The immediate metabolomic effects of whole-genome duplication in the greater duckweed, Spirodela polyrhiza.

PREMISE: In plants, whole-genome duplication (WGD) is a common mutation with profound evolutionary potential. Given the costs associated with a superfluous genome copy, polyploid establishment is enigmatic. However, in the right environment, immediate phenotypic changes following WGD can facilitate establishment. Metabolite abundances are the direct output of the cell's regulatory network and determine much of the impact of environmental and genetic change on the phenotype. While it is well known that an increase in the bulk amount of genetic material can increase cell size, the impact of gene dosage multiplication on the metabolome remains largely unknown. METHODS: We used untargeted metabolomics on four genetically distinct diploid-neoautotetraploid pairs of the greater duckweed, Spirodela polyrhiza, to investigate how WGD affects metabolite abundances per cell and per biomass. RESULTS: Autopolyploidy increased metabolite levels per cell, but the response of individual metabolites varied considerably. However, the impact on metabolite level per biomass was restricted because the increased cell size reduced the metabolite concentration per cell. Nevertheless, we detected both quantitative and qualitative effects of WGD on the metabolome. Many effects were strain-specific, but some were shared by all four strains. CONCLUSIONS: The nature and impact of metabolic changes after WGD depended strongly on the genotype. Dosage effects have the potential to alter the plant metabolome qualitatively and quantitatively, but were largely balanced out by the reduction in metabolite concentration due to an increase in cell size in this species.

Interspecific transfer of genetic information through polyploid bridges.

Hybridization blurs species boundaries and leads to intertwined lineages resulting in reticulate evolution. Polyploidy, the outcome of whole genome duplication (WGD), has more recently been implicated in promoting and facilitating hybridization between polyploid species, potentially leading to adaptive introgression. However, because polyploid lineages are usually ephemeral states in the evolutionary history of life it is unclear whether WGD-potentiated hybridization has any appreciable effect on their diploid counterparts. Here, we develop a model of cytotype dynamics within mixed-ploidy populations to demonstrate that polyploidy can in fact serve as a bridge for gene flow between diploid lineages, where introgression is fully or partially hampered by the species barrier. Polyploid bridges emerge in the presence of triploid organisms, which despite critically low levels of fitness, can still allow the transfer of alleles between diploid states of independently evolving mixed-ploidy species. Notably, while marked genetic divergence prevents polyploid-mediated interspecific gene flow, we show that increased recombination rates can offset these evolutionary constraints, allowing a more efficient sorting of alleles at higher-ploidy levels before introgression into diploid gene pools. Additionally, we derive an analytical approximation for the rate of gene flow at the tetraploid level necessary to supersede introgression between diploids with nonzero introgression rates, which is especially relevant for plant species complexes, where interspecific gene flow is ubiquitous. Altogether, our results illustrate the potential impact of polyploid bridges on the (re)distribution of genetic material across ecological communities during evolution, representing a potential force behind reticulation.

The duplication of genomes and genetic networks and its potential for evolutionary adaptation and survival during environmental turmoil.

The importance of whole-genome duplication (WGD) for evolution is controversial. Whereas some view WGD mainly as detrimental and an evolutionary dead end, there is growing evidence that polyploidization can help overcome environmental change, stressful conditions, or periods of extinction. However, despite much research, the mechanistic underpinnings of why and how polyploids might be able to outcompete or outlive nonpolyploids at times of environmental upheaval remain elusive, especially for autopolyploids, in which heterosis effects are limited. On the longer term, WGD might increase both mutational and environmental robustness due to redundancy and increased genetic variation, but on the short-or even immediate-term, selective advantages of WGDs are harder to explain. Here, by duplicating artificially generated Gene Regulatory Networks (GRNs), we show that duplicated GRNs-and thus duplicated genomes-show higher signal output variation than nonduplicated GRNs. This increased variation leads to niche expansion and can provide polyploid populations with substantial advantages to survive environmental turmoil. In contrast, under stable environments, GRNs might be maladaptive to changes, a phenomenon that is exacerbated in duplicated GRNs. We believe that these results provide insights into how genome duplication and (auto)polyploidy might help organisms to adapt quickly to novel conditions and to survive ecological uproar or even cataclysmic events.

The immediate effects of polyploidization of Spirodela polyrhiza change in a strain-specific way along environmental gradients.

The immediate effects of plant polyploidization are well characterized and it is generally accepted that these morphological, physiological, developmental, and phenological changes contribute to polyploid establishment. Studies on the environmental dependence of the immediate effects of whole-genome duplication (WGD) are, however, scarce but suggest that these immediate effects are altered by stressful conditions. As polyploid establishment seems to be associated with environmental disturbance, the relationship between ploidy-induced phenotypical changes and environmental conditions is highly relevant. Here, we use a common garden experiment on the greater duckweed Spirodela polyrhiza to test whether the immediate effects of WGD can facilitate the establishment of tetraploid duckweed along gradients of two environmental stressors. Because successful polyploid establishment often depends on recurrent polyploidization events, we include four genetically diverse strains and assess whether these immediate effects are strain-specific. We find evidence that WGD can indeed confer a fitness advantage under stressful conditions and that the environment affects ploidy-induced changes in fitness and trait reaction norms in a strain-specific way.

Studying Whole-Genome Duplication Using Experimental Evolution of Chlamydomonas.

In this chapter, we present the use of Chlamydomonas reinhardtii in experiments designed to study the evolutionary impacts of whole genome duplication. We shortly introduce the algal species and depict why it is an excellent model for experimental evolution. Subsequently, we discuss the most relevant steps and methods in the design of a ploidy-related Chlamydomonas experiment. These steps include strain selection, ploidy determination, different methods of making diplo- and polyploid Chlamydomonas cells, replication, culturing conditions, preservation, and the ways to quantify phenotypic and genotypic change.

Studying Whole-Genome Duplication Using Experimental Evolution of Spirodela polyrhiza.

In this chapter, we present the use of Spirodela polyrhiza in experiments designed to study the evolutionary impact of whole-genome duplication (WGD). We shortly introduce this duckweed species and explain why it is a suitable model for experimental evolution. Subsequently, we discuss the most relevant steps and methods in the design of a ploidy-related duckweed experiment. These steps include strain selection, ploidy determination, different methods of making polyploid duckweeds, replication, culturing conditions, preservation, and the ways to quantify phenotypic and transcriptomic change.