Homeolog loss and expression changes in natural populations of the recently and repeatedly formed allotetraploid Tragopogon mirus (Asteraceae)

Abstract

Background

Although polyploidy has long been recognized as a major force in the evolution of plants, most of what we know about the genetic consequences of polyploidy comes from the study of crops and model systems. Furthermore, although many polyploid species have formed repeatedly, patterns of genome evolution and gene expression are largely unknown for natural polyploid populations of independent origin. We therefore examined patterns of loss and expression in duplicate gene pairs (homeologs) in multiple individuals from seven natural populations of independent origin of Tragopogon mirus (Asteraceae), an allopolyploid that formed repeatedly within the last 80 years from the diploids T. dubius and T. porrifolius.

Results

Using cDNA-AFLPs, we found differential band patterns that could be attributable to gene silencing, novel expression, and/or maternal/paternal effects between T. mirus and its diploid parents. Subsequent cleaved amplified polymorphic sequence (CAPS) analyses of genomic DNA and cDNA revealed that 20 of the 30 genes identified through cDNA-AFLP analysis showed additivity, whereas nine of the 30 exhibited the loss of one parental homeolog in at least one individual. Homeolog loss (versus loss of a restriction site) was confirmed via sequencing. The remaining gene ( ADENINE-DNA GLYCOSYLASE) showed ambiguous patterns in T. mirus because of polymorphism in the diploid parent T. dubius. Most (63.6%) of the homeolog loss events were of the T. dubius parental copy. Two genes, NUCLEAR RIBOSOMAL DNA and GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE, showed differential expression of the parental homeologs, with the T. dubius copy silenced in some individuals of T. mirus.

Conclusions

Genomic and cDNA CAPS analyses indicated that plants representing multiple populations of this young natural allopolyploid have experienced frequent and preferential elimination of homeologous loci. Comparable analyses of synthetic F ₁ hybrids showed only additivity. These results suggest that loss of homeologs and changes in gene expression are not the immediate result of hybridization, but are processes that occur following polyploidization, occurring during the early (<40) generations of the young polyploid. Both T. mirus and a second recently formed allopolyploid, T. miscellus, exhibit more homeolog losses than gene silencing events. Furthermore, both allotetraploids undergo biased loss of homeologs contributed by their shared diploid parent, T. dubius. Further studies are required to assess whether the results for the 30 genes so far examined are representative of the entire genome.