The protein phosphatase PC1 dephosphorylates and deactivates CatC to negatively regulate H2O2 homeostasis and salt tolerance in rice

Abstract

Catalase (CAT) is often phosphorylated and activated by protein kinases to maintain hydrogen peroxide (H2O2) homeostasis and protect cells against stresses, but whether and how CAT is switched off by protein phosphatases remains inconclusive. Here, we identified a manganese (Mn2+)-dependent protein phosphatase, which we named PHOSPHATASE OF CATALASE 1 (PC1), from rice (Oryza sativa L.) that negatively regulates salt and oxidative stress tolerance. PC1 specifically dephosphorylates CatC at Ser-9 to inhibit its tetramerization and thus activity in the peroxisome. PC1 overexpressing lines exhibited hypersensitivity to salt and oxidative stresses with a lower phospho-serine level of CATs. Phosphatase activity and seminal root growth assays indicated that PC1 promotes growth and plays a vital role during the transition from salt stress to normal growth conditions. Our findings demonstrate that PC1 acts as a molecular switch to dephosphorylate and deactivate CatC and negatively regulate H2O2 homeostasis and salt tolerance in rice. Moreover, knockout of PC1 not only improved H2O2-scavenging capacity and salt tolerance, but also limited rice grain yield loss under salt stress conditions. Together, these results shed light on the mechanisms that switch off CAT and provide a strategy for breeding highly salt-tolerant rice.

Evidence for dual targeting control of Arabidopsis 6-phosphogluconate dehydrogenase isoforms by N-terminal phosphorylation

“…Under certain conditions (stress/oxidative transients in the cytosol), a kinase is activated that leads to early (or even co-translational) phosphorylation of the PGD N-termini, which allows partner proteins (such as 14-3-3) to bind and enables efficient import of monomeric PGD2 subunits via Pex5 into peroxisomes (and of PGD1/3 into plastids). Phosphatase activity at the target locations is needed to enable dimer formation as a prerequisite for catalytic activity of the dehydrogenases, which is also present in peroxisomes ( Kataya et al , 2016 ; Liu et al , 2023 ). Concerning the need for early/co-translational phosphorylation of the PGD N-termini, known interaction of translating polysomes with the actin cytoskeleton ( Davies et al , 1991 ; Klyachko et al , 2000 ) that is also involved in mediating the close proximity of plastids with peroxisomes—especially during photosynthesis ( Oikawa et al, 2015 )—should surely be beneficial for stimulus-induced efficient organelle import ( Fig.…”

“…Our results suggest exclusive import of folded PGD2 monomers, which is in line with earlier reports on catalase subunits and other peroxisomal proteins in mammalian cells ( Freitas et al , 2015 ). In fact, tetramerization of catalase was recently shown to be regulated by de-phosphorylation in rice peroxisomes ( Liu et al , 2023 ). This is strong additional support for our findings, with the cytosolic kinase responsible for the complete localization shift remaining to be identified.…”

Review of Crop Response to Soil Salinity Stress: Possible Approaches from Leaching to Nano-Management

“…There are many suggested mechanisms to adapt cultivated crops to different salty soil environments [34]. These proposed mechanisms include mediating plant hormone signaling [36,38], regulating ion homeostasis [39], activating the osmotic stress pathway [40], and regulating cell wall organization [41]. Understanding these mechanisms, including different physiological, biochemical, and molecular responses to salinity stress, are considered crucial strategies to improve agricultural crop productivity [42,43].…”