Summary
The sequences of seven complementary DNAs or genes encoding the small subunit (SSU) of ribulose-1,5-bisphosphate carboxylase oxygenase (RUBISCO) in several Nicotianeae were examined. Two new SSU genes isolated fromNicotiana sylvestris were included. Both sequence comparisons and Southern analyses with specific probes reveal that SSU genes fall into two homogeneous subfamilies that are highly conserved in Nicotianeae and are also present in other Solanaceae. Additional criteria such as number of introns and level of expression fitted to this classification. Homogeneity must have been maintained by gene conversion and/or an unusually high fidelity of DNA replication, whereas traces of slippage-stranded DNA mispairing and/or transposition probably explain local changes. Taken as a whole, these results show that the divergence between the two subfamilies predated the divergence between genera inside the Solanaceae, but that Nicotianeae retained the most simple SSU gene family structure.
Similar content being viewed by others
References
Dean C, van den Elzen P, Tamaki S, Dunsmuir P, Bedbroock J (1985) Differential expression of the eight genes of the petunia ribulose bisphosphate carboxylase small subunit multigene family. EMBO J 4:3055–3061
Dean C, van den Elzen P, Tamaki S, Black M, Dunsmuir P, Bedroock J (1987) Molecular characterization of the rbcS multi-gene family of petunia (Mitchell). Mol Gen Genet 206: 465–474
Dover GA (1986) Molecular drive in multigene families: how biological novelties arise, spread and are assimilated. Trends Genet 2:159–165
Ellis RJ (1981) Chloroplast proteins: synthesis, transport and assembly. Annu Rev Plant Physiol 32:111–137
Fluhr R, Kuhlemeier C, Nagy F, Chua NH (1986) Organ-specific and light-induced expression of plant genes. Science 232: 1106–1112
Goodspeed TH (1954) The genusNicotiana: origins, relationships and evolution of its species in the light of their distribution, morphology and cytogenetics. Chronica Botanica Co., Waltham MA
Grandbastien MA, Spielmann A, Caboche M (1989) Tnt 1. a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature 337:376–380
Gray JC, King SD, Wildman SG, Shen SJ (1974) Origin ofNicotiana tabacum detected by polypeptide composition of fraction 1 protein. Nature 252:226–227
Jamet E, Durr A, Fleck J (1987) Absence of some truncated genes in the amphidiploidNicotiana tabacum. Gene 59:213–221
Jamet E, Fargeas C, Durr A, Fleck J (1990) Nucleotide sequences of two genes encoding the small subunit of RUBISCO inNicotiana sylvestris. Nucleic Acids Res 18:4589
Kunkel TA (1988) Exonucleolytic proofreading. Cell 53:837–840
Levinson G, Gutman GA (1987) Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 4:203–221
Maeda N, Smithies O (1986) The evolution of multigene families: human haptoglobin genes. Annu Rev Genet 20:81–108
Mazur BJ, Chui CF (1985) Sequence of a genomic DNA clone for the small subunit of ribulose bis-phosphate carboxylase-oxygenase from tobacco. Nucleic Acids Res 13:2373–2386
Meagher RB, Berry-Lowe S, Rice K (1989) Molecular evolution of the small subunit of ribulose bisphosphate carboxylase: nucleotide substitution and gene conversion. Genetics 123: 845–863
Okamuro JK, Goldberg RB (1985) Tobacco single-copy DNA is highly homologous to sequences present in the genomes of its diploid progenitors. Mol Gen Genet 198:290–298
O'Neal JK, Pokalsky AR, Kiehne KL, Shewmaker CK (1987) Isolation of tobacco SSU genes: characterization of a transcriptionally active pseudogene. Nucleic Acids Res 15:8661–8677
Pichersky E, Bernarzky R, Tanksley SD, Cashmore AR (1986) Evidence for selection as a mechanism in the concerted evolution ofLycopersicon esculentum (tomato) genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Proc Natl Acad Sci USA 83:3880–3884
Pinck M, Dore JM, Guilley E, Durr A, Pinck L, Hirth L, Fleck J (1986) A simple gene expression system for the small subunit of ribulose bisphosphate carboxylase in leaves ofN. sylvestris. Plant Mol Biol 7:301–309
Poulsen C, Chua NH (1988) Dissection of the 5′ upstream sequences for selective expression of theNicotiana plumbaginifolia rbcS-8B gene. Mol Gen Genet 214:16–23
Poulsen C, Fluhr R, Kauffman JM, Boutry M, Chua NH (1986) Characterization of an rbcS gene fromNicotiana plumbaginifolia and expression of an rbcS-CAT chimeric gene in homologous and heterologous nuclear background. Mol Gen Genet 205:193–200
Radman M, Wagner R (1988) The high fidelity of DNA duplication. Sci Am August 1988, pp 24–30
Roman H (1985) Gene conversion and crossing-over. Environ Mutagen 7:923–932
Saedler H, Nevers P (1985) Transposition in plants: a molecular model. EMBO J 4:585–590
Schwarz-Sommer Z, Gierl A, Cuypers H, Peterson A, Saedler H (1985) Plant transposable elements generate the DNA sequence diversity needed in evolution. EMBO J 4:591–597
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
Temin HM (1985) Reverse transcription in the eukaryotic genome: retroviruses: pararetroviruses, retrotransposons and retrotranscripts. Mol Biol Evol 2:455–468
Uchiyama H, Chen K, Wildman SG (1977) Polypeptide composition of fraction I protein as an aid in the study of plant evolution. Stadler Symp 9:83–99
Weiner A, Deininger PL, Efstratiadis A (1986) Nonviral retroposons: genes, pseudogenes, and transposable elements generated by the reverse flow of genetic information. Annu Rev Biochem 55:631–661
Wolter FP, Fritz CC, Willmitzer L, Schell J, Schreier P (1988) rbcS genes inSolanum tuberosum: conservation of transit peptide and exon shuffling during evolution. Proc Natl Acad Sci USA 85:846–850
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Jamet, E., Parmentier, Y., Durr, A. et al. Genes encoding the small subunit of RUBISCO belong to two highly conserved subfamilies in Nicotianeae. J Mol Evol 33, 226–236 (1991). https://doi.org/10.1007/BF02100673
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF02100673