ArabidopsisSTN7 Kinase Provides a Link between Short- and Long-Term Photosynthetic Acclimation

Abstract

Flowering plants control energy allocation to their photosystems in response to light quality changes. This includes the phosphorylation and migration of light-harvesting complex II (LHCII) proteins (state transitions or short-term response) as well as long-term alterations in thylakoid composition (long-term response or LTR). Both responses require the thylakoid protein kinase STN7. Here, we show that the signaling pathways triggering state transitions and LTR diverge at, or immediately downstream from, STN7. Both responses require STN7 activity that can be regulated according to the plastoquinone pool redox state. However, LTR signaling does not involve LHCII phosphorylation or any other state transition step. State transitions appear to play a prominent role in flowering plants, and the ability to perform state transitions becomes critical for photosynthesis in Arabidopsis thaliana mutants that are impaired in thylakoid electron transport but retain a functional LTR. Our data imply that STN7-dependent phosphorylation of an as yet unknown thylakoid protein triggers LTR signaling events, whereby an involvement of the TSP9 protein in the signaling pathway could be excluded. The LTR signaling events then ultimately regulate in chloroplasts the expression of photosynthesis-related genes on the transcript level, whereas expression of nuclear-encoded proteins is regulated at multiple levels, as indicated by transcript and protein profiling in LTR mutants.

PHOTOSYSTEM II PROTEIN33, a Protein Conserved in the Plastid Lineage, Is Associated with the Chloroplast Thylakoid Membrane and Provides Stability to Photosystem II Supercomplexes in Arabidopsis

“…5A). The effect on NPQ observed with the mutant could be related to the observed loss of the PSII-LHCII supercomplex in the psb33 mutants, but we were interested to determine whether the PSB33 mutant also displayed other phenotypes indicative of impaired NPQ, such as an altered luminal pH, increased activity of the violaxanthin cycle, and state transitions (Niyogi et al, 1998;Kanazawa and Kramer, 2002;Pesaresi et al, 2009).…”

Regulation of the photosynthetic apparatus under fluctuating growth light

“…Regulation of excitation energy distribution between PSI and PSII through phosphorylation of LHCII proteins is thought to be a mechanism for low lightacclimation [38] or to adjust thylakoid function to changing quality of light, as concluded from experiments employing very low light intensity [39,40]. Using normal white light, however, the excitation balance between PSII and PSI provided by steady-state LHCII phosphorylation is essential only for plants grown under light intensity fluctuations [41].…”

Fast Retrograde Signaling in Response to High Light Involves Metabolite Export, MITOGEN-ACTIVATED PROTEIN KINASE6, and AP2/ERF Transcription Factors in Arabidopsis

“…Arabidopsis thaliana wild-type Columbia-0 (Col-0) and wild-type Wassilewskija plants and the mutants KatE2 (Oelze et al, 2012), erf6 (SAIL_1236_H11), mdh (Hameister et al, 2007), mpk6-2 (Müller et al, 2010), mpk6-3 (Bethke et al, 2009, stn7 (Pesaresi et al, 2009), tpt1 (Schneider et al, 2002), and tpt2 (Schmitz et al, 2012) were grown in soil culture (1:1:1 mixture of Frühsdorfer Erde Klocke P, perlite, and vermiculite) for 4.5 weeks under the following conditions: 10 h of light, 80 mmol quanta m 22 s 21 , 23°C, and 14 h darkness at 18°C; 55% relative humidity. Except for the KatE2 mutant, all mutants used in this study are T-DNA exon insertion mutants (Supplemental Figure 4).…”

“…Chloroplast thylakoid protein kinase STN7 mediates shortterm and long-term acclimation and senses the redox state of the plastoquinone pool and thus links nuclear gene expression to intersystem electron transport (Allen and Pfannschmidt, 2000;Pesaresi et al, 2009). The stn7 mutant, which carries a T-DNA insertion in the fourth exon (Supplemental Figure 4A), is defective in a thylakoid-bound kinase responsible for state transition and might unravel a connection between the expression of AP2/ERF-TFs and plastoquinone-dependent redox signaling.…”