Induction of Acclimative Proteolysis of the Light-Harvesting Chlorophyll a/b Protein of Photosystem II in Response to Elevated Light Intensities

Abstract

Most plants have the ability to respond to fluctuations in light to minimize damage to the photosynthetic apparatus. A proteolytic activity has been discovered that is involved in the degradation of the major light-harvesting chlorophyll a/b-binding protein of photosystem II (LHCII) when the antenna size of photosystem II is reduced upon acclimation of plants from low to high light intensities. This ATP-dependent proteolytic activity is of the serine or cysteine type and is associated with the outer membrane surface of the stroma-exposed thylakoid regions. The identity of the protease is not known, but it does not correspond to the recently identified chloroplast ATP-dependent proteases Clp and FtsH, which are homologs to bacterial enzymes. The acclimative response shows a delay of 2 d after transfer of the leaves to high light. This lag period was shown to be attributed to expression or activation of the responsible protease. Furthermore, the LHCII degradation was found to be regulated at the substrate level. The degradation process involves lateral migration of LHCII from the appressed to the nonappressed thylakoid regions, which is the location for the responsible protease. Phosphorylated LHCII was found to be a poor substrate for degradation in comparison with the unphosphorylated form of the protein. The relationship between LHCII degradation and other regulatory proteolytic processes in the thylakoid membrane, such as D1-protein degradation, is discussed.The main focus of photosynthesis research has been the functional and structural aspects behind the energytransducing process. The progress has been significant, and the photosynthetic protein complexes can now be described at a very refined molecular level (Barber and Andersson, 1994). Conversely, relatively little is known about the acclimating, regulatory, and protective processes that maintain high photosynthetic efficiency during everfluctuating and even stressful environmental conditions.The identification of such auxiliary processes associated with thylakoid membranes and the characterization of the enzymes involved are therefore central tasks of current photosynthesis research. Examples of auxiliary enzymes or components are kinases and phosphatases responsible for reversible protein phosphorylation (Gal et al., 1997), desaturases controlling the lipid composition and dynamics of thylakoid membranes (Wada et al., 1990), stress-induced proteins such as the ELIPs (Adamska, 1997), and several enzymatic activities involved in various forms of regulatory proteolysis Andersson and Aro, 1997). In the latter case, D1-protein turnover during repair of damage caused by photoinhibition is the most illustrative example (Prasil et al., 1992; Andersson and Aro, 1997). The knowledge of chloroplast proteases involved in regulatory proteolysis is still very limited. The presence of homologs to bacterial proteases in chloroplasts, such as the Clp and FtsH proteins, has provided new insights and possibilities (Gray et al., 1990;Moore and Keegstra, 1993; Lindahl et...

Overexpression of chlorophyllide a oxygenase (CAO) enlarges the antenna size of photosystem II in Arabidopsis thaliana

“…These results are apparently not consistent with the observation in many Chl-b de®cient mutants lacking most of the Lhc proteins, except for Lhcb5 (Harrison and Melis, 1992;Bossman et al, 1997;Kro  l et al, 1995). A mechanism involving Lhc-speci®c proteases (Lindahl et al, 1995;Yang et al, 1998) and/or a vesiclemediating transport system of Lhcb proteins (Hoober and Eggink, 1999) Genetic modi®cation of the antenna size might be a useful tool for future improvement in crop productivity. Plants that are distributed both in sun and shade conditions tend to change their a : b ratio more drastically upon change in the light environment than those distributed exclusively in sun or shade conditions (Murchie and Horton, 1997).…”

Identification of Mutants of Arabidopsis Defective in Acclimation of Photosynthesis to the Light Environment

“…The ape1 mutation carried by line 99-1 had a specific effect on the ability to alter thylakoid composition in response to a LL to HL transfer as shown by measurements of Chl a/b and PSII content, correlated with reductions in the photochemical efficiency of PSII as measured by Chl fluorescence; in contrast, there was no effect on acclimation of maximum photosynthetic rate P max to an increase in light. The increase in Chl a/b during acclimation of wild-type plants to an increase in growth irradiance results principally from proteolytic degradation of surplus LHCII, which binds a large proportion of total Chl b, together with parallel de novo synthesis of additional PSII reaction centers; one possibility is therefore that the ape1 mutant has a defect in this aspect of acclimation-perhaps in promoting the synthesis of additional PSII and/or related to the proteolytic degradation of surplus LHCII (Yang et al, 1998). Thus the Chl fluorescence screen has exposed a potential role in acclimation for a protein with no previously identified function either in photosynthesis or in the regulation of gene expression but that has been strongly conserved during evolution-for instance, the predicted APE1 protein product shows 39% identity, 55% similarity to the slr0575 open reading frame of Synechocystis sp.…”

“…The acclimation response is complex: It involves changes in the relative abundance of a large number of proteins encoded by both chloroplast and nuclear genomes; expression of some of these proteins also responds to altered spectral quality of light and is influenced by other environmental factors; and control of the levels of a number of photosynthetic proteins occurs at levels other than transcription (Flachmann and Kü hlbrandt, 1995;Kim and Mayfield, 1997;Petracek et al, 1997), including degradation of particular pigment-protein complexes by specific proteases (Yang et al, 1998). Therefore, the regulation of acclimation potentially involves multiple signal transduction chains, with crosstalk between redox control and other pathways that control photosynthetic gene expression Oswald et al, 2001).…”

AtFtsH6 is involved in the degradation of the light-harvesting complex II during high-light acclimation and senescence

“…All of these functions necessitate a very efficient and highly effective regulation of LHC II apoproteins during shortand long-term acclimation to different environments (14)(15)(16). However, despite much research, very little is known about the proteases involved in the regulation of LHC II apoproteins.…”