Evolution and expression of homeologous loci in Tragopogon miscellus (Asteraceae), a recent and reciprocally formed allopolyploid

Abstract

On both recent and ancient time scales, polyploidy (genome doubling) has been a significant evolutionary force in plants. Here, we examined multiple individuals from reciprocally formed populations of Tragopogon miscellus, an allotetraploid that formed repeatedly within the last 80 years from the diploids T. dubius and T. pratensis. Using cDNA-AFLPs followed by genomic and cDNA cleaved amplified polymorphic sequence (CAPS) analyses, we found differences in the evolution and expression of homeologous loci in T. miscellus. Fragment variation within T. miscellus, possibly attributable to reciprocal formation, comprised 0.6% of the cDNA-AFLP bands. Genomic and cDNA CAPS analyses of 10 candidate genes revealed that only one "transcript-derived fragment" (TDF44) showed differential expression of parental homeologs in T. miscellus; the T. pratensis homeolog was preferentially expressed by most polyploids in both populations. Most of the cDNA-AFLP polymorphisms apparently resulted from loss of parental fragments in the polyploids. Importantly, changes at the genomic level have occurred stochastically among individuals within the independently formed populations. Synthetic F(1) hybrids between putative diploid progenitors are additive of their parental genomes, suggesting that polyploidization rather than hybridization induces genomic changes in Tragopogon.

Figure 1.—

Origins of the New World Tragopogon allotetraploids. (A) Following the introduction of three diploid species (T. dubius, T. porrifolius, and T. pratensis) to the northwestern United States in the early 1900s, two polyploid species (T. miscellus and T. mirus) formed recurrently. The direction of the arrow indicates the maternal progenitor. (B) Populations of T. miscellus that differ in maternal parentage can be readily distinguished by their inflorescence morphology. T. pratensis is the maternal parent of the short-liguled form, and T. dubius is the maternal parent of the long-liguled form of T. miscellus.

Figure 2.—

cDNA–AFLP display of gene expression in Tragopogon allotetraploids and their diploid progenitors. T. dubius (Pullman, 2×), lanes 1–6; T. miscellus (Moscow, 4×), lanes 7–12; T. miscellus (Pullman, 4×), lanes 13–18; T. pratensis (Moscow, 2×), lanes 19–24. Arrows indicate examples of polymorphic fragments that were examined with genomic and cDNA CAPS analysis. The primer combination used was EcoRI–AA/MseI–CTT.

Figure 3.—

Genomic and cDNA CAPS analyses for 10 candidate genes in individuals of allotetraploid T. miscellus from reciprocally formed populations. Arrows indicate the parental origin of the homeolog retained or expressed in the allopolyploid individual when one parental copy was missing.

Figure 4.—

Genomic CAPS analyses for two sets of Tragopogon F₁ hybrids and their progenitors. Tp′, T. pratensis (Spangle, 2609-28); Td′, T. dubius (Spokane, 2615-22); Tp′′, T. pratensis (Moscow, 2608-11); Td′′, T. dubius (Pullman, 2613-41). For both sets of hybrids, T. pratensis was the maternal parent and T. dubius the paternal parent.