Genetic Consequences of Polyploidy and Hybridization

Schematic of the independent, recurrent origins of the allotetraploid fern Polypodium hesperium. Polypodium hesperium formed by hybridization, concomitant with genome doubling (yellow stars), between the diploid species P. amorphum (A) and P. glycyrrhiza (G) at least two times in the last 1.2 mya. Ha represents individuals of P. hesperium with P. amorphum as their maternal parent, whereas Hg represents individuals of P. hesperium with P. glycyrrhiza as their maternal parent.  A. Phyloreticulogram of P. hesperium and its diploid progenitors represented by herbarium vouchers. B. Phyloreticulogram of P. hesperium and its diploid progenitors represented by chromosomes. Homeologs refer to gene copies or chromosomes derived from different progenitor species. At time of formation, P. hesperium has a full set of homeologs from both P. amorphum and P. glycyrrhiza. 

Schematic of the independent, recurrent origins of the allotetraploid fern Polypodium hesperium. Polypodium hesperium formed by hybridization, concomitant with genome doubling (yellow stars), between the diploid species P. amorphum (A) and P. glycyrrhiza (G) at least two times in the last 1.2 mya. Ha represents individuals of P. hesperium with P. amorphum as their maternal parent, whereas Hg represents individuals of P. hesperium with P. glycyrrhiza as their maternal parent.  A. Phyloreticulogram of P. hesperium and its diploid progenitors represented by herbarium vouchers. B. Phyloreticulogram of P. hesperium and its diploid progenitors represented by chromosomes. Homeologs refer to gene copies or chromosomes derived from different progenitor species. At time of formation, P. hesperium has a full set of homeologs from both P. amorphum and P. glycyrrhiza. 

Increasingly, it is recognized that many, if not most, allopolyploid species form recurrently from distinct hybridization events among different populations of the same progenitor species and comprise multiple, independently-formed lineages. At the time of formation independently-formed lineages contribute to the genetic diversity of an allopolyploid species by incorporating different parental genotypes, but the influence of recurrent origins on genetic and phenotypic variation in subsequent generations is less apparent.

As a first effort towards understanding how ferns utilize the genetic diversity imparted by allopolyploidy and recurrent origins, I am working with Dr. Joshua Der (California State University, Fullerton) to assess patterns of gene expression between the two independent and reciprocally-formed derived lineages of allopolyploid fern Polypodium hesperium (see Research section on the Polypodium vulgare complex). Specifically, we ask the following questions: (1) Do the independently-formed lineages of P. hesperium exhibit similar patterns of gene expression levels relative to their diploid progenitor species? (2) Do independently-formed lineages of P. hesperium exhibit similar patterns of homeolog-specific gene expression? (3) Because this is the first study to focus on gene expression patterns in ferns, do we find that P. hesperium exhibits expression level dominance and homeolog-bias that is comparable to what is being found in other (non-fern) allopolyploid lineages?

This work utilizes a biologically-replicated common garden design and Illumina RNA-Seq technology. Our findings to date indicate that both independently-formed lineages of P. hesperium have broadly similar patterns of gene expression levels and homeolog-specific expression at the transcriptome level, but substantial variation at the level of individual genes. This suggests that the expression patterns resulting from the union of divergent parental genomes and regulatory systems are largely due to non-stochastic processes, but that multiple, independent origins may impart significant phenotypic variation to an allopolyploid taxon. We detect a significant amount of unbalanced expression level dominance (expression levels mirroring that of only one parent) and homeolog expression bias favoring a particular diploid progenitor. Expression level dominance and homeolog expression bias have been widely reported in studies of allopolyploid angiosperms. Detection of these phenomena in ferns suggest that they may be a pervasive consequence of allopolyploidization in land plants.

  Upper: Simplified diagram of the methods used to estimate and compare gene expression levels in the independently-formed lineages of Polypodium hesperium (Ha and Hg) relative to the diploid progenitor species P. amorphum (A) and P. glycyrrhiza (G). Examples differential expression patterns (far right) are modified from Rapp et al. 2009.  Lower: Simplified diagram of the methods used to estimate homeolog expression ratios expressed by the independently-formed lineages of P. hesperium (Ha and Hg). 

 

Upper: Simplified diagram of the methods used to estimate and compare gene expression levels in the independently-formed lineages of Polypodium hesperium (Ha and Hg) relative to the diploid progenitor species P. amorphum (A) and P. glycyrrhiza (G). Examples differential expression patterns (far right) are modified from Rapp et al. 2009.  Lower: Simplified diagram of the methods used to estimate homeolog expression ratios expressed by the independently-formed lineages of P. hesperium (Ha and Hg).