(NAS Colloquium) Variation and Evolution in Plants and Microorganisms: Towards a New Synthesis: 50 Years after Stebbins

The following HTML text is provided to enhance online readability. Many aspects of typography translate only awkwardly to HTML. Please use the page image as the authoritative form to ensure accuracy.

COLLOQUIUM ON Variation and Evolution in Plants and Microorganisms: Toward a New Synthesis: 50 Years after Stebbins

across the angiosperms is partially consistent with Stebbins' hypothesis. Although the high chromosome numbers of the basal angiosperm groups make it difficult to infer base chromosome numbers for those groups of angiosperms and therefore for angiosperms as a whole, our reconstructions show an ancestral number of x = 8 for the eudicots (D.E.S., unpublished data), that is, the large clade that makes up 75% of angiosperm species. Identifying the ancestral number for all angiosperms will require teasing apart the base numbers of the ancient polyploid groups and will require further work.

Most, if not all, angiosperms may have experienced one or more cycles of genome doubling (6), and these hypotheses of ancient polyploidy have several implications for the genetics, genomics, and evolutionary biology of these plants. First, if they are indeed polyploids, then these plants should exhibit extra copies of their genes above the level that one would expect for diploid plants (10,11). Analyses of enzyme expression indicate that multiple enzymes are indeed expressed in putatively paleopolyploid angiosperm families, such as those listed in Table 3 (59); issues of the regulation of duplicated genes are discussed by Wendel (6). Second, some copies of these multiple genes might be expected to be silenced, particularly in the more ancient families (see Gene Silencing below). Third, reorganization of the original polyploid genome might have led to a novel genomic arrangement and perhaps to novel phenotypes. Finally, given that all members of a family have chromosome numbers that are multiples of a single lower number, it appears that, after polyploidization, diversification continued at the new polyploid level, with subsequent episodes of polyploidy superimposed on this initial polyploid level. This pattern of divergent speciation at the polyploid level contradicts the view of polyploids as evolutionary dead-ends.

Homosporous Pteridophytes. Homosporous pteridophytes are those ferns (including Psilotum and Tmesipteris; refs.60 –62), lycophytes, and Equisetum with a homosporous life cycle; all of these groups are the descendants of ancient plant lineages that extend back to the Devonian Period (63). The mean gametic chromosome number for homosporous pteridophytes is n = 57; for angiosperms, it is n = 16 (64). Despite their high chromosome numbers, however, homosporous pteridophytes exhibit diploid gene expression at isozyme loci (65 –68). At least two possible explanations can explain this paradox of high chromosome numbers and genetic diploidy. First, these plants are ancient polyploids that have undergone extensive gene silencing to produce genetic diploids, and second, they may have achieved high chromosome numbers through another mechanism, such as chromosomal fission.

Gene Silencing. Genes duplicated through polyploidy have several possible fates: retention of both copies as functional genes, acquisition of new function by one copy, and gene silencing (6). Several models of genome evolution, in which a polyploid genome gradually will undergo gene silencing and return to a diploid condition, have been presented (69,70). Unfortunately, little empirical evidence is available to support or to refute these models.

Potential examples occur in the homosporous pteridophytes. Data for the ferns Polystichum munitum (n = 41) and Ceratopteris richardii (n = 39) may address these alternatives. Pichersky et al. (71) studied the genes for the chlorophyll a/b binding proteins in P. munitum. These proteins are important in photosynthesis and are encoded by a small multigene family (71). P. munitum exhibits diploid isozyme expression (22,35,72). If this species is of ancient polyploid origin but has since undergone substantial gene silencing, then pseudogenes should be detectable in the genome. Five clones of the CAB genes were analyzed by Pichersky et al. Three of the five clones were structurally nonfunctional, a fourth clone had a structurally intact sequence but was nonfunctional at the sequence level, and a fifth clone was a functional sequence. Possible explanations for these results (71) are (i) amplification of nonfunctional sequences in the genome of P. munitum, regardless of the ploidy of P. munitum, (ii) P. munitum is diploid with a large number of mutant CAB genes, and (iii) P. munitum is polyploid, with silencing of multiple genes that are present because of ancient polyploidy. In C. richardii, cDNA clones hybridized to multiple fragments on genomic DNA blots, suggesting that 50% or more of these expressed sequences were present in multiple copies in this fern genome (73). In contrast, a similar experiment with A. thaliana detected only 15% duplicated fragments (74). Further characterization of the hybridizing fragments of the genome is necessary to document that they are in fact duplicated sequences. However, this evidence for multiple hybridizing fragments in C. richardii, along with the CAB gene data for P. munitum, suggests that the genomes of homosporous ferns may in fact be anciently polyploid.

Gene silencing remains an underinvestigated area of polyploid research. If it occurs as described in models of wholesale diploidization of the polyploid genome (70), what are the mechanisms and at what rate does such silencing occur? Or does silencing occur gradually, essentially one locus at a time? Many unanswered questions remain.

Conclusions

Leitch and Bennett (48) have suggested that the evolutionary potential of a polyploid depends on a number of factors associated with the formation of the polyploid and with genetic divergence between the parents; unfortunately, the factors involved in the origin and establishment of polyploids in nature are largely unknown (75). The success of a polyploid may depend, in part, on the parental origin of particular DNA sequences—is the sequence maternal or paternal and does it interact favorably with the organellar genomes? The type of sequence under study also may be important: is it coding or noncoding DNA, is it telomeric or centric in origin, and is it located near heterochromatin? Finally, what is the level of genetic differentiation between the parents?

Although unreduced gamete production and even polyploid formation may be quite common in many groups of plants (75), there are many obstacles to establishment of a polyploid population. Minority cytotype exclusion (76 –78) may be particularly important in newly formed outcrossing polyploids where there are few potential mates unless there is substantial assortative mating (79); when only one or a few polyploid individuals emerge within a population of diploids, outcrossing polyploid individuals may spend most of their gametes in sterile or partially sterile matings with their diploid parents. The apparent success of polyploids is biased toward those species that have overcome the barrier(s) to establishment, and this success may ultimately derive from a number of the genetic attributes of the polyploids. Polyploids have increased heterozygosity, an attribute that may be beneficial (80,81). Polyploids also harbor higher levels of genetic and genomic diversity than was anticipated, with recurrent formation from genetically divergent diploid parents and possibly genome rearrangements contributing genetic diversity. This genetic diversity results in greater biochemical diversity, which also may be beneficial to the polyploid (82). Finally, these genetic attributes may have ecological consequences. For example, if polyploids have lower inbreeding depression and are more highly selfing, they may be better colonizers, explaining the prevalence of polyploids on the list of the world's worst weeds. Polyploids may have broader ecological amplitudes than do their diploid progenitors because of their increased genetic and biochemical diversity (82). Polyploids may experience new interactions with other species, such as pollinators (83,84).

Free Resources

Related Titles