Distinct redox behaviors of chloroplast thiol enzymes and their relationships with photosynthetic electron transport in Arabidopsis thaliana.
The thiol/disulfide redox network mediated by the thioredoxin (Trx) system in chloroplasts ensures light-responsive control of diverse crucial functions. Despite the suggested importance of this system, the working dynamics against changing light environments remains largely unknown. Thus, we directly assessed the in vivo redox behavior of chloroplast Trx-targeted thiol enzymes in Arabidopsis thaliana. In a time-course analysis throughout a day period that was artificially mimicked to natural light conditions, thiol enzymes showed a light-dependent shift in redox state, but the patterns were distinct among thiol enzymes. Notably, the ATP synthase CF(1-γ) subunit was rapidly reduced even under low-light conditions, whereas the stromal thiol enzymes fructose 1,6-bisphosphatase, sedoheptulose 1,7-bisphosphatase, and NADP-malate dehydrogenase were gradually reduced/re-oxidized along with the increase/decrease in light intensity. Photo-reduction of thiol enzymes was suppressed by the impairment of photosynthetic linear electron transport using DCMU and 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone, but sensitivity to the impairment was uneven between CF(1-γ) and other stromal thiol enzymes. These different dependencies of photo-reduction on electron transport, rather than the redox state of Trx and the circadian clock, could readily explain the distinct diurnal redox behaviors of thiol enzymes. In addition, our results indicate that the cyclic electron transport around PSI is also involved in redox regulation of some thiol enzymes. Based on these findings, we propose an in vivo working model of the redox regulation system in chloroplasts.
Chemical Resources Laboratory, Tokyo Institute of Technology, Nagatsuta 4259-R1-8, Midori-ku, Yokohama, 226-8503 JapanCore Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Tokyo, 102-0075 Japan.
Keisuke
K
Yoshida
Chemical Resources Laboratory, Tokyo Institute of Technology, Nagatsuta 4259-R1-8, Midori-ku, Yokohama, 226-8503 Japan.
Yuta
Y
Matsuoka
Chemical Resources Laboratory, Tokyo Institute of Technology, Nagatsuta 4259-R1-8, Midori-ku, Yokohama, 226-8503 Japan.
Satoshi
S
Hara
Chemical Resources Laboratory, Tokyo Institute of Technology, Nagatsuta 4259-R1-8, Midori-ku, Yokohama, 226-8503 JapanImaging Research Division, Bio-AFM Frontier Research Center, Kanazawa University, Kakuma, Kanazawa, 920-1192 Japan.
Hiroki
H
Konno
Chemical Resources Laboratory, Tokyo Institute of Technology, Nagatsuta 4259-R1-8, Midori-ku, Yokohama, 226-8503 JapanCore Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Tokyo, 102-0075 Japan thisabor@res.titech.ac.jp.
Toru
T
Hisabori
D000968:Antimycin A / Q000494:pharmacology; D017360:Arabidopsis / Q000187:drug effects / Q000201:enzymology* / Q000235:genetics / Q000528:radiation effects; D029681:Arabidopsis Proteins / Q000037:antagonists & inhibitors*; D025222:Chloroplast Proton-Translocating ATPases / Q000037:antagonists & inhibitors; D002736:Chloroplasts / Q000201:enzymology*; D002940:Circadian Rhythm; D003991:Dibromothymoquinone / Q000494:pharmacology; D004237:Diuron / Q000494:pharmacology; D004579:Electron Transport / Q000187:drug effects; D006597:Fructose-Bisphosphatase / Q000037:antagonists & inhibitors; D015971:Gene Expression Regulation, Enzymologic; D018506:Gene Expression Regulation, Plant; D006540:Herbicides / Q000494:pharmacology; D008027:Light; D050538:Malate Dehydrogenase (NADP+) / Q000037:antagonists & inhibitors; D008954:Models, Biological; D009154:Mutation; D010084:Oxidation-Reduction; D010744:Phosphoric Monoester Hydrolases / Q000037:antagonists & inhibitors; D010788:Photosynthesis; D045331:Photosystem I Protein Complex / Q000378:metabolism; D018515:Plant Leaves / Q000187:drug effects / Q000235:genetics / Q000378:metabolism / Q000528:radiation effects; D013879:Thioredoxins / Q000378:metabolism
D029681:Arabidopsis Proteins; D006540:Herbicides; D045331:Photosystem I Protein Complex; D003991:Dibromothymoquinone; D013879:Thioredoxins; D000968:Antimycin A; D004237:Diuron; D050538:Malate Dehydrogenase (NADP+); D006597:Fructose-Bisphosphatase; D010744:Phosphoric Monoester Hydrolases; C022627:sedoheptulose-bisphosphatase; D025222:Chloroplast Proton-Translocating ATPases
Arabidopsis thaliana; Chloroplast; Photosynthetic electron transport; Redox regulation; Thiol enzymes; Thioredoxin (Trx)