Genetic and epigenetic consequences of recent hybridization and polyploidy in Spartina (Poaceae)

Abstract

To study the consequences of hybridization and genome duplication on polyploid genome evolution and adaptation, we used independently formed hybrids (Spartina x townsendii and Spartina x neyrautii) that originated from natural crosses between Spartina alterniflora, an American introduced species, and the European native Spartina maritima. The hybrid from England, S. x townsendii, gave rise to the invasive allopolyploid, salt-marsh species, Spartina anglica. Recent studies indicated that allopolyploid speciation may be associated with rapid genetic and epigenetic changes. To assess this in Spartina, we performed AFLP (amplified fragment length polymorphism) and MSAP (methylation sensitive amplification polymorphism) on young hybrids and the allopolyploid. By comparing the subgenomes in the hybrids and the allopolyploid to the parental species, we inferred structural changes that arose repeatedly in the two independently formed hybrids. Surprisingly, 30% of the parental methylation patterns are altered in the hybrids and the allopolyploid. This high level of epigenetic regulation might explain the morphological plasticity of Spartina anglica and its larger ecological amplitude. Hybridization rather than genome doubling seems to have triggered most of the methylation changes observed in Spartina anglica.

Mechanisms of genomic rearrangements and gene expression changes in plant polyploids

“…Sunfish is methylated in the autotetraploid parent, but demethylated and reactivated in the allotetraploids, suggesting that allopolyploidization provokes perturbation of genomic structure and chromatin remodeling, giving rise to the reactivation and silencing of transposons (44) and proteincoding genes. (43,70) It is conceivable that changes in DNA methylation detected in recent Spartina (60) polyploids and synthetic Arabidopsis (44) allotetraploids are associated with gene expression changes and phenotypic variation. Notably, synthetic Arabidopsis allotetraploids are more sensitive than their parents to treatments of aza-dC, (44) a chemical inhibitor for DNA methylation, indicating that DNA methylation and other chromatin modifications become sensitized in the allotetraploids, probably due to remodeling activities during allopolyploid formation.…”

“…(59) Similarly, genomic changes in Spartina polyploids occur at a very low frequency. (60) The data suggest that, compared to Brassica and wheat, cotton and Spartina have a high-level of tolerance for genome doubling and interspecific hybridization. Hence, they may represent just one of the diverse array of molecular evolutionary phenomena observed in polyploids in general.…”

Non-additive gene regulation in a citrus allotetraploid somatic hybrid between C. reticulata Blanco and C. limon (L.) Burm

“…Polyploid plants often produce new phenotypes, exceeding the range of variability existing in the diploid gene pool (Osborn et al, 2003) and it is generally considered that allopolyploid plants confer an evolutionary advantage over their progenitor (Salmon et al, 2005;Wendel and Doyle, 2005;Chen, 2007). Genomic reorganization, independent evolution and subfunctionalization of duplicated genes (Lynch and Force, 2000;Adams et al, 2003), are important elements of the evolution of polyploid populations.…”

Epigenetic, transposon and small RNA determinants of hybrid dysfunctions

“…Dobzhansky-Muller's model of genetic incompatibilities has long provided a useful theoretical framework for speciation genetics, but it is becoming increasingly clear that the model is too general to generate more specific predictions regarding the genetic mechanisms involved. Accumulating evidence indicates that the merging of two distinct genomes typically sets in motion extensive modifications of the genome and transcriptome, creating cascades of novel gene expression patterns (Michalak and Noor, 2003;Wu et al, 2003;Ranz et al, 2004;Auger et al, 2005;Hegarty et al, 2006), regulatory interactions and new phenotypic variation (Riddle and Birchler, 2003;Adams and Wendel, 2005a, b), chromosomal rearrangements (Rieseberg et al, 2003;Metcalfe et al, 2007), transposable element mobilization (Liu and Wendel, 2000;Shan et al, 2005;Ungerer et al, 2006), miRNA deficiency (Michalak and Malone, 2008) and DNA methylation changes (Waugh O'Neill et al, 1998;Vrana et al, 2000;Salmon et al 2005;Josefsson et al, 2006).…”