Proc. Natl. Acad. Sci. USA 92: 7719-7723 (Aug 1995)
Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution
Keming Song, Ping Lu, Keliang Tang, and Thomas C. Osborn

ABSTRACT Although the evolutionary success of polyploidy in higher plants has been widely recognized, there is virtually no information on how polyploid genomes have evolved after their formation. In this report, we used synthetic polyploids of Brassica as a model system to study genome evolution in the early generations after polyploidization. The initial polyploids we developed were completely homozygous, and thus, no nuclear genome changes were expected in self-fertilized progenies. However, extensive genome change was detected by 89 nuclear DNA clones used as probes. Most genome changes involved loss and/or gain of parental restriction fragments and appearance of novel fragments. Genome changes occurred in each generation from F2 to F5, and the frequency of change was associated with divergence of the diploid parental genomes. Genetic divergence among the derivatives of synthetic polyploids was evident from variation in genome composition and phenotypes. Directional genome changes, possibly influenced by cytoplasmic-nuclear interactions, were observed in one pair of reciprocal synthetics. Our results demonstrate that polyploid species can generate extensive genetic diversity in a short period of time. The occurrence and impact of this process in the evolution of natural polyploids is unknown, but it may have contributed to the success and diversification of many polyploid lineages in both plants and animals.

Plant Materials. The synthetic polyploids used in this study were derived from reciprocal interspecific hybridizations between single plants of the diploid species B. rapa (A genome), B. nigra (B genome), and B. oleracea (C genome) (17) and are designated as AB (A X B), BA (B X A), AC (A X C), and CA (C X A). AB and BA are reciprocal hybrids analogous to the natural polyploid B. juncea, and AC and CA are reciprocal hybrids analogous to the natural polyploid B. napus. The colchicine doubled hybrids were bud self-pollinated to form F2 progenies (17). For each synthetic polyploid, nine F5 plants were derived from a single F2 plant by controlled bud self-pollination in isolation.

Directional Genome Change and Cytoplasmic Effect. The synthetic polyploids were analyzed for directional changes in their component genomes by comparing genetic distances of F2 and F5 individuals to each of their diploid parents (Fig. 3). For the AB polyploid, the nine F5 plants showed significant directional change away from the B genome parent but not from the A genome parent (Fig. 3, AB). Most of the directional change was probably due to greater loss of B genome fragments than A genome fragments (25 vs. 9, respectively, Table 1). For the BA polyploid, there was no significant directional change when all nine F5 plants were included in the analysis (Fig. 3, BA). However, five of the plants (BAF5-2, -3, -4, -8, and -9) derived from two F4 plants showed much higher levels of change, and these five plants deviated significantly from both the A and B diploid parents. In four of the five plants, the A genome changed more than the B genome, an opposite situation to that observed in the AB polyploid.

Because the synthetic polyploids we developed contained maternally donated cytoplasm (17), differences in cytoplasmic-nuclear interactions of specific genomes could have contributed to differences in the extent and direction of genome changes. The AB polyploid contained the A genome cytoplasm, and in these plants the paternally donated nuclear genome (B genome) showed significant directional change, whereas the maternally donated nuclear genome (A genome) did not. These results are consistent with our previous study showing that the AB nuclear genome of the natural B. juncea polyploid, which has the A cytoplasm, is more similar to B. rapa (A genome) than to B. nigra (B genome) (14). Interpretation of results from the BA polyploid was hindered by the highly variable rates of genome changes among F5 progenies; however, the paternally donated nuclear genome (A genome) also showed significant directional change in a subset of rapidly changing F5 plants.

Significant directional changes were not observed for the AC and CA polyploids (Fig. 3, AC and CA). Thus, changes in these polyploids seemed to cause only random fluctuation of genome compositions. Because the A and C cytoplasmic genomes are more closely related than the A and B cytoplasmic genomes (14), the absence of directional changes and overall lower frequencies of genome change in the AC and CA vs. AB and BA polyploids may be due, in part, to higher levels of cytoplasmic-nuclear genome compatibility in the AC and CA polyploids.

Implications of Rapid Genome Change for Polyploid Evolution. Using synthetic polyploids, we have demonstrated that extensive genome change can occur in the early generations of Brassica polyploids. Genetic diversity accumulated among self-fertilized progenies, even when the starting materials were completely homozygous. We do not know whether these types of changes or this extent of change has occurred in the early generations of natural Brassica or other polyploid species. However, our molecular results, when combined with variation in fertility and other morphological traits observed in our synthetic polyploids and in previous studies (26, 27), suggest that rapid genome change in newly formed polyploids can produce many novel genotypes that would provide new genetic variation for selection. Thus, rapid genome change could accelerate evolutionary processes among progenies of newly formed polyploids, and this may, in part, account for the success and diversification of many ancient polyploid lineages in both plants and animals.

26. Olson, G. (1960) Species crosses within the genus Brassica I. Artificial  Brassica juncea cross. Hereditas 46, 171-223.
27. Olson, G. (1960) Species crosses within the genus Brassica II. Artificial Brassica napus L. Hereditas 46, 351-386.

Chromosome Changes in Evolution