Abstract
In plants the physiological and biochemical demands on each cell vary greatly between day and night, mostly due to the differing output of photosynthesis. Chloroplasts, the organelles of photosynthesis, are biochemically closely linked to the other energy generating organelles, the mitochondria. We have now investigated whether gene expression in plant mitochondria is influenced by these daily physiological variations. Transcript synthesis in these organelles cycles in a diurnal rhythm, while steady state transcript levels do not vary between light and dark phases and are stable throughout the diurnal (as well as the circadian) time course. This finding suggests that available steady state transcript levels in plant mitochondria are sufficient to provide the required biochemical capacities also at times of peak respiratory and physiological demands.
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References
Bailey-Serres J, Hanson DK, Fox TD, Leaver CJ (1986) Mitochondrial genome rearrangement leads to extension and relocation of the cytochrome c oxidase subunit I gene in sorghum. Cell 47:567–576
Bläsing OE, Gibon Y, Günther M, Höhne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible WR, Stitt M (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17:3257–3281
Deng XW, Gruissem W (1987) Control of plastid gene expression during development: the limited role of transcriptional regulation. Cell 49:379–387
Dessi P, Whelan J (1997) Temporal regulation of in vitro import of precursor proteins into tobacco mitochondria. FEBS Lett 415:173–178
Doyle MR, Davis SJ, Bastow RM, McWatters HG, Kozma-Bognar L, Nagy F, Millar AJ, Amasino RM (2002) The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana. Nature 419:74–77
Dutilleul C, Driscoll S, Cornic G, de Paepe R, Foyer CH, Noctor G (2003a) Functional mitochondrial complex I is required by tobacco leaves for optimal photosynthetic performance in photorespiratory conditions and during transients. Plant Physiol 131:264–275
Dutilleul C, Garnier M, Noctor G, Mathieu C, Chétrit P, Foyer CH, de Paepe R (2003b) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signalling and diurnal regulation. Plant Cell 15:1212–1226
Eberhard S, Drapier D, Wollman FA (2002) Searching limiting steps in the expression of chloroplast-encoded proteins: relations between gene copy number, transcription, transcript abundance and translation rate in the chloroplast of Chlamydomonas reinhardtii. Plant J 31:149–160
Escobar MA, Franklin KA, Svensson AS, Salter MG, Whitelam GC, Rasmusson AG (2004) Light regulation of the Arabidopsis respiratory chain. Multiple discrete photoreceptor responses contribute to induction of type II NAD(P)H dehydrogenase genes. Plant Physiol 136:2710–2721
Gardeström P, Igamberdiev AU, Raghavendra AS (2002) Mitochondrial functions in the light and significance to carbon-nitrogen interactions. In: Foyer CH, Noctor G (eds) Photosynthetic nitrogen assimilation and associated carbon and respiratory metabolism. Kluwer Academic Publishers, Nijmwegen pp 151–172
Giegé P, Hoffmann M, Binder S, Brennicke A (2000) RNA degradation buffers asymmetries of transcription in Arabidopsis mitochondria. EMBO Rep 1:164–170
Giegé P, Sweetlove LJ, Cognat V, Leaver CJ (2005) Coordination of nuclear and mitochondrial genome expression during mitochondrial biogenesis in Arabidopsis. Plant Cell 17:1497–1512
Hoefnagel MHN, Atkin OK, Wiskich JT (1998) Interdependence between chloroplasts and mitochondria in the light and the dark. Biochim Biophys Acta 1366:235–255
Klaff P, Gruissem W (1991) Changes in chloroplast mRNA stability during leaf development. Plant Cell 3:517–529
Krömer S (1995) Respiration during photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 46:45–70
Kuhn J, Tengler U, Binder S (2001) Transcript lifetime is balanced between stabilizing stem-loop structures and degradation-promoting polyadenylation in plant mitochondria. Mol Cell Biol 2:731–742
Legen J, Kemp S, Krause K, Profanter B, Herrmann RG, Maier RW (2002) Comparative analysis of plastid transcription profiles of entire plastid chromosomes from tobacco attributed to wild-type and PEP-deficient transcription machineries. Plant J 31:171–188
Logan DC, Millar AH, Sweetlove LJ, Hill SA, Leaver CJ (2001) Mitochondrial biogenesis during germination in maize embryos. Plant Physiol 125:662–672
Makaroff CA, Palmer JD (1988) Mitochondrial DNA rearrangements and transcriptional alterations in the male-sterile cytoplasm of Ogura radish. Mol Cell Biol 8:1474–1480
McClung CR, Hsu M, Painter JE, Gagne JM, Karlsberg SD, Salomé PA (2000) Integrated temporal regulation of the photorespiratory pathway. Circadian regulation of two Arabidopsis genes encoding serine hydroxymethyltransferase. Plant Physiol 123:381–391
Michalecka AM, Svensson AS, Johansson FI, Agius SC, Johanson U, Brennicke A, Binder S, Rasmusson AG (2003) Arabidopsis genes encoding mitochondrial type II NAD(P)H dehydrogenases have different evolutionary origins and show distinct responses to light. Plant Physiol 133:642–652
Monéger F, Smart CJ, Leaver CJ (1994) Nuclear restoration of cytoplasmic male sterility in sunflower is associated with the tissue-specific regulation of a novel mitochondrial gene. EMBO J 13:8–17
Raghavendra AS, Padmasree K (2003) Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends Plant Sci 8:546–553
Smart CJ, Moneger F, Leaver CJ (1994) Cell-specific regulation of gene expression in mitochondria during anther development in sunflower. Plant Cell 6:811–825
Svensson AS, Rasmusson AG (2001) Light-dependent gene expression for proteins in the respiratory chain of potato leaves. Plant J 28:73–82
Unseld M, Marienfeld JR., Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet 15:57–61
Wise RP, Pring DR (2002) Nuclear mediated mitochondrial male-fertility in higher plants: light at the end of the tunnel? Proc Natl Acad Sci USA 99:10240–10242
Acknowledgements
We are grateful to J. Legen and R. G. Herrmann at the Department Biologie I of the Universität München for their kind support with the macroarrays and to D. Gagliardi and T. Börner for their very constructive discussions. This work was supported by post-doctoral fellowships from the Humboldt-Foundation (S.O.) and the Japanese Society for the Promotion of Science (S.O.), and by a research grant from the Deutsche Forschungsgemeinschaft (S.O.).
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Okada, S., Brennicke, A. Transcript levels in plant mitochondria show a tight homeostasis during day and night. Mol Genet Genomics 276, 71–78 (2006). https://doi.org/10.1007/s00438-006-0119-7
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DOI: https://doi.org/10.1007/s00438-006-0119-7