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Expression of nuclear and plastid genes for photosynthesis-specific proteins during tomato fruit development and ripening

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Summary

The expression of plastid and nuclear genes coding for photosynthesis-specific proteins has been studied during tomato fruit formation. The steady-state transcript levels for the large (rbcL) and small (rbcS) subunit of RuBPC/Oase, as well as the thylakoid membrane proteins, the 32 kD QB-binding protein of PS II (psbA), the P700 reaction center protein of PS I (psaA) and the chlorophyll a/b-binding protein (cab) vary at different time points during fruit development and ripening. Messenger RNA levels of plastid-encoded photosynthesis-specific genes (rbcL, psbA) are at least several fold higher, relative to respective nuclear-encoded genes (rbcS, cab). The transcript levels for the large and small subunit of RuBPC/Oase are highest in approximately 14-day-old tomato fruits, while the chl a/b-binding protein, the P700 reaction center protein and the 32 kD QB-binding protein reach their maxima in approximately 7-, 14- and 25-day-old tomato fruits, respectively. The inactivation of the photosynthesis-specific genes occurs during the first period of fruit formation. In addition, there is considerable variation in the mRNA levels of these photosynthesis-specific genes in four organs of tomato (leaves, fruits, stems, roots).

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References

  1. Alexander DC, McKnight TD, Williams BG: A simplified and efficient vector-primer cDNA cloning system. Gene 31:79–89, 1984.

    Google Scholar 

  2. Bedbrook JR, Link G, Coen DM, Bogorad L, Rich A: Maize plastid gene expression during photoregulated development. Proc Natl Acad Sci USA 75:3060–3064, 1978.

    Google Scholar 

  3. Ben-Shaul Y, Naftali Y: The development and ultrastructure of lycopene bodies in chromoplasts of Lycopersicon esculentum. Protoplasma 67:333–334, 1969.

    Google Scholar 

  4. Berry JO, Nikolau BJ, Carr JP, Klessig DF: Transcriptional and post-transcriptional regulation of ribulose-1.5-bisphosphate carboxylase gene expression in light- and darkgrown Amaranth cotyledons. Mol Cell Biol 5:2238–2246, 1985.

    Google Scholar 

  5. Berry-Lowe SL, McKnight TD, Shah DM, Meagher RB: The nucleotide sequence, expression, and evolution of one member of a multigene family encoding the small subunit of ribulose-1.5-bisphosphate carboxylase in soybean. J Mol Appl Gen 1:483–498, 1982.

    Google Scholar 

  6. Cashmore AR: Reiteration frequency of the gene coding for the small subunit of ribulose-1.5-bisphosphate carboxylase. Cell 17:383–388, 1979.

    Google Scholar 

  7. Coruzzi G, Broglie R, Cashmore AR, Chua NH: Nucleotide sequences of two pea cDNA clones encoding the small subunit of ribulose-1.5-bisphosphate carboxylase and the major chlorophyll a/b binding thylakoid polypeptide. J Biol Chem 258:1399–1402, 1983.

    Google Scholar 

  8. Crossland LD, Rodermel SR, Bogorad L: Single gene for the large subunit of ribulosebisphosphate carboxylase in maize yields two differentially regulated mRNAs. Proc Natl Acad Sci USA 81:4060–4064, 1984.

    Google Scholar 

  9. Davies JW, Cocking EC: Changes in carbohydrates, proteins and nucleic acids during cellular development in tomato fruit locule tissue. Planta 67:242–253, 1965.

    Google Scholar 

  10. Dean C, van den Elzen P, Tamaki S, Dunsmuir P, Bedbrook J: Differential expression of the eight genes of the petunia ribulose-1.5-bisphosphate carboxylase small subunit multigene family. EMBO J 4:3055–3061, 1985.

    Google Scholar 

  11. Dunsmuir P, Smith SM, Bedbrook J: The major chlorophyll a/b binding protein of petunia is composed of several polypeptides encoded by a number of distinct nuclear genes. J Mol Appl Gen 2:285–300, 1983.

    Google Scholar 

  12. Erion JL: Characterization of the mRNA transcripts of the maize, ribulose-1.5-bisphosphate carboxylase, large subunit gene. Plant Mol Biol 4:169–179, 1985.

    Google Scholar 

  13. Gruissem W, Zurawski G: Analysis of promoter regions for the spinach chloroplast rbcL, atpB, psbA genes. EMBO J 4:3375–3383, 1985.

    Google Scholar 

  14. Hall TC: Plant messenger RNA. In: Hall TC, Davies JW (eds) Nucleic acids in plants. CRC Press, Boca Roton, Florida, 1979, 217–225.

    Google Scholar 

  15. Harpster M, Apel K: The light-dependent regulation of gene expression during plastid development in higher plants. Physiol Plant 64:147–152, 1985.

    Google Scholar 

  16. Harpster M, Mayfield SP, Taylor WC: Effects of pigment-deficient mutants on the accumulation of photosynthetic proteins in maize. Plant Mol Biol 3:59–71, 1984.

    Google Scholar 

  17. Harris WM, Spurr AR: Chromoplasts of tomato fruits: I. Ultrastructure of low-pigment and high-beta mutants: carotene analyses, Amer J Bot 56:369–379, 1969.

    Google Scholar 

  18. Harris WM, Spurr AR: Chromoplasts of tomato fruits: II. The red tomato. Amer J Bot 56:380–389, 1969.

    Google Scholar 

  19. Herrera-Estrella L, van den Broeck G, Maenhaut R, van Montagu M, Schell J, Timko M, Cashmore A: Light-inducible and chloroplast-associated expression of a chimaeric gene introduced into Nicotiana tabacum using Ti plasmid vector. Nature 310:115–120, 1984.

    Google Scholar 

  20. Herrmann RG, Westhoff P, Alt J, Tittgen J, Nelson N: Thylakoid membrane proteins and their genes. In: van Vloten-Doting L, Groot GSP, Hall TC (eds) Molecular form and function of the plant genome. Plenum Press, New York, London, 1984, pp 233–256.

    Google Scholar 

  21. Inamine G, Nash B, Weissbach H, Brot N: Light regulation of the synthesis of the large subunit of ribulose-1.5-bisphosphate carboxylase in peas: Evidence for translational control. Proc Natl Acad Sci USA 82:5690–5694, 1985.

    Google Scholar 

  22. Iwatsuki N, Hirai A, Asahi T: A comparison of tomato fruit chloroplast and chromoplast DNAs as analyzed with restriction endonucleases. Plant Cell Physiol 26:599–601, 1985.

    Google Scholar 

  23. Jorgensen RA, Cuellar RE, Thompson WF: Modes and tempos in the evolution of nuclear-encoded ribosomal RNA genes in legumes. Carnegie Institution of Washington Year Book 81:98–101, 1981–1982.

    Google Scholar 

  24. Kleinkopf GE, Huffaker RC, Matheson A: Light-induced de novo synthesis of ribulose-1.5-bisphosphate carboxylase in greening leaves of barley. Plant Physiol 46:416–418, 1970.

    Google Scholar 

  25. Lamppa GK, Morelli G, Chua NH: Structure and developmental regulation of a wheat gene encoding the major chlorophyll a/b-binding polypeptide. Mol Cell Biol 5:1370–1378, 1985.

    Google Scholar 

  26. Link G, Langridge U: Structure of the chloroplast gene for the precursor of the Mr 32000 photosystem II protein from mustard (Sinapsis alba I). Nucl Acid Res 12:945–958, 1984.

    Google Scholar 

  27. Maniatis T, Fritsch EF, Sambrook J: Molecular cloning, a laboratory manual. Cold Spring Harbor, 1982.

  28. Morelli G, Nagy F, Fraley RT, Rogers SG, Chua NH: A short conserved sequence is involved in the light-inducibility of a gene encoding ribulose-1.5-bisphosphate carboxylase small subunit of pea. Nature 315:200–204, 1985.

    Google Scholar 

  29. Mullet JE, Orozco EM, Chua NH: Multiple transcripts for higher plant rbcL and atpB genes and localization of the transcription initiation site of the rbcL gene. Plant Mol Biol 4:39–54, 1985.

    Google Scholar 

  30. Nelson T, Harpster MH, Mayfield SP, Taylor WC: Light-regulated gene expression during maize leaf development. J Cell Biol 98:558–564, 1984.

    Google Scholar 

  31. Pichersky E, Bernatzky R, Tanksley SD, Cashmore AR: Evidence for selection as a mechanism in the concerted evolution of Lycopersicon esculentum (tomato) genes encoding the small subunit of ribulose-1.5-bisphosphate carboxylase/oxygenase. Proc Natl Acad Sci USA, in press, 1986.

  32. Pichersky E, Bernatzky R, Tanksley SD, Breidenbach RW, Kausch AP, Cashmore AR: Molecular characterization and genetic mapping of two clusters of genes encoding chlorophyll a/b-binding proteins in Lycopersicon esculentum (tomato). Gene 40:247–258, 1985.

    Google Scholar 

  33. Piechulla B, Chonoles Imlay KR, Gruissem W: Plastid gene expression during fruit ripening in tomato. Plant Mol Biol 5:373–384, 1985.

    Google Scholar 

  34. Piechulla B, Glick RE, Bahl H, Melis A, Gruissem W: Changes in photosynthetic capacity and photosynthetic protein pattern during tomato fruit ripening. Plant Physiol, in press, 1986.

  35. Phillips AL: Localization of genes for chloroplast components in tomato plastid DNA. Current Genetics 10:153–161, 1985.

    Google Scholar 

  36. Poulsen C: Two mRNA species differing by 258 nucleotides at the 5′ end are formed from barley chloroplast rbcL gene. Carlsberg Res Commun 49:89–104, 1984.

    Google Scholar 

  37. Rosso SW: The ultrastructure of chromoplast development in red tomato. J Ultrastruc Res 25:307–322, 1968.

    Google Scholar 

  38. Sasaki Y, Ishiye M, Sakihama T, Kamikubo T: Light-induced increase in mRNA activity coding for the small subunit of ribulose-1.5-bisphosphate carboxylase. J Biol Chem 256:2315–2320, 1981.

    Google Scholar 

  39. Sasaki Y, Tomoda Y, Komikubo T: Light regulates the expression of ribulose-1.5-bisphosphate carboxylase at the level of transcription and gene dosage in greening pea leaves. FEBS Lett 173:31–35, 1984.

    Google Scholar 

  40. Schmidt GW, Mishkind ML: Rapid degradation of unassembled ribulose-1.5-bisphosphate carboxylase small subunits in chloroplasts. Proc Natl Acad Sci USA 80:2632–2636, 1983.

    Google Scholar 

  41. Shinozaki K, Sugiura M: The nucleotide sequence of the tobacco chloroplast gene for the large subunit of ribulose-1.5-bisphosphate carboxylase/oxygenase. Gene 20:91–102, 1982.

    Google Scholar 

  42. Shinozaki K, Sasaki Y, Sakihama T, Kamikubo T: Coordinate light-induction of two mRNAs, encoded in nuclei and chloroplasts, of ribulose-1.5-bisphosphate carboxylase/oxygenase. FEBS Lett 144:73–76, 1982.

    Google Scholar 

  43. Simpson J, Timko M, Cashmore AR, Schell J, van Montagu M, Herrera-Estrella L: Light-inducible and tissue-specific expression of a chimaeric gene under control of the 5′-flanking sequence of pea chlorophyll a/b-binding protein gene. EMBO J 4:2723–2729, 1985.

    Google Scholar 

  44. Smeekens S, de Groot M, van Binsbergen J, Weisbeek P: Sequence of the precursor of the chloroplast thylakoid lumen protein plastocyanin. Nature 317:456–458, 1985.

    Google Scholar 

  45. Smith SM, Ellis RJ: Light-stimulated accumulation of transcripts of nuclear and chloroplast genes for ribulose-1.5-bisphosphate carboxylase. J Mol Appl Gen 1:127–137, 1981.

    Google Scholar 

  46. Sugita M, Sugiura M: Nucleotide sequence and transcription of the gene for the 32000 dalton thylakoid membrane protein from Nicotiana tabacum. Mol Gen Genet 195:308–313, 1984.

    Google Scholar 

  47. Tobin EM, Silverthorne J: Light regulation of gene expression in higher plant. In: Annual review of Plant Physiology, in press, 1986.

  48. Westhoff P, Alt J, Nelson N, Bottomley W, Buenemann H, Herrmann RG: Genes and transcripts for the P700 chlorophyll a apoprotein and subunit of the photosystem I reaction center complex from spinach thylakoid membranes. Plant Mol Biol 2:95–107, 1983.

    Google Scholar 

  49. Westhoff P, Alt J, Herrmann RG: Localization of the two chlorophyll a-conjugated polypeptides (mol. wt. 51 and 44 kd) of the photosystem II reaction center on the spinach plastid chromosome. EMBO J 2:2229–2237, 1983.

    Google Scholar 

  50. Zurawski G, Bohnert HJ, Whitfeld PR, Bottomley W: Nucleotide sequence of the gene for the Mr 32000 thylakoid membrane protein from Spinach oleracea and Nicotiana debneyi predicts a totally conserved primary translation product of Mr 38950. Proc Natl Acad Sci USA 79:7699–7703, 1982.

    Google Scholar 

  51. Zurawski G, Perrot B, Bottomley W, Whitfeld PR: The structure of the gene for the large subunit of ribulose-1.5-bisphosphate carboxylase from spinach chloroplast DNA. Nucl Acid Res 9:3251–3270, 1981.

    Google Scholar 

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Piechulla, B., Pichersky, E., Cashmore, A.R. et al. Expression of nuclear and plastid genes for photosynthesis-specific proteins during tomato fruit development and ripening. Plant Mol Biol 7, 367–376 (1986). https://doi.org/10.1007/BF00032566

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  • DOI: https://doi.org/10.1007/BF00032566

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