Evidence for a selective destabilization of an integral membrane protein, the cytochrome b₆/f complex, during gametogenesis in Chlamydomonas reinhardtii

Abstract

We studied the process of photosynthetic inactivation during gametogenesis of the unicellular green alga Chlamydomonas reinhardtii. We show that it is caused by the selective destabilization of a single transmembrane protein complex, the cytochrome b6/f complex, which is initially accumulated in the thylakoid membranes of vegetative cells. This protein destabilization is controlled by the intracellular energy sources available in the gametes, i. e. the coupled electron flow in the mitochondria and the amount of starch accumulated in the chloroplast. It nevertheless requires the expression of gamete-specific proteins. The loss of cytochrome b6/f complexes during gametogenesis is prevented by the addition of cycloheximide, but is chloramphenicol insensitive. Therefore, it is likely to involve some translation product of nuclear origin, specifically expressed during gametogenesis. Among the new polypeptides specifically found in the gametes, we detected a soluble polypeptide Ma (approximate molecular mass of 63 kDa), which shared common epitopes with cytochromef. Its synthesis displays an antibiotic sensitivity typical of a nuclear-encoded polypeptide and is controlled by the same intracellular signals which control the destabilization of the cytochrome b6/fcomplexes in the thylakoid membranes.

Changes in Transcript Abundance in Chlamydomonas reinhardtii following Nitrogen Deprivation Predict Diversion of Metabolism

“…In C. reinhardtii, there is evidence that the cytochrome subunits are degraded not in response to the low concentrations of N per se but rather to the changed energy content of the cell. Thus, one possible advantage for the cells to decrease photosynthesis following N deprivation is to prevent the accumulation of reactive oxygen species (Bulté and Wollman, 1992). At the same time, genes encoding proteins of the respiratory chain in mitochondria were only moderately affected following N deprivation except for those encoding alternative oxidases, which showed elevated transcript abundance.…”

“…In C. reinhardtii, photosynthetic efficiency decreases following N deprivation, at least partially due to a reduction in the abundance of light-harvesting complexes (Plumley and Schmidt, 1989;Peltier and Schmidt, 1991) and selective degradation of the cytochrome b 6 f complex (Bulté and Wollman, 1992;Majeran et al, 2000). Likewise, the abundance of transcripts encoding photosynthesis-related proteins was substantially reduced following N deprivation.…”

Chloroplast Biogenesis of Photosystem II Cores Involves a Series of Assembly-Controlled Steps That Regulate Translation

“…Most likely, assembly of the CES subunits in their target complex induces a proteasesensitive conformation that allows their proteolysis if PSII assembly cannot proceed further. Similarly, cytochrome f, a stable protein when unassembled (Kuras and Wollman, 1994;Choquet et al, 2003), becomes susceptible to proteolytic degradation upon nitrogen starvation once assembled within cytochrome b 6 f complexes (Bulte and Wollman, 1992).…”

Systems-Level Analysis of Nitrogen Starvation-Induced Modifications of Carbon Metabolism in a Chlamydomonas reinhardtii Starchless Mutant

“…Because of the potential for using algae to generate biodiesel precursors, there is interest in understanding carbon metabolism and its regulation in the context of TAG accumulation in algae (reviewed in Johnson and Alric, 2013). In addition to triggering starch and TAG synthesis, N starvation also induces a number of other responses, including ribosome turnover, gametogenesis, and chlorosis (Siersma and Chiang, 1971;Martin and Goodenough, 1975;Plumley and Schmidt, 1989;Bulté and Wollman, 1992).…”