-2-(E)-butenyl4-diphosphate synthase (HDS), respectively. 26,29 Analysis of the rps1 mutant demonstrated that the chloroplast ribosomal protein S1 (RPS1) mediates retrograde signaling to modulate the expression of the heat-responsive nuclear transcription factor HsfA2 and its target genes during heat stress, although the specific plastid retrograde signal is unknown. 30 Recently, gene cloning and transcriptional analysis of the Arabidopsis ammonium-overly-sensitive 1 (amos1) that are needed for maintaining the stability of the thylakoid membrane system under normal growth conditions.…”

“…An example of the first type can be seen in chloroplastic SAL1, a phosphatase that regulates the level of its substrate 3'-phosphoadenosine-5'-phosphate (PAP); high levels of PAP were demonstrated to accumulate in sal1 mutants. 26 Similarly, the stress-inducible nuclear HDS gene encodes a plastidial enzyme that participates in isoprenoid synthesis, converting methylerythritol cyclodiphosphate (MEcPP) to hydroxymethylbutenyl diphosphate (HMBPP) in the methylerythritol phosphate (MEP) pathway in plastids; large amounts of MEcPP were shown to accumulate in ceh1 mutants. 29 Likewise, tAPX regulates the production of H 2 O 2 in chloroplasts.…”

“…[2][3][4][5][6][7][8][9][10][11][12][13][14][15][16] More recently, several plastid retrograde signaling pathways have been identified to regulate the expression of stress-related nuclear genes during several stresses such as high light, drought, wounding, heat, and excess ammonium. [17][18][19][20][21][22][23][24][25][26][27][28][29][30][31] Based on the new stress-responsive plastid retrograde signaling pathways just reported in 2012 alone, this review will focus on properties of currently proposed molecular components in the plastid retrograde signaling network under stress. We also specifically discuss possible plastid retrograde signals involved in plant response to ammonium stress.…”

“…Several major signals, including singlet oxygen ( 1 O 2 ), 17-20 3'-phosphoadenosine 5'-phosphate (PAP), 26 hydrogen peroxide (H 2 O 2 ), 27 and methylerythritol cyclodiphosphate (MEcPP), 29 are known to be produced as metabolic intermediates in chloroplasts in response to a variety of stresses. However, the involvement of these signals remains to be established for heat and ammonium stress.…”