The immediate effects of polyploidization of Spirodela polyrhiza change in a strain-specific way along environmental gradients. Issue 1 (31st January 2023)

• Record Type: Journal Article
• Authors: Bafort, Quinten; Wu, Tian; Natran, Annelore; De Clerck, Olivier; Van de Peer, Yves
• Is Part Of: Evolution letters. Volume 7:Issue 1(2023)
• Page Start: 37
• Page End: 47
• Publication Date: 2023-01-31
• Subjects: polyploidy -- whole-genome duplication -- Spirodela polyrhiza; Evolution (Biology) -- Periodicals; Evolution (Biology); Biological Evolution; Electronic journals; Fulltext; Internet Resources; Periodicals; Periodicals; Periodical; 576.8
• DOI: 10.1093/evlett/qrac003
• Languages: English
• ISSNs: 2056-3744

Abstract

Abstract: 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. Lay Summary: Polyploidization, resulting from genome duplication and/or merger, is a major force in plant evolution. Despite high numbers of polyploid species and intraspecific karyotypical variation, the challenges faced by a newly formed polyploid are multifarious. Higher resource requirements, difficulties finding compatible polyploid mates, genomic instability, and competition with their well-adapted diploid ancestors all impede establishment. Nevertheless, while many polyploids are short-lived, some of them manage to survive, reproduce, and even thrive. The basis for this inequality amongst polyploids remains largely unknown. Part of the key to polyploid success must lie in the immediate effects of genome doubling. Genome size is correlated with cell size and as such, genome duplication triggers a cell size increase and a whole battery of cascading effects on the phenotype. Although these immediate effects are well characterized, variation between and even within species is considerable. Using a common garden experiment in which we exposed four genetically different diploid-tetraploid pairs of the greater duckweed Spirodela polyrhiza to stress gradients, we hope to improve our understanding of what determines the fate of neopolyploid plants. Here, we show that although the immediate effects of WGD can result in a decreased fitness of the tetraploid in the prevailing environment, they can confer a fitness advantage in another and that ploidy-induced changes in trait plasticity and fitness homeostasis are strain-specific. Consequently, we show that the fate of neopolyploid plants depends at least partially on the interplay of the identity of the individuals present in the polyploid population (the genotypes), and the environmental conditions they face. Our findings support the idea that stressful environments can facilitate polyploid establishment and that recurrent polyploidization can help polyploid establishment through variation in the outcomes of independent polyploidization events. Whenever possible, future studies on nucleotypic effects should include diverse ecotypes and environmental conditions in their designs.