Occurrence of a High Temperature Sensitivity of Chloroplast Ribosome Formation in Several Higher Plants

Feierabend, J.; Mikus, Magdalene

doi:10.1104/pp.59.5.863

Cited by 49 publications

(24 citation statements)

References 14 publications

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“…During heat bleaching of Euglena [8], which is also accompanied by a deficiency in plastid ribosomes [9], the cpDNA was found to be eliminated [10,11]. A loss of cpDNA would, of course, necessarily imply the absence of plastid ribosomes because the plastid rRNA and also some ribosomal polypeptides are coded on cpDNA .…”

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confidence: 99%

The Presence of DNA in Ribosome-Deficient Plastids of Heat-Bleached Rye Leaves

Herrmann

Feierabend

1980

Eur J Biochem

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In leaves of rye seedlings (Secale cereale L.) grown at 32°C the formation of plastid (70-S) ribosomes is specifically prevented. The resulting plastid-ribosome-deficient leaves can be used as a suitable system to identify chloroplast proteins which are translation products of cytosolic (80-S) ribosomes. The ribosome deficiency in plastids is accompanied by a bleaching of the leaves in light. In experiments aimed at finding the primary heat-sensitive event leading to ribosome deficiency the DNA of rye chloroplasts has been identified. Its properties are similar to those of chloroplast DNAs from other higher plants. The ribosome-deficient plastids isolated from heat-bleached rye leaves contained a DNA species which was indistinguishable from that of chloroplasts with regard to buoyant density in CsCl equilibrium gradients, reassociation properties and fragment patterns obtained upon cleavage by restriction endonucleases. Its quantity was comparable to that of chloroplast DNA of green leaves grown at a permissive temperature (22 "C). These results suggest that, unlike the effect in heat-bleached Euglena strains, lack of chloroplast DNA cannot be considered as the reason for the primary effect of high temperature on rye leaves but steps in the biosynthetic pathway of plastid ribosomes themselves must be affected more directly.In several higher plants, especially in cereal seedlings, the biogenesis of plastid ribosomes was found to be heat-sensitive [l]. When seedlings of these plants are grown at an appropriate non-permissive temperature, usually in the range between 32°C and 34 "C, the accumulation of plastid (70-S) ribosomes as well as that of plastid rRNA in leaves is prevented [2,3]. Consequently, defective plastids develop and the ribosome-deficient leaves grown in light are chlorotic [3,4]. In rye seedlings the interference of the high temperature was confined to events of plastid development and the high temperature apparently had no major damaging effects on the organization or functions of the rest of the cell [2-41.The high temperature appeared specifically to block the formation of the 70-S ribosomes in plastids and the defects observed seem to result primarily Abbreviations. NaCI/Cit, 0.15 M NaC1,0.015 M citrate, pH 7.2; cpDNA, chloroplast DNA, nDNA, nuclear DNA.

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The Presence of DNA in Ribosome-Deficient Plastids of Heat-Bleached Rye Leaves

Herrmann

Feierabend

1980

Eur J Biochem

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“…In an attempt to determine whether the enzyme is synthesized in the cytoplasm or within the plastid, it was decided to make use of the observation that a deficiency of plastid ribosomes can be induced in certain higher plants by growth at high temperatures, a phenomenon first described and extensively investigated by Feierabend (11,12). Rye was chosen for study because in this species an elevated growth temperature sufficient to bring about an almost total lack of plastid ribosomes has little effect on cytoplasmic or mitochondrial protein synthesis (12).…”

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Site of Synthesis of NADPH

Griffiths¹,

Beer²

1982

Plant Physiol.

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The site of synthesis of the plastid membrane-located enzyme, protochlorophyllide reductase, has been determined. Plastid ribosome-deficient and normal rye (Secale cereake L., cv Rheidol) plants were grown in darkness at 33°C and 22°C, respectively. Extracts from these plants were analyzed for the levels of different ribosomal RNAs and cytochrome f and the activity of a number of enzymes with well-established sites of synthesis. The results confirmed that the higher temperature had induced a specific inhibition of protein synthesis in the plastids. The activity and level of protochlorophyllide reductase was unaffected by growth at the higher temperature, suggesting it to be a cytoplasmically synthesized enzyme.NADPH-Pchlide oxidoreductase is an enzyme of the Chl biosynthetic pathway and is responsible for the light-dependent reduction of Pchilde in higher plants. The enzyme is present at high activity in etiolated tissue (13) and has recently been purified and shown to be one of the major proteins of the etioplast internal membrane system (2, 21). Light exerts an interesting regulatory effect on the enzyme in that illumination ofpreviously dark-grown plants results in a decrease in both the activity (19) and amount (2) of the enzyme. To characterize this light effect, it is obviously essential to gain information about the synthesis of the enzyme, and in this paper the site of synthesis of the enzyme is reported.In an attempt to determine whether the enzyme is synthesized in the cytoplasm or within the plastid, it was decided to make use of the observation that a deficiency of plastid ribosomes can be induced in certain higher plants by growth at high temperatures, a phenomenon first described and extensively investigated by Feierabend (11,12). Rye was chosen for study because in this species an elevated growth temperature sufficient to bring about an almost total lack of plastid ribosomes has little effect on cytoplasmic or mitochondrial protein synthesis (12). An alternative approach to answer the question might have been the analysis of plastid ribosome-deficient mutants (5); however, in view of the findings of Bradbeer et at. (7) that certain cytoplasmically synthesized plastid enzymes can still occur, but in greatly reduced amounts, in plastid ribosome-free mutants, it was felt that measurement of Pchilde reductase activity in plants with a heatinduced plastid ribosome deficiency would yield more reliable data regarding the site of synthesis of the enzyme. A previous study of the enzymes of Chl synthesis failed to detect a significant level of Pchilde reductase, measured as photoconvertible Pchilde, in such high-temperature-grown plants (10), but in the present work use was made of a much more sensitive assay of enzymic activity (13). A growth temperature of 33°C was adopted here to 'Supported by the Science and Engineering Research Council.

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Section: The Effect Of Intermittently Lowered Temperatures On Heat Blmentioning

confidence: 99%

“…Phenocopies of the mutants can be obtained by growing the wild type at temparatures above 32~ (5,17). Analogous phenotypes are obtained with oat, wheat and pea wild type seedlings grown under restrictive temperature conditions (5,13). Since the etioplasts formed in the mutants at the permissive temperature can apparently develop into fully active chloroplasts at the restrictive temperature (32~ the six genes must code for six products either not needed in the assembly of the photosynthetic membranes or preformed in the dark.…”

Section: The Effect Of Intermittently Lowered Temperatures On Heat Blmentioning

confidence: 99%

“…This phenomenon in barley and in rye results in plants deficient in chlorophyll (5) and chloroplast thylakoid membranes (13), chloroplast ribosomes (5, 13) and ribulose-l,5-bisphosphate carboxylase (5,6). Several enzymes of the photosynthetic CO 2 fixation cycle (6) and the small subunit of ribulose-l,5-bisphosphate carboxylase (3), which is made on cytoplasmic ribosomes, continue to be synthesized.…”

Section: Introductionmentioning

confidence: 99%

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Mutants of barley heat-sensitive for chloroplast development

Smillie

Henningsen

Bain

et al. 1978

Carlsberg Res. Commun.

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Six nuclear gene mutants of barley, heat-sensitive for chloroplast development, are described. These conditional lethal mutants in six different genes can be grown as homozygous viable plants in the field, their mutant phenotype only being expressed with development at high temperature. Chlorophyll accumulation in the mutants but not in the wild type is inhibited by a growth temperature of 310C. The degree of temperature sensitivity varies amongst the mutants. For example, partial inhibition of chlorophyll production is evident in the mutant vir-zf is4 above 20 ~ while inhibition is complete at a growth temperature of 29 ~ The mutant vir-zi ts49 remains green at 29 ~ but is bleached at 31 ~ The reduction in chlorophyll content of the leaves at high growth temperatures is accompanied by the appearances of structural abnormalities in the chloroplasts and reduced photochemical activity per mg chlorophyll. The inhibitory effect of elevated temperatures is confined to some early stage of plastid development as the light-dependent conversion of ctioplasts into chloroplasts in the mutants is not inhibited at 32 ~ Leaf elongation in the mutants compared with the wild type is not affected by high growth temperatures. When the mutants are grown at temperatures permitting normal chlorophyll accumulation, the chloroplast thylakoid membranes appear to be no less heat stable than in the wild type.

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Occurrence of a High Temperature Sensitivity of Chloroplast Ribosome Formation in Several Higher Plants

Cited by 49 publications

References 14 publications

The Presence of DNA in Ribosome-Deficient Plastids of Heat-Bleached Rye Leaves

The Presence of DNA in Ribosome-Deficient Plastids of Heat-Bleached Rye Leaves

Site of Synthesis of NADPH

Mutants of barley heat-sensitive for chloroplast development

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