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Evolutionary consequences of genome-plastome interaction in Oenothera species and hybrids

Michael J Chapman, University of Massachusetts Amherst


Many Oenothera species are complete translocation heterozygotes and arose by hybridization. Since complete translocation heterozygosity suppresses nuclear genetic recombination, examination of any chloroplast gene effects on hybridization is particularly suitable in these flowering plants. To verify translocation status in Oenothera villaricae, Oe. picensis ssp. picensis and lines of their interspecific hybrids, meiotic figures from parents and hybrids were obtained using confocal optical sectioning (a new application of this technique). These data confirm published results, and are consistent with a bivalent-forming common ancestor which underwent translocations to produce each of the parent species. The full translocation ring appeared in only one of the four possible hybrid nuclei. Oenothera species of hybrid origin form translocation rings at meiosis; progenitor species are structurally homozygous and form seven bivalents. Comparison of ring- and bivalent-forming species revealed hollow, abortive pollen grains in the ring-forming species (25-30% relative to 0-3% abortive pollen abortion in bivalent-forming species). F$\sb1$ hybrids of the picensis maternal lineage may abort up to 85% of pollen; nonreciprocality in the corresponding villaricae hybrid indicates nucleocytoplasmic incompatibility. Statistical analysis shows a high correlation between pollen stainability and meiotic disjunction frequency in Oe. villaricae, Oe. picensis and hybrids, suggesting that the abortive grains are the products of nondisjunctional meiosis. Significant effects (P $<$.001) on disjunction frequency and pollen stainability were noted for nucleus and cytoplasm alone and in combination, revealing an interaction or combined effect of nucleus and cytoplasm. This combined effect influences the chromosomal pairing behavior at meiosis; hence also the pollen viability. The fitness consequences of cytoplasmic hybridization intolerance (e.g., chlorosis, pollen abortion, lethality) probably affect the relative success of incipient species. Of the two cytoplasmically inherited genetic systems, the plastid genome (plastome) is the more accessible to study. Five discrete European plastid genotypes (typified by Oe. hookeri, biennis, Lamarckiana, parviflora and argillicola), as well as those of South American Oe. villaricae and picensis, have been identified by restriction fragment length polymorphisms (RFLPs) using endonucleases PvuII, SalI, KpnI and PstI. The present RFLP study employed PvuII and KpnI to analyze plastid DNAs from across subsection Munzia, the South American taxonomic group which includes Oe. villaricae and picensis, in comparison with known European plastomes. Subsect. Munzia is divided into three series: Ancestral Renneria, the younger Allochroa, and the most recently evolved, Clelandia, composed entirely of hybrids between members of Renneria and Allochroa. At least ten new plastid genotypes are noted among 28 Munzia species examined. All three series were to some degree polymorphic. In certain hybrids of known origin, comparison of the cpDNA genetic fingerprint with those of the parent species can reveal the maternal and paternal lineage, i.e. the direction of hybridization. One particular cpDNA fingerprint which predominates throughout the subsection is presumed to represent the ancestral plastome type.

Subject Area

Botany|Genetics|Cellular biology

Recommended Citation

Chapman, Michael J, "Evolutionary consequences of genome-plastome interaction in Oenothera species and hybrids" (1997). Doctoral Dissertations Available from Proquest. AAI9721437.