Cytotype distribution patterns, ecological differentiation, and genetic structure in a diploid–tetraploid contact zone of <i>Cardamine amara</i>

Zozomová‐Lihová, Judita; Malánová-Krásná, Iva; Vít, Petr; Urfus, Tomáš; Senko, Dušan; Svitok, Marek; Kempa, Matúš; Marhold, Karol

doi:10.3732/ajb.1500052

Cited by 42 publications

(47 citation statements)

References 95 publications

(159 reference statements)

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“…1A; Table S1). We chose these populations based on a comprehensive cytological survey of over 3,000 C. amara samples throughout the Czech Republic 18 . The populations we sampled represent core areas of each cytotype, away from potential hybrid zones and distant from any triploid-containing populations.…”

Section: Resultsmentioning

confidence: 99%

“…C. amara populations sampled in the Czech Republic (red, diploids LUZ and VKR; blue, tetraploids CEZ and PIC; measure corresponds to 200 km; shaded area represents each cytotype range from 18 , with evident tetraploid range expansion southward). B, Population structure represented by Principal Component Analysis (PCA) of ~124,000 fourfold degenerate SNPs.…”

Section: Figure 1 Sample Population Locations and Population Structumentioning

confidence: 99%

“…To do this, we take advantage of a divergent 16 , well-characterised diploid/autopolyploid species, Cardamine amara (Brassicaceae, tribe Cardamineae). A large-scale cytotyping survey and genetic structure analysis demonstrated an autopolyploid origin of the tetraploid cytotype found in the Eastern and Central Alps [17][18][19][20] . Importantly, C. amara occupies similar territory as both A. arenosa and A. lyrata and similar life history (perennial herb) and evolutionary history (likely single origin in the target study area, followed by tetraploid expansion associated with glacial oscillations) 18,19 .…”

Section: Introductionmentioning

confidence: 99%

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Genomic novelty and process-level convergence in adaptation to whole genome duplication

Bohutínská

Alston

Monnahan

et al. 2020

Preprint

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Whole genome duplication (WGD) occurs across kingdoms and can promote adaptation. However, the sudden increase in chromosome number, as well as immediate changes in cellular physiology, are traumatic to conserved cellular processes. Previous work in Arabidopsis arenosa revealed a clearly coordinated genomic response to WGD, involving a set of functionally and physically interacting proteins mediating crossover number and distribution during prophase I of meiosis. Here we ask: is this highly coordinated coevolutionary shift repeated in other species? We also test globally for convergence for all processes under selection in independent cases of adaptation to WGD, as other processes were under selection in A. arenosa and may be common to other independent adaptation events following WGD. Taking advantage of a well-characterised diploid/autopolyploid system, Cardamine amara, we test our hypothesis that convergence will be detected in the form of directional selection. We also investigate at what level convergence may be evident: identical genes, networks, or analogous processes. To do this we performed a genome scan between diploid and autotetraploid populations, while utilising a quartet-based sampling design to minimise false positives. Among the genes exhibiting the strongest signatures of selection in C. amara autotetraploids we detect an enrichment for DNA maintenance, chromosome organisation, and meiosis, as well as stress signalling. We find that gene-level convergence between the independent WGD adaptation events in C. amara and A. arenosa is negligible, with no more orthologous genes in common than would be expected by chance. In contrast to this, however, we observe very strong convergence at the level of functional processes and homologous (but not orthologous) genes. Taken together, our results indicate that these two autopolyploids survived the challenges attendant to WGD by modifying similar or identical processes through different molecular players and gives the first insight into the salient adaptations required to cope with a genome-doubled state.

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Section: Resultsmentioning

confidence: 99%

Section: Figure 1 Sample Population Locations and Population Structumentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Genomic novelty and process-level convergence in adaptation to whole genome duplication

Bohutínská

Alston

Monnahan

et al. 2020

Preprint

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“…giraldii , and A. melanandra is characterized by a high frequency of mixed-ploidy populations (56.25%). The cytotype mixture was considered to be an evolutionarily unstable pattern, likely reflecting in situ formation or frequent cytotype immigration, consistent with the minority cytotype exclusion model (Levin, 1975), resulting in the elimination of the minority cytotypes (Baack, 2005; Zozomová-Lihová et al, 2015). Recent studies, however, have shown that mixed-cytotype populations are frequent and that balancing selection is commonly observed in these populations (Burton and Husband, 1999; Keeler, 2004; Kao, 2007; Castro et al, 2012; Duchoslav et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Agronomic Trait Variations and Ploidy Differentiation of Kiwiberries in Northwest China: Implication for Breeding

et al. 2017

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Polyploid plants often have higher biomass and superior crop qualities. Breeders therefore search for crop germplasm with higher ploidy levels; however, whether higher ploidy levels are associated with better performance remains unclear. Actinidia arguta and related species, whose commercialized fruit are referred to as kiwiberries, harbor a series of ploidy races in nature, offering an opportunity to determine the link between ploidy levels and agronomic traits. In the present study, we determined the ploidy levels of A. arguta var. arguta, A. arguta var. giraldii, and A. melanandra in 16 natural populations using flow cytometry, and examined 31 trait variations in fruits, leaves and flowers by field observations, microscopic examination and laboratory analyses. Our results showed that octaploid and decaploid A. arguta var. giraldii had larger dimension of leaves than tetraploid A. arguta var. arguta and A. melanandra, but their fruits were significantly smaller. In addition, A. arguta var. giraldii (8x and 10x) had higher contents of nutrients such as ascorbic acid and amino acids; however, some important agronomic traits, including the content of total sugar and total acid, were significantly lower in the octaploids and decaploids. Moreover, octaploids and decaploids did not result in greater ecological adaptability for the challenging environments and climates. In conclusion, the differentiation of ecological adaptability and traits among natural kiwiberries' cytotypes suggested that higher ploidy levels are not inevitably advantageous in plants. The findings of A. arguta and related taxa in geographical distribution and agronomic trait variations will facilitate their germplasm domestication.

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“…Specifically, polyploids tend to speciate faster than diploids but also to experience faster rates of extinction. On the one hand, faster speciation rates are potentially related to the rate of successful establishment of polyploids to novel habitats (46)(47)(48)(49)(50)(51)(52)(53)(54)(55), or even to their ability to mask deleterious mutations (41)(42)(43)(44)(45)56). On the other hand, polyploidy may trigger extinction rates by decreasing effective population sizes (57,58), increasing rates of segregation errors during meiosis (59), or even by increasing the number of deleterious mutations that may contribute to extinction during diploidization (5,58).…”

Section: Discussionmentioning

confidence: 99%

Polyploidy increases overall diversity despite higher turnover than diploids in the Brassicaceae

Román‐Palacios

Molina-Henao

Barker

2019

Preprint

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Although polyploidy, or whole-genome duplication, is widespread across the Plant Tree of Life, its long-term evolutionary significance is still poorly understood. Here we examine the effects of polyploidy in driving macroevolutionary patterns within the angiosperm family Brassicaceae, a speciose clade exhibiting extensive inter-specific variation in chromosome numbers. We inferred ploidal levels from haploid chromosome numbers for 80% of species in the most comprehensive species-level chronogram for the Brassicaceae published to date. After evaluating a total of 54 phylogenetic models of diversification, we found that ploidy drives diversification rates across the Brassicaceae, with polyploids experiencing faster rates of speciation and extinction, but relatively slower rates of diversification. Nevertheless, diversification rates are, on average, positive for both polyploids and diploids. We also found that despite diversifying significantly slower than diploids, polyploids have played a significant role in driving present-day differences in species richness among clades. Overall, although most polyploids go extinct before sustainable populations are established, rare successful polyploids persist and significantly contribute to the long-term evolution of lineages. Our findings suggest that polyploidy has played a major role in shaping the long-term evolution of the Brassicaceae and highlight the importance of polyploidy in shaping present-day diversity patterns across the plant Tree of Life. Significance statementAlthough polyploidy is a source of innovation, its long-term evolutionary significance is still debated. Here we analyze the evolutionary role of polyploidy within the Brassicaceae, a diverse clade exhibiting extensive variation in chromosome numbers among species. We found that, although polyploids diversify slower than diploids, polyploids have faster extinction and speciation rates. Our results also suggest that polyploidy has played an important role in shaping present-day differences in species richness within the Brassicaceae, with potential implications in explaining diversity patterns across the plant Tree of Life.\body IntroductionAlthough polyploidy-the heritable condition of carrying more than two complete sets of chromosomes-is widespread across the plant phylogeny (1), its evolutionary significance is still debated (2-6). Discussions on the evolutionary role of polyploidy date back to Stebbins (7,8) and Wagner (9) who considered polyploidy to have negligible effects on the long-term evolution of plants. This idea, later known as the 'dead-end' hypothesis, was recently reframed as an expectation that polyploid species will undergo extinction more frequently than diploids (4, 5, 10-12). However, polyploidy can influence the long-term evolution of lineages (1,(13)(14)(15)(16)(17) regardless of whether polyploids are more likely to go extinct than diploids (4,5, 10-12). Both interpretations of the 'dead-end' hypothesis are thus not equivalent to each other. The original hypothesis focused on t...

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Cytotype distribution patterns, ecological differentiation, and genetic structure in a diploid–tetraploid contact zone of Cardamine amara

Abstract: The observed spatial and genetic patterns likely reflect the evolutionary and colonization history of the two cytotypes and have been maintained by multiple factors such as ecological divergence, limited gene flow between the cytotypes, and the restricted dispersal capacity.

Cited by 42 publications

References 95 publications

Genomic novelty and process-level convergence in adaptation to whole genome duplication

Genomic novelty and process-level convergence in adaptation to whole genome duplication

Agronomic Trait Variations and Ploidy Differentiation of Kiwiberries in Northwest China: Implication for Breeding

Polyploidy increases overall diversity despite higher turnover than diploids in the Brassicaceae

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