Changes induced by cadmium stress and iron deficiency in the composition and organization of thylakoid complexes in sugar beet (Beta vulgaris L.)

• Cd-induced chloroplast Fe deficiency is a prime trigger for thylakoid acclimation to Cd excess.
• Both Cd stress and Fe deficiency induce PSII supercomplex and LHCII disassembly.
• Thermal dissipation by inactive PSII complexes is markedly induced by Cd stress.
• The amounts of PSI supercomplexes and zeaxanthin rise with Fe deficiency.
• Cyclic electron flow and zeaxanthin are likely to be energy quenchers under low Fe.

In intact plants, Cd-induced Fe deficiency is thought to play a role in the toxic effects of Cd on photosynthesis. To investigate the contribution of the Cd-induced Fe deficiency to Cd stress symptoms we studied the composition and organization changes of thylakoid pigment–protein complexes by two-dimensional Blue Native-SDS gel electrophoresis and mass spectrometry, in parallel to functional changes, using Beta vulgaris plants grown in hydroponics. Plants were treated by withdrawing Fe or with 10 μM CdCl2 for 10 days. Both metal stresses caused a marked decline in leaf chlorophyll concentration and chloroplast Fe content, as well as a loss of photosystem I (PSI) and light harvesting complex II (LHCII) complexes. Furthermore, marked organizational changes of the photosynthetic apparatus were found, including a decrease in the ratio of the PSII mega-/supercomplexes and an increase in the monomeric form of the LHCII antennae, with the extent of these changes being similar under both stresses. This supports that Fe deficiency responses have a major role in the responses of plants under Cd stress. In Fe-deficient thylakoids the increase in the ratio of PSI supercomplexes and degrading PSII particles was more pronounced, and higher zeaxanthin content was found. Under Cd stress, a stronger inhibition of PSII activity and enhancement of thermal dissipation of the inactive PSII complexes were observed. The differences detected under the two metal stresses lead to the conclusion that both local Fe deficiency in chloroplasts and other direct or indirect inhibitory effects of Cd are behind the response mechanisms of plants grown under Cd stress.