Stress‐induced degradation of the photosynthetic apparatus is accompanied by changes in thylakoid protein turnover and phosphorylation

Abstract

Development of chlorosis and loss of PSII were compared in young spinach plants suffering under a combined magnesium and sulphur deficiency. Loss of chlorophyll could be detected already after the first week of deficiency and preceded any permanent functional inhibition of PSII as detected by changes in the chlorophyll fluorescence parameter Fv/Fm. A substantial decrease in Fv/Fm was observed only after the second week of deficiency. After 4 weeks, the plants had lost about 70% of their original chlorophyll content, but fluorescence data indicated that 80% of the existing PSII centers were still capable of initiating photosynthetic electron transport. The degradation of the photosynthetic apparatus without loss of PSII activity was due to changes in protein turnover, especially of the PSII D1 reaction center protein. Already by day 7 of deficiency, a 1.4‐fold increase in D1 protein synthesis was observed measured as incorporation of 14C‐leucine. Immunological determination by western‐blotting did not reveal a change in D1 protein content. Thus, D1 protein was also degraded more rapidly. The increased turnover was high enough to prevent any loss or inhibition of PSII. After 3 weeks, D1 protein synthesis on a chlorophyll basis was further increased by a factor of 2. However, this was not enough to prevent a net loss of D1 protein of about 70%. Immunological determination revealed that together with the D1 protein also other polypeptides of PSII became degraded. This process prevented a large accumulation of photo‐inactivated PSII centers. However, it initiated the breakdown of the other thylakoid proteins, especially of LHCII, resulting in the observed chlorosis. Together with the change in protein turnover and stability, a characteristic change in thylakoid protein phosphorylation was observed. In the deficient plants steady state phosphorylation of both LHCII and PSII proteins was increased in the dark. In the light phosphorylation of PSII proteins was stimulated and after 3 weeks of deficiency was even higher in the deficient leaves than in the control plants. In contrast, the phosphorylation level of LHCII decreased in the light and could hardly be detected after 3 weeks of deficiency. Phosphorylation of the reaction center polypeptides presumably increased their stability against proteolytic attack, whereas phosphorylated LHCII seems to be the substrate for proteolysis.

Changes in D1-protein turnover and recovery of photosystem II activity precede accumulation of chlorophyll in plants after release from mineral stress

“…Our data show that in Mg-and S-deficient spinach the steady-state phosphorylation levels of the PSII polypeptides D1 and D2, and also of CP43 of the inner antennae and the 9-kDa psbH gene product in the light were increased compared with the non-deficient control (see also Dannehl et al 1995). Obviously, the more stable form of the Dl-protein accumulates when PSII is degraded.…”

“…As a consequence, phosphorylated LHCII moves from the PSII-containing grana to the PSI-containing stromal regions of the thylakoid membrane, in this way redirecting excitation energy from PSII to PSI. Phosphorylation of LHCII was observed in the dark in both nutrient-deficient and non-deficient plants (see also Dannehl et al 1995). A similar dark phosphorylation of LHCII is also known from green algae and from leaves of higher plants (Allen 1992;Elich et al 1993).…”

“…As shown by studies in vitro and in organello, degradation of the phosphorylated form of the Dl-protein is drastically reduced (Aro et al 1992) and the phosphorylated Dl-protein does not take part in D1-protein turnover (Ebbert and Godde 1994). Although the physiological significance of Dl-protein phosphorylation is still unknown, recent investigations of Mg-and S-deficient plants have shown that the steady-state level of Dl-protein phosphorylation increases when Dl-protein is lost by degradation (Dannehl et al 1995). Nothing is known about Dl-protein phosphorylation when PSII is under repair and new PSII reaction-centres have been formed.…”

Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: The role of back electron flow

“…•Ϫ (14) and the phosphorylation of the PSII core proteins preventing the D1 protein degradation (4,43). Thus the damage per light absorbed may be further enhanced in absence of these protective conditions as compared with that induced at light intensities above saturation of electron flow.…”

Environmentally Modulated Phosphoproteome of Photosynthetic Membranes in the Green Alga Chlamydomonas reinhardtii

“…It is worth noting that until our present work, reversible phosphorylation of the D1 protein has been considered as plant-specific (13,15,16). Phosphorylation of thylakoid proteins in plants has also been implicated in adaptive responses to a number of environmental stress factors, such as high light (17,18), cold stress (19), combined high light and cold treatment (20), heat shock (21), combined magnesium and sulfur deficiency (22), and waterdeficient conditions (23). However, molecular mechanisms underlying regulation of photosynthesis by environmentally dependent thylakoid protein phosphorylation are still largely unknown.…”