title: Defects in the Expression of Chloroplast Proteins Leads to H2O2Accumulation and Activation of Cyclic Electron Flow around Photosystem I.
abstract: We describe a new member of the class of mutants in Arabidopsis exhibiting high rates of cyclic electron flow around photosystem I (CEF), a light-driven process that produces ATP but not NADPH. High cyclic electron flow 2 (hcef2) shows strongly increased CEF activity through the NADPH dehydrogenase complex (NDH), accompanied by increases in thylakoid proton motive force (pmf), activation of the photoprotective qEresponse, and the accumulation of H2O2. Surprisingly,hcef2was mapped to a non-sense mutation in the TADA1 (tRNA adenosine deaminase arginine) locus, coding for a plastid targeted tRNA editing enzyme required for efficient codon recognition. Comparison of protein content from representative thylakoid complexes, the cytochromebfcomplex, and the ATP synthase, suggests that inefficient translation ofhcef2leads to compromised complex assembly or stability leading to alterations in stoichiometries of major thylakoid complexes as well as their constituent subunits. Altered subunit stoichiometries for photosystem I, ratios and properties of cytochromebfhemes, and the decay kinetics of the flash-induced thylakoid electric field suggest that these defect lead to accumulation of H2O2inhcef2, which we have previously shown leads to activation of NDH-related CEF. We observed similar increases in CEF, as well as increases in H2O2accumulation, in other translation defective mutants. This suggests that loss of coordination in plastid protein levels lead to imbalances in photosynthetic energy balance that leads to an increase in CEF. These results taken together with a large body of previous observations, support a general model in which processes that lead to imbalances in chloroplast energetics result in the production of H2O2, which in turn activates CEF. This activation could be from either H2O2acting as a redox signal, or by a secondary effect from H2O2inducing a deficit in ATP.
authors.affiliation: Department of Plant Biology, Michigan State UniversityEast Lansing, MI, USA; DOE-Plant Research Laboratory, Michigan State UniversityEast Lansing, MI, USA.
authors.forename: Deserah D
authors.initials: DD
authors.lastname: Strand
authors.affiliation: Institute of Biological Chemistry, Washington State University Pullman, WA, USA.
authors.forename: Aaron K
authors.initials: AK
authors.lastname: Livingston
authors.affiliation: DOE-Plant Research Laboratory, Michigan State University East Lansing, MI, USA.
authors.forename: Mio
authors.initials: M
authors.lastname: Satoh-Cruz
authors.affiliation: Department of Horticulture, Washington State University Pullman, WA, USA.
authors.forename: Tyson
authors.initials: T
authors.lastname: Koepke
authors.affiliation: Institute of Biological Chemistry, Washington State University Pullman, WA, USA.
authors.forename: Heather M
authors.initials: HM
authors.lastname: Enlow
authors.affiliation: DOE-Plant Research Laboratory, Michigan State University East Lansing, MI, USA.
authors.forename: Nicholas
authors.initials: N
authors.lastname: Fisher
authors.affiliation: DOE-Plant Research Laboratory, Michigan State UniversityEast Lansing, MI, USA; Department of Biochemistry and Molecular Biology, Michigan State UniversityEast Lansing, MI, USA.
authors.forename: John E
authors.initials: JE
authors.lastname: Froehlich
authors.affiliation: DOE-Plant Research Laboratory, Michigan State University East Lansing, MI, USA.
authors.forename: Jeffrey A
authors.initials: JA
authors.lastname: Cruz
authors.affiliation: Department of Horticulture, Washington State University Pullman, WA, USA.
authors.forename: Deepika
authors.initials: D
authors.lastname: Minhas
authors.affiliation: Institute of Biological Chemistry, Washington State UniversityPullman, WA, USA; Environmental Molecular Sciences Laboratory, Pacific Northwest National LaboratoryRichland, WA, USA.
authors.forename: Kim K
authors.initials: KK
authors.lastname: Hixson
authors.affiliation: DOE-Plant Research Laboratory, Michigan State University East Lansing, MI, USA.
authors.forename: Kaori
authors.initials: K
authors.lastname: Kohzuma
authors.affiliation: Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory Richland, WA, USA.
authors.forename: Mary
authors.initials: M
authors.lastname: Lipton
authors.affiliation: Department of Horticulture, Washington State University Pullman, WA, USA.
authors.forename: Amit
authors.initials: A
authors.lastname: Dhingra
authors.affiliation: Department of Plant Biology, Michigan State UniversityEast Lansing, MI, USA; DOE-Plant Research Laboratory, Michigan State UniversityEast Lansing, MI, USA; Department of Biochemistry and Molecular Biology, Michigan State UniversityEast Lansing, MI, USA.
authors.forename: David M
authors.initials: DM
authors.lastname: Kramer
keywords: Arabidopsis; chloroplast translation; cyclic electron flow around photosystem I; hydrogen peroxide (H2O2); photosynthesis