Recovery of plastids from photooxidative damage: Significance of a plastidic factor

Abstract

It was inferred from previous findings that a plastid-derived factor (plastidic factor) is involved in the transcriptional control of nuclear genes coding for proteins destined for the chloroplast. Photooxidative damage to the plastid destroys the ability of the organelle to give off this factor. Cytosolic enzyme levels are not impaired if plastids are damaged, and morphogenesis of seedlings is normal. The only exception found so far is nitrate reductase, a cytosolic enzyme, which is regulated by the cellas if it were a plastidic protein. In the present study we have shown that the plastids in the mesophyll of mustard (Sinapis alba L.) cotyledons, damaged by 3 h photooxidation in red light (6.8 W·m(-2)) and then returned to darkness or to continuous, non-photooxidative far-red light (cFR), recover from photooxidative damage. The rate of recovery is stimulated by phytochrome (operationally, cFR). Since the cytosolic enzyme nitrate reductase is affected by the different treatments in principally the same way as the levels of plastidic enzymes, we conclude that it is recovery of the plastids' ability to give off the plastidic factor rather than structural recovery which leads to recovery of gene expression and protein (and chlorophyll) re-accumulation. The extent of recovery varied according to the enzyme and this variation could be explained by different plastidic-factor requirements for gene expression. This explanation was confirmed by measurements of translatable mRNAs. It was found that LHCP-gene expression (light-harvesting chlorophyll a/b-binding protein of photosystem II) is far more sensitive to photooxidative damage of the plastids than SSU-gene expression (small subunit of ribulose-1.5-bisphosphate carboxylase). Correspondingly, recovery is expressed to a much greater extent in the latter than in the former case.

Photooxidative Destruction of Chloroplasts and Its Effect on Nuclear Gene Expression and Extraplastidic Enzyme Levels *

“…This indicates that plastidogenesis per se is not affected by the absence of carotenoids (e.g. Frosch et al, 1979;Reiss et al, 1983;Oelmiiller et al, 1986b;Batschauer et al, 1986;Burgess and Taylor, 1987;Schuster et al, 1988b;Sagar et d., 1988).…”

“…of unprotected Chl is high enough, the entire plastidic compartment can be destroyed under appropriate light conditions and only small chlorophyll-free rudiments without detectable internal structure remain (Bachmann et al, 1967;Troxler et al, 1969;Bartels and Hyde, 1970;Reiss ef al., 1983: Oelmiiller et al, 1986bSimpson et al, 1986a;Schuster et al, 1988b).…”

“…As a second strategy to limit photooxidative damage in carotenoid-free seedlings, far-red light has been used which causes only a limited protochlorophyl-I(ide) to chlorophyll(ide) photoconversion. Moreover, the resulting small amount of Chl absorbs farred light so weakly that photooxidation does not take place even in high fluence rate far-red light (Frosch et al, 1979;Reiss et al, 1983;Oelmuller et al, 1986bOelmuller et al, , 1988Schuster et al, 1988b).…”

“…the amount of Chl is usually sufficiently high enough to destroy the already developed plastids (Bachmann et al. 1973;Frosch et al, 1979;Batschauer et al, 1986;Oelmiiller et al, 1986bOelmiiller et al, , 1988Schuster et al, 1988b). However, as soon as all Chl is photooxidized, no further photodamage occurs even if the seedlings are maintained in strong light (Frosch et al, 1979;Oelmiiller et al, 1988).…”

“…carotenoidfree white seedlings grown under high fluence rates contain little or no internal membrane structure (Bachmann et al, 1967;Frosch et a [ . , 1979;Feierabend et al, 1979;Reiss et al, 1983) and only traces of typical plastidic enzymes and proteins (Feierabend and Schubert, 1978;Reiss et al, 1983;Mayfield et al, 1986aMayfield et al, , 1986bRajasekhar and Mohr, 1986;Schuster -et al, 1988b). Plastidic ribosomes and ribosomal RNA are no longer detectable (Bartels and Hyde, 1970;Feierabend and Schubert, 1978;Reiss et al, 1983;Batschauer et al, 1986).…”