Altered gene expression and ecological divergence in sibling allopolyploids of Dactylorhiza (Orchidaceae)

Abstract

BackgroundHybridization and polyploidy are potent forces that have regularly stimulated plant evolution and adaptation. Dactylorhiza majalis s.s., D. traunsteineri s.l. and D. ebudensis are three allopolyploid species of a polyploid complex formed through unidirectional (and, in the first two cases, recurrent) hybridization between the widespread diploids D. fuchsii and D. incarnata. Differing considerably in geographical extent and ecological tolerance, the three allopolyploids together provide a useful system to explore genomic responses to allopolyploidization and reveal their role in adaptation to contrasting environments.ResultsAnalyses of cDNA-AFLPs show a significant increase in the range of gene expression of these allopolyploid lineages, demonstrating higher potential for phenotypic plasticity than is shown by either parent. Moreover, allopolyploid individuals express significantly more gene variants (including novel alleles) than their parents, providing clear evidence of increased biological complexity following allopolyploidization. More genetic mutations seem to have accumulated in the older D. majalis compared with the younger D. traunsteineri since their respective formation.ConclusionsMultiple origins of the polyploids contribute to differential patterns of gene expression with a distinct geographic structure. However, several transcripts conserved within each allopolyploid taxon differ between taxa, indicating that habitat preferences shape similar expression patterns in these independently formed tetraploids. Statistical signals separate several transcripts - some of them novel in allopolyploids - that appear correlated with adaptive traits and seem to play a role favouring the persistence of individuals in their native environments. In addition to stabilizing the allopolyploid genome, genetic and epigenetic alterations are key determinants of adaptive success of the new polyploid species after recurrent allopolyploidization events, potentially triggering reproductive isolation between the resulting lineages.

Adaptive sequence evolution is driven by biotic stress in a pair of orchid species (Dactylorhiza) with distinct ecological optima

“…Elevated evolution of further protein‐coding sequences potentially related to abiotic‐imposed selection in D. incarnata includes a SUGAR CARRIER C homolog, potentially involved in hexose transmembrane transport likely linked to hypoxia (Gharbi, Ricard, Smiti, Bizid, & Brouquisse, 2009) that the roots of D. incarnata may suffer, given the high soil moisture to which this species adapted (Paun et al., 2011). Preferences for distinct soil chemistry (i.e., organic vs. mineral soil typically preferred by D. incarnata and D. fuchsii , respectively) and soil pH may be linked to elevated rates of evolution of an INORGANIC PHOSPHATE TRANSPORTER 1‐8 homolog in D. incarnata and of POTASSIUM TRANSPORTER 9 in D. fuchsii .…”

“…The two orchid species broadly share geographical distribution (northern and central Europe and Western Asia, Tutin et al., 1980) and often grow in proximity. However, they have clearly distinct morphologies and also differ in their ecological preference (Paun et al., 2011). Dactylorhiza fuchsii inhabits grasslands, open woods and disturbed habitats such as road margins, whereas D. incarnata prefers marshes, fens and bog habitats.…”

Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous–Paleogene boundary

“…Newly formed polyploids frequently display profound morphological and physiological differences (te Beest et al 2012), and may have a higher capacity for phenotypic plasticity (Paun et al 2011;Hahn et al 2012) founder population, increased phenotypic plasticity most likely allowed polyploid Ceratocapnos claviculata species to recolonize northern European habitats after the last glacial maximum (Voss et al 2012). Similarly, polyploid Centaurea stoebe species most likely displayed ''pre-adaptation'' for some traits that predisposed them for colonization success upon introduction in North America ;120 yr ago (Henery et al 2010).…”

Ecological and genetic factors linked to contrasting genome dynamics in seed plants

“…Furthermore, epigenetically controlled developmental or physiological plasticity reported in angiosperms may enable the establishment of small viable populations in different ecological settings. Certainly, different epigenetic profiles are observed between populations of orchids and it can be envisaged that over time drift and selection will result in their divergence (Paun et al, 2010(Paun et al, , 2011.…”