Autopolyploidy differentially influences body size in plants, but facilitates enhanced accumulation of secondary metabolites, causing increased cytosine methylation

Abstract

SUMMARYWhole genome duplication leads to autopolyploidy and brings about an increase in cell size, concentration of secondary metabolites and enhanced cytosine methylation. The increased cell size offers a positive advantage to polyploids for cell-surface-related activities, but there is a differential response to change in body size across species and taxonomic groups. Although polyploidy has been very extensively studied, having genetic, ecological and evolutionary implications, there is no report that underscores the significance of native secondary metabolites vis-à -vis body size with ploidy change. To address this problem we targeted unique diploid-autotetraploid paired sets of eight diverse clones of six species of Cymbopogon -a species complex of aromatic grasses that accumulate qualitatively different monoterpene essential oils (secondary metabolite) in their vegetative biomass. Based on the qualitative composition of essential oils and the plant body size relationship between the diploid versus autotetraploid paired sets, we show that polyploidy brings about enhanced accumulation of secondary metabolites in all cases, but exerts differential effects on body size in various species. It is observed that the accumulation of alcohol-type metabolites (e.g. geraniol) does not inhibit increase in body size with ploidy change from 2· to 4· (r = 0.854, P < 0.01), but aldehyde-type metabolites (e.g. citral) appear to drastically impede body development (r = )0.895). Such a differential response may be correlated to the metabolic steps involved in the synthesis of essential oil components. When changed to tetraploidy, the progenitor diploids requiring longer metabolic steps in production of their secondary metabolites are stressed, and those having shorter metabolite routes better utilize their resources for growth and vigour. In situ immunodetection of 5-methylcytosine sites reveals enhanced DNA methylation in autopolyploids. It is underpinned that the qualitative composition of secondary metabolites found in the vegetative biomass of the progenitor diploid has a decisive bearing on the body size of the derived autotetraploids and brings about an enhancement in genome-wide cytosine methylation.

Autotetraploid rice methylome analysis reveals methylation variation of transposable elements and their effects on gene expression

“…Ploidy-induced DNA hypermethylation changes have been reported in Eragrostis curvula (54) and Cymbopogon spp. (17). In contrast, DNA methylation sites were found to be comparable between diploids and autotetraploids in Paspalum sp.…”

“…Biologists have long sought to understand how natural selection enabled neopolyploids to overcome early challenges. Many autopolyploidy systems have been developed for this purpose, such as Arabidopsis (11)(12)(13), potato (14), Elymus elongatus (15), Paspalum (16), and Cymbopogon (17). However, further investigations are still needed to examine the scope and scale of neopolyploids' responses to WGDs.…”

Genetic and Epigenetic Aspects of Polyploid Evolution in Plants

“…Over the past 2 decades, genomic, epigenetic and cytogenetic analyses have repeatedly validated McClintock's predictions in many allopolyploid systems [for some recent reviews see Hufton and Panopoulou, 2009;Jackson and Chen, 2010;Mayfield et al, 2011;De Smet and Van de Peer, 2012;Heslop-Harrison, 2012;Soltis and Soltis, 2012]. Specifically, polyploidization has been associated with sequence loss [Shaked et al, 2001;Ozkan et al, 2003;Han et al, 2005;Tate et al, 2009], changes in epigenetic marks, such as cytosine methylation [Shaked et al, 2001;Madlung et al, 2005;Lavania et al, 2012], the activation of transposons [Kashkush et al, 2003;Madlung et al, 2005;Chen et al, 2008;Kraitshtein et al, 2010;Petit et al, 2010;Hegarty et al, 2011], and recombination between homoeologous chromosomes [Gaeta and Pires, 2010;Salmon et al, 2010;Szadkowski et al, 2010].…”

Multifoliate Leaf Formation in Induced Tetraploids of <i>Trifolium alexandrinum</i> L.

“…In unique diploid-autotetraploid paired sets of eight diverse clones of six species of Cymbopogon, it has been reported that polyploidy brings about enhanced accumulation of secondary metabolites in all cases, but exerts differential effects on body size in various species. When changed to tetraploidy, the progenitor diploids requiring longer metabolic steps in production of their secondary metabolites are stressed, and those having shorter metabolite routes better utilize their resources for growth and vigour (Lavania et al 2012).…”