Genetically Programmed Chloroplast Dedifferentiation as a Consequence of Plastome-Genome Incompatibility in Oenothera

Comparision of chloroplast from plants with one of four plastome types (I, II, III, IV) in the nuclear background of Oenothera elata strain Johansen addressed the effects of plastome-genome incompatibility with respect to leaf pigmentation, plastid ultrastructure, chlorophyll a/chlorophyll b ratio, and photosynthetic electron transport. Previous observations of plastomes I, II, and IV in this nuclear background have revealed no indications of incompatibility, but the studies reported here demonstrate that chloroplasts of plastome IV have subtle alterations in their photosynthetic abilities, in particular, deficiencies in photosystem II. The well-characterized "hybrid bleaching" of plants with the AA genotype and plastome III involves leaves that become bleached in the center while remaining green at the tips, edges, and veins. Electron transport assays performed on fractionated bleached and green tissue from the same plants show photosynthetic defects in both the green and bleached regions, although defects in the latter are more severe. Ultrastructural studies show that chloroplasts in the bleached areas enlarge, thylakoid membranes become swollen and vesiculated, and production of new thylakoids is blocked, with chloroplasts appearing to undergo a programmed senescence. A time course revealed that the senescence is actually a reversible dedifferentiation. Alterations in the composition of medium to which AA/III seedlings were transferred showed that the presence of auxin can prevent the development of the typical incompatibility response, with leaf tissue remaining green rather than bleaching. It is proposed that differences in concentrations of plant growth regulators may be responsible for the persistence of normal chloroplasts near the vascular tissue and leaf blade edges and that seasonal fluctuations in auxin levels could explain the periodic bleaching that occurs in older plants.