Abstract
In this study we have constructed a number of plants (cybrids), in which the nuclear genome of Nicotiana plumbaginifolia is combined with the plastome of Atropa belladonna, or the nuclear genome of N. tabacum with plastomes of Lycium barbarum, Scopolia carniolica, Physochlaine officinalis or Nolana paradoxa. Our biochemical and immunological analyses prove that in these cybrids the biogenesis of the chlorophyll a/b binding proteins (CAB) of the light harvesting complex II (LHCII) is altered. Besides normal sized CAB polypeptides of 27, 25.5 and 25 kDa, which become less abundant, the cybrids analyzed have additional polypeptides of 26, 24.5 and 24 kDa. Direct protein micro-sequencing showed that at least two truncated 26 kDa CAB polypeptides in plant cells containing a nucleus of N. plumbaginifolia and plastids of A. belladonna are encoded by the type 1 Lhcb genes. These polypeptides are 11–12 amino acids shorter at the N-terminus than the expected size. Based on the available data we conclude that the biogenesis of the LHCII in vivo may depend on plastome-encoded factor(s). These results suggest that plastome-encoded factors that cause specific protein degradation and/or abnormal processing might determine compartmental genetic incompatibility in plants.
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References
Abad MS, Clark SE, Lamppa GK (1989) Properties of a chloroplast enzyme that cleaves the chlorophyll a/b binding protein precursor. Plant Physiol 90:11–124
Abad MS, Oblong JE, Lamppa GK (1991) Soluble chloroplast enzyme cleaves preLHCP made in Escherichia coli to a mature form lacking a basic N-terminal domain. Plant Physiol 96:1220–1227
Bennett J (1991) Protein phosphorylation in green plant chloroplasts. Annu Rev Plant Physiol Plant Mol Biol 42:281–311
Camm EL, Green BR (1980) Fractionation of thylakoid membranes with the nonionic detergent octyl-β-d-glucopyranoside. Plant Physiol 66:428–432
Caspari E (1948) Cytoplasmic inheritance. Adv Genet 2:2–68
Castresana C, Staneloni R, Malik VS, Cashmore AR (1987) Molecular characterization of two clusters of genes encoding the type I CAB polypeptides of PSII in Nicotiana plumbaginifolia. Plant Mol Biol 10:117–126
Chia CP, Duesing JH, Arntzen CJ (1986) Developmental loss of photosystem II activity and structure in a chloroplast-encoded tobacco mutant, Lutescens-II. Plant Physiol 82:19–27
Clark SE, Abad MS, Lamppa GK (1989) Mutations at the transit peptide-mature protein junction separate two cleavage events during chloroplast import of the chlorophyll a/b-binding protein. J Biol Chem 264:17544–17550
D'Arcy WG (1979) The classification of the Solanaceae. In: Hawkes JG, Lester RN, Skelding AD (eds) The biology and taxonomy of the Solanaceae, vol. 7. Academic Press, London, pp 3–49
Darr SC, Sommerville SC, Arntzen CJ (1986) Monoclonal antibodies to the light-harvesting chlorophyll a/b protein complex of photosystem II. J. Cell Biol 103:733–740
Dewey RE, Timothy DH, Levings CS III (1987) A mitochondrial protein associated with cytoplasmic male sterility in the T cytoplasm of maize. Proc Natl Acad Sci USA 84:5374–5378
Gerstel DU (1980) Cytoplasmic male sterility in Nicotiana. North Carolina Agric Res Serv 263:1–31
Green BR, Pichersky E, Kloppstech K (1991) Chlorophyll a/b-binding proteins: an extended family. Trends Biochem Sci 16:181–186
Gleba YY, Komarnitsky IK, Kolesnik NN, Meshkiene I, Martyn GI (1985) Transmission genetics of the somatic hybridization process in Nicotiana. II. Plastome heterozygotes. Mol Gen Genet 198:476–481
Guiamet JJ, Schwartz E, Pichersky E, Nooden LD (1990) Characterization of cytoplasmic and nuclear mutations affecting chlorophyll and chlorophyll-binding proteins during senescence in soybean. Plant Physiol 96:227–231
Jansson S, Pichersky E, Bassi R, Green RB, Ikeuchi M, Melis A, Simpson DJ, Spangfort M, Staehelin A, Thornber JP (1992) A nomenclature for the genes encoding the chlorophyll a/b-binding proteins of higher plants. Plant Mol Biol Reporter 10:242–253
Johnson EM, Schnabelrauch LS, Sears BB (1991) A plastome mutation affects processing of both chloroplast and nuclear DNA-encoded plastid proteins. Mol Gen Genet 225:106–112
Houlne G, Schantz R (1987) Molecular analysis of the transcripts encoding the light-harvesting chlorophyll a/b protein in Euglena gracilis: unusual size of the mRNA. Curr Genet 12:611–616
Kirk JTO, Tilney-Bassett RAE (1978) The Plastids: chemistry, structure, growth and inheritance. Elsevier-North Holland, New York-Amsterdam
Kofer W, Glimelius K, Bonnett H (1991) Modifications of mitochondrial DNA cause changes in floral development in homeotic-like mutants of tobacco. Plant Cell 3:759–769
Kuchka MR, Goldschmidt-Clermont M, van Dillewijn J, Rochaix J-D (1989) Mutations at the Chlamydomonas nuclear NAC2 locus specifically affects stability of the chloroplast psbD transcript encoding polypeptide D2 of PSII. Cell 58:869–876
Kushnir SG, Shlumukov LR, Pogrebnyak NJ, Berger S, Gleba Y (1987) Functional cybrid plants possessing a Nicotiana genome and an Atropa plastome. Mol Gen Genet 209:159–163
Kushnir S, Babiychuk E, Bannikova M, Momot V, Cherep N, Gleba Y (1991) Nucleo-cytoplasmic incompatibility in cybrid plants possessing an Atropa genome and a Nicotiana plastome. Mol Gen Genet 225:225–230
Machold O, Simpson DJ, Moller BJ (1979) Chlorophyll-proteins of thylakoids from wild type and mutants of barley (Hordeum vulgare L.). Carlsberg Res Commun 44:235–254
Mayfield SP (1990) Chloroplast gene regulation: interaction of the nuclear and chloroplast genomes in the expression of photosynthetic proteins. Curr Biol 2:509–513
McCabe PF, Timmons AM, Dix PJ (1989) A simple procedure for the isolation of streptomycin resistant plants in Solanaceae. Mol Gen Genet 216:132–137
Michaelis P (1954) Cytoplasmic inheritance in Epilobium and its theoretical significance. Adv Genet 6:287–401
Moneger F, Smart CJ, Leaver CJ (1994) Nuclear restoration of cytoplasmic male sterility in sunflower is associated with tissue-specific regulation of a novel mitochondrial gene. EMBO J 13:8–17
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–497
Oehlkers F (1964) Cytoplasmic inheritance in the genus Streptocarpus Lindley. Adv Genet 12:329–371
Piccioni R, Bellemare G, Chua N-H (1982) Methods of polyacrylamide gel electrophoresis in the analysis and preparation of plant polypeptides. In: Edelman M, Hallick RB, Chua N-H (eds) Methods in chloroplast molecular biology. Elsevier Biomedical Press, pp 985–1014
Schmidt GW, Mishkind ML (1983) Rapid degradation of unassembled ribulose 1,5-bisphosphate carboxylase small subunit in chloroplasts. Proc Natl Acad Sci USA 80:2632–2636
Svab Z, Maliga P (1986) Nicotiana tabacum mutants with chloroplast encoded streptomycin resistance and pigment deficiency. Theor Appl Genet 72:637–643
Theg SM, Scott SV (1993) Protein import into chloroplasts. Trends Cell Biol 3:186–190
Thompson WF (1991) Physiological and molecular studies of light-regulated nuclear genes in higher plants. Annu Rev Plant Physiol Plant Mol Biol 42:423–466
Vierstra RD (1993) Protein degradation in plants. Annu Rev Plant Physiol Plant Mol Biol 44:385–410
Young EG, Hanson M (1987) A fused mitochondrial gene associated with cytoplasmic male sterility is developmentally regulated. Cell 50:41–49
Yuan J, Henry R, Cline K (1993) Stromal factor plays an essential role in protein integration into thylakoids that cannot be replaced by unfolding or by heat shock protein Hsp70. Proc Natl Acad Sci USA 90:8552–8556
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Communicated by R. G. Herrmann
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Babiychuk, E., Schantz, R., Cherep, N. et al. Alterations in chlorophyll a/b binding proteins in Solanaceae cybrids. Molec. Gen. Genet. 249, 648–654 (1995). https://doi.org/10.1007/BF00418034
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DOI: https://doi.org/10.1007/BF00418034