TY - JOUR
T1 - Dissecting the Role of SAL1 in Metabolizing the Stress Signaling Molecule 3′-Phosphoadenosine 5′-Phosphate in Different Cell Compartments
AU - Ashykhmina, Natallia
AU - Chan, Kai Xun
AU - Frerigmann, Henning
AU - Van Breusegem, Frank
AU - Kopriva, Stanislav
AU - Flügge, Ulf Ingo
AU - Gigolashvili, Tamara
N1 - Publisher Copyright:
Copyright © 2022 Ashykhmina, Chan, Frerigmann, Van Breusegem, Kopriva, Flügge and Gigolashvili.
PY - 2022/1/21
Y1 - 2022/1/21
N2 - Plants possess the most highly compartmentalized eukaryotic cells. To coordinate their intracellular functions, plastids and the mitochondria are dependent on the flow of information to and from the nuclei, known as retrograde and anterograde signals. One mobile retrograde signaling molecule is the monophosphate 3′-phosphoadenosine 5′-phosphate (PAP), which is mainly produced from 3′-phosphoadenosine 5′-phosphosulfate (PAPS) in the cytosol and regulates the expression of a set of nuclear genes that modulate plant growth in response to biotic and abiotic stresses. The adenosine bisphosphate phosphatase enzyme SAL1 dephosphorylates PAP to AMP in plastids and the mitochondria, but can also rescue sal1 Arabidopsis phenotypes (PAP accumulation, leaf morphology, growth, etc.) when expressed in the cytosol and the nucleus. To understand better the roles of the SAL1 protein in chloroplasts, the mitochondria, nuclei, and the cytosol, we have attempted to complement the sal1 mutant by specifically cargoing the transgenic SAL1 protein to these four cell compartments. Overexpression of SAL1 protein targeted to the nucleus or the mitochondria alone, or co-targeted to chloroplasts and the mitochondria, complemented most aspects of the sal1 phenotypes. Notably, targeting SAL1 to chloroplasts or the cytosol did not effectively rescue the sal1 phenotypes as these transgenic lines accumulated very low levels of SAL1 protein despite overexpressing SAL1 mRNA, suggesting a possibly lower stability of the SAL1 protein in these compartments. The diverse transgenic SAL1 lines exhibited a range of PAP levels. The latter needs to reach certain thresholds in the cell for its impacts on different processes such as leaf growth, regulation of rosette morphology, sulfate homeostasis, and glucosinolate biosynthesis. Collectively, these findings provide an initial platform for further dissection of the role of the SAL1–PAP pathway in different cellular processes under stress conditions.
AB - Plants possess the most highly compartmentalized eukaryotic cells. To coordinate their intracellular functions, plastids and the mitochondria are dependent on the flow of information to and from the nuclei, known as retrograde and anterograde signals. One mobile retrograde signaling molecule is the monophosphate 3′-phosphoadenosine 5′-phosphate (PAP), which is mainly produced from 3′-phosphoadenosine 5′-phosphosulfate (PAPS) in the cytosol and regulates the expression of a set of nuclear genes that modulate plant growth in response to biotic and abiotic stresses. The adenosine bisphosphate phosphatase enzyme SAL1 dephosphorylates PAP to AMP in plastids and the mitochondria, but can also rescue sal1 Arabidopsis phenotypes (PAP accumulation, leaf morphology, growth, etc.) when expressed in the cytosol and the nucleus. To understand better the roles of the SAL1 protein in chloroplasts, the mitochondria, nuclei, and the cytosol, we have attempted to complement the sal1 mutant by specifically cargoing the transgenic SAL1 protein to these four cell compartments. Overexpression of SAL1 protein targeted to the nucleus or the mitochondria alone, or co-targeted to chloroplasts and the mitochondria, complemented most aspects of the sal1 phenotypes. Notably, targeting SAL1 to chloroplasts or the cytosol did not effectively rescue the sal1 phenotypes as these transgenic lines accumulated very low levels of SAL1 protein despite overexpressing SAL1 mRNA, suggesting a possibly lower stability of the SAL1 protein in these compartments. The diverse transgenic SAL1 lines exhibited a range of PAP levels. The latter needs to reach certain thresholds in the cell for its impacts on different processes such as leaf growth, regulation of rosette morphology, sulfate homeostasis, and glucosinolate biosynthesis. Collectively, these findings provide an initial platform for further dissection of the role of the SAL1–PAP pathway in different cellular processes under stress conditions.
KW - 3′-phosphoadenosine 5′-phosphate (PAP)
KW - SAL1
KW - chloroplasts
KW - cytosol
KW - metabolite signaling
KW - mitochondria
KW - nuclei
KW - nucleotidase/phosphatase
UR - http://www.scopus.com/inward/record.url?scp=85124099619&partnerID=8YFLogxK
U2 - 10.3389/fmolb.2021.763795
DO - 10.3389/fmolb.2021.763795
M3 - Article
SN - 2296-889X
VL - 8
JO - Frontiers in Molecular Biosciences
JF - Frontiers in Molecular Biosciences
M1 - 763795
ER -