Summary
The expression of genes involved in plastid differentiation is subject to developmental control. To understand better the molecular basis of this regulation, we have analyzed in parallel the changes in relative levels of four chloroplast and two nuclear transcripts during differentiation of chloroplasts into chromoplasts in ripening bell pepper fruits and in maturing sunflower petals, as well as in the case of chemically-induced chromoplast formation in leaves. Amongst the prominent features, we noted that transcripts of nuclear genes coding for chloroplast proteins, such as the major chlorophyll a/b-binding protein (encoded by cab) and the small subunit of ribuloses-1,5-bisphosphate carboxylase (encoded by rbcS), were detected in chromoplast-containing bell pepper leaves and sunflower petals, whilst they disappeared in bell pepper fruit chromoplasts. Transcripts of the plastid gene coding for the large subunit of ribulose-1,5-bisphosphate carboxylase were detected during the whole differentiation process. The steady-state level of the mRNA corresponding to the 32 kDa herbicide-binding protein increased in fruit and petal chromoplasts. Changes in the relative transcriptional activities of plastid genes and in their relative mRNA levels occurred during bell pepper fruit ripening. However, no significant change in the overall transcriptional activity was found when comparing both types of plastids, whereas dramatic changes in translational activity occur, indicating the prevalence of translational control of plastid gene expression in the chromoplast differentiation process.
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References
Arrand JE (1985) Preparation of nucleic acid probes. In: Hames BD, Higgins SJ (eds) Nucleic Acid hybridisation: a practical approach. IRL Press, Oxford, Washington, pp 17–45
Bathgate B, Purton ME, Grierson D, Goodenough PW (1985) Plastid changes during the conversion of chloroplasts to chromoplasts in ripening tomatoes. Planta 165:197–204
Batschauer A, Mösinger E, Kreuz K, Dörr I, Apel K (1986) The implication of a plastid-derived factor in the transcriptional control of nuclear genes encoding the light-harvesting chlorophyll a/b protein. Eur J Biochem 154:625–634
Blake MS, Johnston KH, Russel-Jones GJ, Gotschlich EC (1984) A rapid, sensitive method for detection of alkaline phosphatase-conjugated anti-antibody on western blots. Anal Biochem 136:175–179
Camara B (1985) Carotene synthesis in Capsicum chromoplasts. Methods Enzymol 110:244–253
Camara B, Monéger R (1978) Free and esterified carotenoids in green and red fruits of Capsicum annuum. Phytochemistry 17:91–93
Carde JP, Camara B, Cheniclet C (1988) Absence of ribosomes in Capsicum chromoplasts. Planta 173:1–11
Cozens AL, Walker JE, Phillips AL, Huttly AK, Gray JC (1986) A sixth subunit of ATP synthase, an F0 component in the pea chloroplast genome. EMBO J 5:217–222
Damerval C, De Vienne D, Zivy M, Thiellement H (1986) Technical improvements in two-dimensional electrophoresis increase the level of genetic variation detected in wheat seedling proteins. Electrophoresis 7:52–54
Davies LG, Dibner MD, Battey JF (1986) Basic Methods in Molecular Biology Elsevier, Amsterdam
Deng XW, Gruissem W (1987) Control of plastid gene expression during development: the limited role of transcriptional regulation. Cell 49:379–387
Deng XW, Stern DB, Tonkyn JC, Gruissem W (1987) Plastid runon transcription: application to determine the transcriptional regulation of spinach plastid genes. J Biol Chem 262:9641–9648
Dogbo O, Laferriere A, d'Harlingue A, Camara B (1988) Carotenoid synthesis: isolation and characterization of a bifunctional enzyme catalyzing the synthesis of phytoene. Proc Natl Acad Sci USA, 85:7054–7058
Fluhr R, Moses P, Morelli G, Coruzzi G, Chua NH (1986) Expression dynamics of the pea rbcS multigene family and organ distribution of the transcripts. EMBO J 5:2063–2071
Gidoni D, Bond-Nutter D, Brosio P, Jones J, Bedbrook J, Dunsmuir P (1988) Coordinated expression between two photosynthetic petunia genes in transgenic plants. Mol Gen Genet 211:507–514
Gounaris I, Price CA (1987) Plastid transcripts in chloroplasts and chromoplasts of Capsicum annuum. Curr Genet 12:219–224
Gounaris I, Michalowski C, Bohnert HJ, Price CA (1986) Comparison of chloroplast and chromoplast DNA. Curr Genet 11:7–16
Grierson D (1986) Molecular biology of fruit ripening. Oxford Surveys Plant Mol Cell Biol 3:363–383
Gruissem W, Zurawski G (1985) Analysis of promoter regions for the spinach chloroplast rbcL, atpB and psbA genes. EMBO J 4:3375–3383
Hansmann P, Junker R, Sauter H, Sitte P (1987) Chloroplast development in daffodil coronae during anthesis. J Plant Physiol 131:133–143
Herrmann RG, Westhoff P, Tittgen J, Nelson N (1985) Thylakoid membrane proteins and their genes. In: Van Vloten-Doting I, Groot GSP, Hall TC (eds) Molecular form and function of the plant genome. Plenum Publishing Corporation. New York, pp 233–256
Heyraud F, Serror P, Kuntz M, Steinmetz A, Heizmann P (1987) Physical map and gene localization on sunflower (Helianthus annuus) chloroplast DNA: evidence for an inversion of a 23.5-kbp segment in the large single copy region. Plant Mol Biol 9:485–496
Hultzmark D, Klemenz R, Gehring WJ (1986) Translational control elements in the untranslated leader of the heat shock genes hsp22. Cell 44:429–438
Klein RR, Mullet JE (1987) Control of gene expression during higher plant chloroplast biogenesis. J Biol Chem 262:4341–4348
Livne A, Gepstein S (1988) Abundance of the major chloroplast polypeptide during development and ripening of tomato fruits. Plant Physiol 87:239–243
Locker J (1979) Analytical and preparative electrophoresis of RNA in agarose-urea. Anal Biochem 98:358–367
Logemann J, Mayer JE, Schell J, Willmitzer L (1988) Differential expression of genes in potato tubers after wounding. Proc Natl Acad Sci USA 85:1136–1140
Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, New York
Mayfield SP, Taylor WC (1984) Carotenoid-deficient maize seedlings fail to accumulate light-harvesting chlorophyll a/b mRNA. Eur J Biochem 144:79–84
Meyerowitz EM (1987) In situ hybridization to RNA in plant tissue. Plant Mol Biol Rep 5:242–250
Mullet JE, Klein RR (1987) Transcription and RNA stability are important determinants of higher plant chloroplast RNA levels. EMBO J 6:1571–1579
Oelmüller R, Mohr H (1986) Photooxidative destruction of chloroplasts and its consequences for expression of nuclear genes. Planta 167:106–113
Piechulla B, Cholones Imlay KR, Gruissem W (1985) Plastid gene expression during fruit ripening in tomato. Plant Mol Biol 5:373–384
Piechulla B, Glick RE, Bahl H, Melis A, Gruissem W (1987) Changes in photosynthetic capacity and photosynthetic protein pattern during tomato fruit ripening. Plant Physiol 84:911–917
Piechulla B, Pichersky E, Cashmore AR, Gruissem W (1986) Expression of nuclear and plastid genes for photosynthesis-specific proteins during tomato fruit development and ripening. Plant Mol Biol 7:367–376
Schreier PH, Reiss B, Kuntz M (1988) Subcellular targeting of proteins in vivo and in vitro. In: Gelvin SB, Schilperoort RA (eds) Plant Molecular Biology Manual, Kluwer Academic Publishers, Dordrecht, Boston London, Chapter B5, pp 1–22
Shaw G, Kamen R (1986) A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46:659–667
Sheen JY, Bogorad L (1986) Differential expression of six light-harvesting chlorophyll a/b binding protein genes in maize leaf cell types. Proc Natl Acad Sci USA 83:7811–7815
Simpson J, Van Montagu M, Herrera-Estrella L (1986) Photosynthesis-associated gene families: differences in response to tissuespecific and environmental factors. Science 233:34–38
Stern DB, Gruissem W (1987) Control of plastid gene expression: 3′ inverted repeats act as mRNA processing and stabilizing elements, but do not terminate transcription. Cell 51:1145–1157
Sugita M, Gruissem W (1987) Developmental, organ-specific, and light-dependent expression of the tomato ribulose-1,5-bisphosphate carboxylase small subunit gene family. Proc Natl Acad Sci USA 84:7104–7108
Suziki S (1974) Ultrastructural development in cherry peppers during fruit ripening. Bot Mag Tokyo 87:165–178
Tobin E, Silverthorne J (1985) Light regulation of gene expression in higher plants. Annu Rev Plant Physiol 36:569–593
Van Grinsven MQJM, Kool AJ (1988) Plastid gene regulation during development: an intriguing complexity of mechanisms. Plant Mol Biol Rep 6:213–239
Vierling E, Alberte RS (1983) Regulation of the photosystem I reaction center. J Cell Biol 97:1806–1814
Waksman G, Freyssinet G (1987) Nucleotide sequence of a cDNA encoding the ribulose-1,5-carboxylase/oxygenase from sunflower (Helianthus annuus.). Nucleic Acids Res 15:1328
Williams RS, Bennett J (1983) Synthesis and assembly of thylakoid membrane proteins in isolated pea chloroplasts. methods. Enzymol 97:487–502
Wolter FP, Fritz CC, Willmitzer L, Schell J, Schreier PH (1988) RbcS genes in Solanum tuberosum: conservation of transit peptide and exon shuffling during evolution. Proc Natl Acad Sci USA 85:846–850
Wrench PM, Oliver M, Hiller RG, Brady C, Speirs J (1987) Changes in plastid proteins during ripening of tomato fruits. J Plant Physiol 129:89–102
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Kuntz, M., Evrard, JL., d'Harlingue, A. et al. Expression of plastid and nuclear genes during chromoplast differentiation in bell pepper (Capsicum annuum) and sunflower (Helianthus annuus). Mol Gen Genet 216, 156–163 (1989). https://doi.org/10.1007/BF00332245
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DOI: https://doi.org/10.1007/BF00332245