The "Polyploid Hop": shifting challenges and opportunities over the evolutionary lifespan of genome duplications

The duplication of an entire genome is no small affair. Whole genome duplication (WGD) is a dramatic mutation with long-lasting effects, yet it occurs repeatedly in all eukaryotic kingdoms. Plants are particularly rich in documented WGDs, with recent and ancient polyploidization events in all major extant lineages. However, challenges immediately following WGD, such as the maintenance of stable chromosome segregation or detrimental ecological interactions with diploid progenitors, commonly do not permit establishment of nascent polyploids. Despite these immediate issues some lineages nevertheless persist and thrive. In fact, ecological modelling supports patterns of adaptive niche differentiation in polyploids, with young polyploids often invading new niches and leaving their diploid progenitors behind. In line with these observations of polyploid evolutionary success, recent work documents instant physiological consequences of WGD associated with increased dehydration stress tolerance in first-generation autotetraploids. Furthermore, population genetic theory predicts both short-and long-term benefits of polyploidy and new empirical data suggests that established polyploids may act as 'sponges' accumulating adaptive allelic diversity. In addition to their increased genetic variability, introgression with other tetraploid lineages, diploid progenitors, or even other species, further increases the available pool of genetic variants to polyploids. Despite this, the evolutionary advantages of polyploidy are still questioned, and the debate over the idea of polyploidy as an evolutionary dead-end carries on. Here we broadly synthesise the newest empirical data moving this debate forward. Altogether, evidence suggests that if early barriers are overcome, WGD can offer instantaneous fitness advantages opening the way to a transformed fitness landscape by sampling a higher diversity of alleles, including some already preadapted to their local environment. This occurs in the context of intragenomic, population genomic, and physiological modifications that can, on occasion, offer an evolutionary edge. Yet in the long run, early advantages can turn into long-term hindrances, and without ecological drivers such as novel ecological niche availability or agricultural propagation, a restabilization of the genome via diploidization will begin the cycle anew

Autopolyploidi: obzvláště slibné hříčky přírody

Autopolyploidie (znásobení celého genomu organismu) je náročná mutace. Přináší druhům, které ji prodělají, jak náročné výzvy, tak mnohé nové možnosti. Jako první se musí vypořádat s problémy, jako je ustálení nové linie v diploidní populaci rodičů, zajištění správného fungování buňky s dvojnásobným množstvím DNA a obnovení funkční mitózy a meiózy. Poté se však mohou projevit výhodné změny populační genetiky, jako je dvojnásobná efektivní velikost populace a polysomická dědičnost, které zvyšují heterozygotnost a genetickou variabilitu v nové polyploidní linii. Dále také snižují negativní působení genetického driftu a inbrední deprese. Z evolučního úhlu pohledu je patrné, že vlastnictví jednoho genomu navíc umožňuje selekci, aby působila na geny mnohem volněji. Alely si tak rychle rozdělí své dřívější funkce nebo získají funkce zcela nové. Abych lépe demonstrovala molekulární mechanismy působení selekce na populační úrovni, zvolila jsem jako modelový příklad evoluci genů pro meiózu u polyploidního druhu Arabidopsis arenosa (brukvovité, Brassicaceae). Je to jediný diploidně-autotetraploidní druh v rodě Arabidopsis, který je klíčovým rostlinným modelem. Jako takový A. arenosa umožňuje klást si obecné otázky ohledně příčin a důsledků celogenomové duplikace u rostlin. A. arenosa zůstával (na rozdíl od...Autopolyploidy, genome duplication per se, is a severe mutation which presents both great challenge and great opportunity for the species which has undergone it. First, a whole series of initial challenges has to be overcome, e.g., establishment within diploid parental population, proper functioning of the cell with doubled genetic information and restoration of proper mitosis and meiosis. The population genetic changes can become beneficial afterwards as the two times higher effective population size and polysomic inheritance increase heterozygosity and genetic variability within the new polyploid lineage. It also reduces negative impacts of genetic drift and inbreeding depression. In evolutionary context, having two genomes allows selection to be more relaxed, thus genes can quickly diversify into alleles with new function or sub-function. To better understand the molecular mechanisms of selection on a population level, I choose example of meiosis genes evolution in a polyploid Arabidopsis arenosa (Brassicaceae) species complex. This only diploid-autotetraploid member of the plant leading model genus Arabidopsis provides an ideal system for addressing general questions on the triggers and consequences of genome duplication in plants. In contrast to other members of the genus, A. arenosa remained...Katedra botanikyDepartment of BotanyPřírodovědecká fakultaFaculty of Scienc

Polyploidization increases meiotic recombination frequency in Arabidopsis

<p>Abstract</p> <p>Background</p> <p>Polyploidization is the multiplication of the whole chromosome complement and has occurred frequently in vascular plants. Maintenance of stable polyploid state over generations requires special mechanisms to control pairing and distribution of more than two homologous chromosomes during meiosis. Since a minimal number of crossover events is essential for correct chromosome segregation, we investigated whether polyploidy has an influence on the frequency of meiotic recombination.</p> <p>Results</p> <p>Using two genetically linked transgenes providing seed-specific fluorescence, we compared a high number of progeny from diploid and tetraploid <it>Arabidopsis </it>plants. We show that rates of meiotic recombination in reciprocal crosses of genetically identical diploid and autotetraploid <it>Arabidopsis </it>plants were significantly higher in tetraploids compared to diploids. Although male and female gametogenesis differ substantially in meiotic recombination frequency, both rates were equally increased in tetraploids. To investigate whether multivalent formation in autotetraploids was responsible for the increased recombination rates, we also performed corresponding experiments with allotetraploid plants showing strict bivalent pairing. We found similarly increased rates in auto- and allotetraploids, suggesting that the ploidy effect is independent of chromosome pairing configurations.</p> <p>Conclusions</p> <p>The evolutionary success of polyploid plants in nature and under domestication has been attributed to buffering of mutations and sub- and neo-functionalization of duplicated genes. Should the data described here be representative for polyploid plants, enhanced meiotic recombination, and the resulting rapid creation of genetic diversity, could have also contributed to their prevalence.</p

The role of duplications in the evolution of genomes highlights the need for evolutionary-based approaches in comparative genomics

Understanding the evolutionary plasticity of the genome requires a global, comparative approach in which genetic events are considered both in a phylogenetic framework and with regard to population genetics and environmental variables. In the mechanisms that generate adaptive and non-adaptive changes in genomes, segmental duplications (duplication of individual genes or genomic regions) and polyploidization (whole genome duplications) are well-known driving forces. The probability of fixation and maintenance of duplicates depends on many variables, including population sizes and selection regimes experienced by the corresponding genes: a combination of stochastic and adaptive mechanisms has shaped all genomes. A survey of experimental work shows that the distinction made between fixation and maintenance of duplicates still needs to be conceptualized and mathematically modeled. Here we review the mechanisms that increase or decrease the probability of fixation or maintenance of duplicated genes, and examine the outcome of these events on the adaptation of the organism