Cytoplasmatic Effects Detected in Various Crops

Introduction from C. LEAVER:
Cytoplasmic genetic information has been ignored as a source of genetic diversity for a long time, which is surprising, given that the mitochondrion and chloroplasts are the major site of energy conversion in the cell and thus play a vital role in determining the overall performance and productivity of crop plants. The cytoplasmic diversity detectable within a series of distantly related varieties is thought to correspond to their nuclear divergence. This reflects nuclear cytoplasmic interactions which can be responsible for the breeding success. Usage of information about correlations between nuclear and organellar genomes could be important in order to optimize their compatibility.
Most, if not all of the major changes which occur during growth and differentiation of higher plants are associated with or dependent upon, marked changes in the number, structure and metabolic activity, of either one or both organelles (LEAVER and GRAY 1982; TOPPING and LEAVER 1990). They also represent a source of genetic diversity in that they both contain their own specific DNA and the transcriptional and translational machinery to express this information as RNA and proteins. However, the biogenesis of both organelles requires the coordinated expression of both nuclear and organellar genomes (SCHUSTER and BRENNICKE 1994). Plant mitochondrial genomes are generally large, multicircular and contain sequences of different stoichiometry. Evolution of these complex genomes appears to occur via reorganization of sequences rather than by point mutation. Within most crop species characteristic differences exist between their mitochondrial genome organisations. Many of these differences probably have no phenotypic consequence. However in specific lines some deviating phenotypes have been shown to be due to the modification of existing genes or the creation of novel genes by aberrant intra- or inter- molecular DNA recombination events (KÖHLER et al. 1991, LÖSSL et al. 1999). These chimaeric genes are expressed as variant polypeptides, which in most cases are associated with the energy-transducing inner mitochondrial membrane, and appear to be causally related to male sterile phenotype or toxin sensitivity as shown for maize by BRAUN et al. (1989).
The only cytoplasmically inherited trait which has been exploited by the plant breeder so far is cytoplasmic male sterility (CMS) which in most cases results from either, an incompatibility between the nuclear genome of one race or species and the mitochondrial genome of another, or specific mutations in the mitochondrial genome. Despite CMS-cytoplasms being rarely used, the analysis of recombinant chondriomes which derive from distant crosses, could prevent similar disasters to that experienced with the so called ´Texas cytoplasm´.
An other phenotype has been described by NEWTON et al. (1990) and by LIN and YU (1995) who observed a maternally inherited phenotype in maize, called nonchromosomal stripes (NCS5) that adversely affects plant growth and yield. Mutant plants are characterized by reduced height, defective yellow striping on leaves, and aborted kernels on ears. The phenomenon is correlated to a mitochondrial recombination event and a reduction of functional coxII genes.
For plant breeding these phenomena appear as side effects and are not of interest as they can be avoided. But in most cases the influence of the cytoplasmic type is not distinguished from biparental inherited traits. Moreover, cytoplasmic phenotypes only occur in combination with distinct nuclear backgrounds and thus hamper the recognition in further breeding work.
Therefore maize breeders give contradictory empirical statements about the effects of the cytoplasmic complement. Unintended counterselection of distinct organellar types takes place, as long as the agronomical value of different cytoplasms remains unknown. Only few reports exist about maternal inherited traits in corn so far. EAGLES and HARDACRE (1989) investigated synthetic populations of maize and compared diallele crosses including reciprocals: The different cytoplasms had influence on grain moisture and silking date, which suggests that cytoplasmic inheritance should be considered when utilizing highland tropical populations. In wheat different cytoplasmic backgrounds have allready been evaluated. For distinct cytoplasms JOHNSON and LUCKEN (1986) detected different effects on seed germination and seedling vigour. Influence of cytoplasmic composition can also be observed in dicotyledones. Within several somatic hybrids of potato with nearly isogenic nuclear genomes differences in hybrid vigour occurred, which were due to a different degree of mitochondrial recombinations (LÖSSL et al. 1994).
Only an optimized mt-cp configuration allowed an efficient interaction with the new generated cell composition.
Evaluations of yield data from fusion populations revealed a superiority for homogenous mitochondrial genomes (Lössl et al. 1994). Such differences could be due to ´biological costs´, which are associated to nuclear-mitochondrial incompatibilities as reported by Mc VETTY and PINNISCH (1994) for different plasma types in Brassica
A first approach for the evaluation of cytoplasmic potential consists of an organellar DNA library. Isolation of chloroplasts and mitochondria and  their DNA is necessary for the production of homologuous probes which serve for an analysis of the more or less far related lines and varieties.

written by A. Lössl (Introduction from C. Leaver)


BRAUN, C.J., SIEDOW, J.N., WILLIAMS, M.E., and LEVINGS III, C.S., (1989): Mutations in the maize mitochondrial T-urf13 gene eliminate sensitivity to a fungal pathotoxin. Proc. Natl. Acad. Sci. 86: 4435-4439

EAGLES, H.A. and HARDACRE, A.K., (1989): Synthetic populations of maize containing highland Mexican or highland Peruvian germplasm. Crop Sci. 29: 660-665

JOHNSON, K.M. and LUCKEN, K.A., (1986): Characteristics and performance of male sterile and hybrid seed produced by cross-pollination in hard red spring wheat. Crop Sci. 26: 55-57

KÖHLER, R., HORN, R., LÖSSL, A. and ZETSCHE, K., (1991): Cytoplasmic male sterility in sunflower is correlated with the co-transcription of a new open reading frame with the atpA gene. Mol. Gen. Genet. 227: 369-376

LÖSSL, A., FREI, U. and WENZEL, G., (1994): Interaction between cytoplasmic composition and yield parameters in somatic hybrids of S. tuberosum L. Theor. Appl. Genet. 89:  873-878

LÖSSL, A., ADLER, N., HORN, FREI, U. and WENZEL, G., (1999): Chondriome Type Characterization of Potato: Mt a, b, g, d, e and Novel Plastid-Mitochondrial Configurations. Theor. Appl. Genet. 99: 1-10

LEAVER, C.J. and GRAY, M., (1982): Mitochondrial genome organization and expression in higher plants. Ann. Rev. Plant Physiol. 33: 373-402

LIN, B.-Y. and YU, H.-J. (1995): Inheritance of a striped-leaf mutant is associated with the cytoplasmic genome in maize. Theor. Appl. Genet. 91: 915-920

Mc VETTY, P.B., PINNISCH, R. (1994) Comparison of the effect of nap and pol cytoplasms on the performance of three summer oilseed rape cultivar-derived isoline pairs. Can. J. Plant Sci. 74: 729-731

NEWTON, K.J., KNUDSEN, C., GABAY-LAUGHNAN, S. and LAUGHNAN, J.R., (1990): An abnormal growth mutant in maize has a defective mitochondrial cytochrome oxidase gene. Plant Cell 2: 107-113

SCHUSTER, W. and BRENNICKE, A., (1994): The plant mitochondrial genome: Physical structure, Information content, RNA editing, and gene migration to the nucleus. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45: 61-78

TOPPING, J.F. and LEAVER, C.J., (1990): Mitochondrial gene expression during wheat leaf development. Planta 182: 399-407

written by A. Lössl (Introduction from C. Leaver)
Andreas Lössl
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