Photosynthetic redox imbalance governs leaf sectoring in the Arabidopsis thaliana variegation mutants immutans, spotty, var1, and var2.
We hypothesized that chloroplast energy imbalance sensed through alterations in the redox state of the photosynthetic electron transport chain, measured as excitation pressure, governs the extent of variegation in the immutans mutant of Arabidopsis thaliana. To test this hypothesis, we developed a nondestructive imaging technique and used it to quantify the extent of variegation in vivo as a function of growth temperature and irradiance. The extent of variegation was positively correlated (R(2) = 0.750) with an increase in excitation pressure irrespective of whether high light, low temperature, or continuous illumination was used to induce increased excitation pressure. Similar trends were observed with the variegated mutants spotty, var1, and var2. Measurements of greening of etiolated wild-type and immutans cotyledons indicated that the absence of IMMUTANS increased excitation pressure twofold during the first 6 to 12 h of greening, which led to impaired biogenesis of thylakoid membranes. In contrast with IMMUTANS, the expression of its mitochondrial analog, AOX1a, was transiently upregulated in the wild type but permanently upregulated in immutans, indicating that the effects of excitation pressure during greening were also detectable in mitochondria. We conclude that mutations involving components of the photosynthetic electron transport chain, such as those present in immutans, spotty, var1, and var2, predispose Arabidopsis chloroplasts to photooxidation under high excitation pressure, resulting in the variegated phenotype.
Rosso
Dominic
D
Department of Biology and the Biotron, University of Western Ontario, London, ON, Canada.
Bode
Rainer
R
Li
Wenze
W
Krol
Marianna
M
Saccon
Diego
D
Wang
Shelly
S
Schillaci
Lori A
LA
Rodermel
Steven R
SR
Maxwell
Denis P
DP
Hüner
Norman P A
NP
D049069:ATP-Dependent Proteases / Q000235:genetics / Q000378:metabolism; D017360:Arabidopsis / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002736:Chloroplasts / Q000235:genetics / Q000378:metabolism; D018548:Cotyledon / Q000235:genetics / Q000254:growth & development / Q000378:metabolism; D045222:Electron Transport Chain Complex Proteins / Q000235:genetics / Q000378:metabolism*; D004734:Energy Metabolism / Q000235:genetics; D018506:Gene Expression Regulation, Plant / Q000235:genetics; D014644:Genetic Variation / Q000502:physiology; D008027:Light; D008565:Membrane Proteins / Q000235:genetics / Q000378:metabolism; D045726:Metalloproteases / Q000235:genetics / Q000378:metabolism; D008928:Mitochondria / Q000235:genetics / Q000378:metabolism; D024101:Mitochondrial Proteins; D009154:Mutation / Q000502:physiology*; D010084:Oxidation-Reduction; D010088:Oxidoreductases / Q000235:genetics / Q000378:metabolism; D010641:Phenotype; D010775:Photic Stimulation; D010788:Photosynthesis / Q000502:physiology*; D018515:Plant Leaves / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D010940:Plant Proteins; D013696:Temperature; D020524:Thylakoids / Q000235:genetics / Q000378:metabolism; D000099188:Alternative Oxidase
D049069:ATP-Dependent Proteases; D029681:Arabidopsis Proteins; D045222:Electron Transport Chain Complex Proteins; D008565:Membrane Proteins; D045726:Metalloproteases; D024101:Mitochondrial Proteins; D010088:Oxidoreductases; D010940:Plant Proteins; D000099188:Alternative Oxidase; C405742:IM protein, Arabidopsis; C547215:FtsH5 protein, Arabidopsis; C402651:AT2G30950 protein, Arabidopsis