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Plant Physiology logoLink to Plant Physiology
. 1996 Jun;111(2):619–626. doi: 10.1104/pp.111.2.619

Developmental and stress regulation of gene expression for plastid and cytosolic isoprenoid pathways in pepper fruits.

P Hugueney 1, F Bouvier 1, A Badillo 1, J Quennemet 1, A d'Harlingue 1, B Camara 1
PMCID: PMC157874  PMID: 8787029

Abstract

Plant cells synthesize a myriad of isoprenoid compounds in different subcellular compartments, which include the plastid, the mitochondria, and the endoplasmic reticulum cytosol. To start the study of the regulation of these parallel pathways, we used pepper (Capsicum annuum) fruit as a model. Using different isoprenoid biosynthetic gene probes from cloned cDNAs, we showed that only genes encoding the plastid enzymes (geranylgeranyl pyrophosphate synthase, phytoene synthase, phytoene desaturase, and capasanthin-capsorubin synthase) are specifically triggered during the normal period of development, at the ripening stage. This pattern of expression can be mimicked and precociously induced by a simple wounding stress. Concerning the cytosol-located enzymes, we observed that the expression of the gene encoding farnesyl pyrophosphate synthase is constitutive, whereas that of farnesyl pyrophosphate cyclase (5-epi-aristolochene synthase) is undetectable during the normal development of the fruit. The expression of these later genes are, however, only selectively triggered after elicitor treatment. The results provide evidence for developmental control of isoprenoid biosynthesis occurring in plastids and that cytoplasmic isoprenoid biosynthesis is regulated, in part, by environmental signals.

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Selected References

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  1. Bouvier F., Hugueney P., d'Harlingue A., Kuntz M., Camara B. Xanthophyll biosynthesis in chromoplasts: isolation and molecular cloning of an enzyme catalyzing the conversion of 5,6-epoxycarotenoid into ketocarotenoid. Plant J. 1994 Jul;6(1):45–54. doi: 10.1046/j.1365-313x.1994.6010045.x. [DOI] [PubMed] [Google Scholar]
  2. Camara B., Hugueney P., Bouvier F., Kuntz M., Monéger R. Biochemistry and molecular biology of chromoplast development. Int Rev Cytol. 1995;163:175–247. doi: 10.1016/s0074-7696(08)62211-1. [DOI] [PubMed] [Google Scholar]
  3. Campbell A. D., Huysamer M., Stotz H. U., Greve L. C., Labavitch J. M. Comparison of ripening processes in intact tomato fruit and excised pericarp discs. Plant Physiol. 1990 Dec;94(4):1582–1589. doi: 10.1104/pp.94.4.1582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Casey W. M., Keesler G. A., Parks L. W. Regulation of partitioned sterol biosynthesis in Saccharomyces cerevisiae. J Bacteriol. 1992 Nov;174(22):7283–7288. doi: 10.1128/jb.174.22.7283-7288.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chappell J. The Biochemistry and Molecular Biology of Isoprenoid Metabolism. Plant Physiol. 1995 Jan;107(1):1–6. doi: 10.1104/pp.107.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chappell J., Wolf F., Proulx J., Cuellar R., Saunders C. Is the Reaction Catalyzed by 3-Hydroxy-3-Methylglutaryl Coenzyme A Reductase a Rate-Limiting Step for Isoprenoid Biosynthesis in Plants? Plant Physiol. 1995 Dec;109(4):1337–1343. doi: 10.1104/pp.109.4.1337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Coggins C. W., Jr, Henning G. L., Yokoyama H. Lycopene accumulation induced by 2-(4-chlorophenylthio)-triethylamine hydrochloride. Science. 1970 Jun 26;168(3939):1589–1590. doi: 10.1126/science.168.3939.1589. [DOI] [PubMed] [Google Scholar]
  8. Delourme D., Lacroute F., Karst F. Cloning of an Arabidopsis thaliana cDNA coding for farnesyl diphosphate synthase by functional complementation in yeast. Plant Mol Biol. 1994 Dec;26(6):1867–1873. doi: 10.1007/BF00019499. [DOI] [PubMed] [Google Scholar]
  9. Deruère J., Römer S., d'Harlingue A., Backhaus R. A., Kuntz M., Camara B. Fibril assembly and carotenoid overaccumulation in chromoplasts: a model for supramolecular lipoprotein structures. Plant Cell. 1994 Jan;6(1):119–133. doi: 10.1105/tpc.6.1.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Facchini P. J., Chappell J. Gene family for an elicitor-induced sesquiterpene cyclase in tobacco. Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):11088–11092. doi: 10.1073/pnas.89.22.11088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gillaspy G., Ben-David H., Gruissem W. Fruits: A Developmental Perspective. Plant Cell. 1993 Oct;5(10):1439–1451. doi: 10.1105/tpc.5.10.1439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Green T. R., Baisted D. J. Development of the activities of enzymes of the isoprenoid pathway during early stages of pea-seed germination. Biochem J. 1972 Dec;130(4):983–995. doi: 10.1042/bj1300983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hugueney P., Camara B. Purification and characterization of farnesyl pyrophosphate synthase from Capsicum annuum. FEBS Lett. 1990 Oct 29;273(1-2):235–238. doi: 10.1016/0014-5793(90)81093-4. [DOI] [PubMed] [Google Scholar]
  14. Hugueney P., Römer S., Kuntz M., Camara B. Characterization and molecular cloning of a flavoprotein catalyzing the synthesis of phytofluene and zeta-carotene in Capsicum chromoplasts. Eur J Biochem. 1992 Oct 1;209(1):399–407. doi: 10.1111/j.1432-1033.1992.tb17302.x. [DOI] [PubMed] [Google Scholar]
  15. Koyama T., Fujii H., Ogura K. Enzymatic hydrolysis of polyprenyl pyrophosphates. Methods Enzymol. 1985;110:153–155. doi: 10.1016/s0076-6879(85)10070-4. [DOI] [PubMed] [Google Scholar]
  16. Kuntz M., Römer S., Suire C., Hugueney P., Weil J. H., Schantz R., Camara B. Identification of a cDNA for the plastid-located geranylgeranyl pyrophosphate synthase from Capsicum annuum: correlative increase in enzyme activity and transcript level during fruit ripening. Plant J. 1992 Jan;2(1):25–34. doi: 10.1111/j.1365-313x.1992.00025.x. [DOI] [PubMed] [Google Scholar]
  17. Römer S., Hugueney P., Bouvier F., Camara B., Kuntz M. Expression of the genes encoding the early carotenoid biosynthetic enzymes in Capsicum annuum. Biochem Biophys Res Commun. 1993 Nov 15;196(3):1414–1421. doi: 10.1006/bbrc.1993.2410. [DOI] [PubMed] [Google Scholar]
  18. Schaller H., Grausem B., Benveniste P., Chye M. L., Tan C. T., Song Y. H., Chua N. H. Expression of the Hevea brasiliensis (H.B.K.) Mull. Arg. 3-Hydroxy-3-Methylglutaryl-Coenzyme A Reductase 1 in Tobacco Results in Sterol Overproduction. Plant Physiol. 1995 Nov;109(3):761–770. doi: 10.1104/pp.109.3.761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Tjamos E. C., Kucacute J. A. Inhibition of steroid glycoalkaloid accumulation by arachidonic and eicosapentaenoic acids in potato. Science. 1982 Aug 6;217(4559):542–544. doi: 10.1126/science.217.4559.542. [DOI] [PubMed] [Google Scholar]
  20. Verwoerd T. C., Dekker B. M., Hoekema A. A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res. 1989 Mar 25;17(6):2362–2362. doi: 10.1093/nar/17.6.2362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Vögeli U., Chappell J. Induction of sesquiterpene cyclase and suppression of squalene synthetase activities in plant cell cultures treated with fungal elicitor. Plant Physiol. 1988 Dec;88(4):1291–1296. doi: 10.1104/pp.88.4.1291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ward E. R., Uknes S. J., Williams S. C., Dincher S. S., Wiederhold D. L., Alexander D. C., Ahl-Goy P., Metraux J. P., Ryals J. A. Coordinate Gene Activity in Response to Agents That Induce Systemic Acquired Resistance. Plant Cell. 1991 Oct;3(10):1085–1094. doi: 10.1105/tpc.3.10.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Wright R., Basson M., D'Ari L., Rine J. Increased amounts of HMG-CoA reductase induce "karmellae": a proliferation of stacked membrane pairs surrounding the yeast nucleus. J Cell Biol. 1988 Jul;107(1):101–114. doi: 10.1083/jcb.107.1.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Zhang H., Scholl R., Browse J., Somerville C. Double stranded DNA sequencing as a choice for DNA sequencing. Nucleic Acids Res. 1988 Feb 11;16(3):1220–1220. doi: 10.1093/nar/16.3.1220. [DOI] [PMC free article] [PubMed] [Google Scholar]

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