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Biology subjects

Becker, F. F. M.

Publications and source records attributed to Becker, F. F. M..

13 recordsLinked to original sources

Local population genetic structure of Andrena flavipes (Hymenoptera, Andrenidae), a nest-philopatric communal mining bee, reveals isolation-by-distance and high inbreeding

Wild bee populations are declining globally and understanding how species-intrinsic traits like nest-philopatry shape local population genetic structure is increasingly important for their conservation. However, few studies have explored this at local spatial scales. To fill this gap, we used SNPs in the nuclear vitellogenin (Vg) gene to assess the local population structure and genetic diversity of the philopatric yellow-legged mining bee, Andrena flavipes, in the Netherlands, one of the most fragmented and urbanized countries in Europe. We investigated whether its reported nest-philopatry, combined with a fragmented landscape, would lead to genetic differentiation and isolation-by-distance (IBD) between populations, and low genetic diversity and inbreeding within populations. A total of 144 A. flavipes bees were sequenced for the full-length Vg gene and genotyped for SNPs. Despite high overall genetic variation, we found a heterozygote deficit and positive inbreeding coefficient in most populations, suggesting non-random mating. Low genetic differentiation was detected between populations, with no distinct genetic clusters, but with a pattern of IBD. These results suggest extensive but spatially structured gene flow, consistent with philopatric behaviour, and indicate that increasing isolation between nest-aggregations potentially leads to genetic differentiation over time. Our findings demonstrate that even in a common and widespread species, nest-philopatry and landscape fragmentation can drive inbreeding and spatially structured gene flow at local scales, highlighting the importance of maintaining habitat connectivity and semi-natural elements in agricultural and urbanized landscapes to sustain wild bee populations.

genetics↗

Species wide inventory of Arabidopsis thaliana organellar variation reveals ample phenotypic variation for photosynthetic performance

Efforts to improve photosynthetic performance are increasingly employing natural genetic variation. However, genetic variation in the organellar genomes (plasmotypes) is often disregarded due to the difficulty of studying the plasmotypes and the lack of evidence that this is a worthwhile investment. Here, we systematically phenotyped plasmotype diversity using Arabidopsis thaliana as a model species. A reanalysis of whole genome resequencing data of 1,531 representative accessions shows that the genetic diversity amongst the mitochondrial genomes is eight times lower than amongst the chloroplast genomes. Plasmotype diversity of the accessions divides the species into two major phylogenetic clusters, within which highly divergent subclusters are distinguished. We combined plasmotypes from 60 A. thaliana accessions with the nuclear genomes (nucleotypes) of four A. thaliana accessions to create a panel of 232 novel cytonuclear genotypes (cybrids). The cybrid plants were grown in a range of different light and temperature conditions and phenotyped using high-throughput phenotyping platforms. Analysis of the phenotypes showed that several plasmotypes alone or in interaction with the nucleotypes have significant effects on photosynthesis, and that the effects are highly dependent on the environment. Moreover, we introduce Plasmotype Association Studies (PAS) as a novel method to reveal plasmotypic effects. Within A. thaliana, several organellar variants can influence photosynthetic phenotypes, which emphasizes the valuable role this variation has on improving photosynthetic performance. The increasing feasibility of producing cybrids in various species calls for further research into how these phenotypes may support breeding goals in crop species. Significance statementPhotosynthesis is one of the few crop traits that has been largely unaddressed which can contribute to increasing crop yield potential. Exploiting genetic variation within organellar genomes presents a promising, yet untapped resource to improve photosynthesis. However, the extent of organellar variation and its impact on photosynthesis within a species remains largely unknown. Using Arabidopsis thaliana as a model species, we revealed highly divergent clusters of organellar variation. We constructed 232 novel combinations of species representative organellar and nuclear genomes, referred to as cybrids. High-throughput phenotyping of these cybrids revealed that organellar variants can substantially impact photosynthesis in different environments. These findings indicate that organellar genomes may be a valuable resource for improving photosynthesis in crops.

plant biology↗

Expanding the Triangle of U: The genome assembly of Hirschfeldia incana provides insights into chromosomal evolution, phylogenomics and high photosynthesis-related traits

The Brassiceae tribe encompasses many economically important crops and exhibits high intraspecific and interspecific phenotypic variation. After a shared whole-genome triplication (WGT) event (Br-, [~]15.9 million years ago), different lineages and species underwent differential chromosomal rearrangements (diploidization) leading to diverse patterns of gene retention and loss (fractionation). Lineage diversification and genomic changes contributed to an array of divergence in morphology, biochemistry, and physiology underlying photosynthesis-related traits. The C3 species Hirschfeldia incana is studied as it displays high photosynthetic rates under high-light conditions. We present an improved chromosome-level genome assembly for H. incana (Nijmegen, v2.0) using nanopore and chromosome conformation capture (Hi-C) technologies, with 409Mb in size and an N50 of 52Mb (a 10x improvement over the previously published scaffold-level v1.0 assembly). The updated assembly and annotation allowed to investigate the WGT history of H. incana in a comparative phylogenomic framework from the Brassiceae ancestral genomic blocks and related diploidized crops. Hirschfeldia incana (x=7) shares extensive genome collinearity with Raphanus sativus (x=9). These two species share some commonalities with Brassica rapa and B. oleracea (A genome, x=10 and C genome, x=9, respectively) and other similarities with B. nigra (B genome, x=8). Phylogenetic analysis revealed that H. incana and R. sativus form a monophyletic clade in between the Brassica A/C and B genomes. We postulate that H. incana and R. sativus genomes are results of reciprocal hybridization combinations of the Brassica A/C and B genome types. Our results might explain the discrepancy observed in published studies regarding phylogenetic placement of H. incana and R. sativus in relation to the "Triangle of U" species. Expression analysis of WGT retained gene copies revealed sub-genome expression divergence, likely due to neo- or sub-functionalization. Finally, we highlighted genes associated with physio-biochemical-anatomical adaptive changes observed in H. incana which likely facilitate its high-photosynthesis traits under high light.

plant biology↗

Maroon rice genomic diversity reflects 350 years of colonial history

Maroons in Suriname and French Guiana descend from enslaved Africans who escaped the plantations during colonial times. Maroon farmers still cultivate a large rice diversity, their oldest staple crop. Maroon oral history and written records by colonial authorities provide contrasting perspectives on the origins of Maroon rice. Here, we integrated genomic ancestry analyses of 136 newly sequenced Maroon rice varieties with ethnobotanical and archival research to reconstruct the historical contexts associated with the introduction of rice varieties to the Guianas. We found that a large subset traces to West Africa, linked to the transatlantic slave trade (c.1530-1825). Maroons obtained other varieties from indentured laborers from Java (1890 onwards), USA rice breeders (1932 onwards), and Hmong refugees from the Vietnam War (1991). Furthermore, we found rice types never documented before, indicating Maroon farmers selected from crosses. Overall, our results demonstrate that the Maroon farming system prioritizes maintenance of a high stock diversity, which we posit reflects the expertise they inherited from their (African) ancestors. Ignored by agricultural modernization initiatives, Maroon farmers today are important custodians of a unique cultural heritage. Moreover, the genomic findings underline many Maroon stories about their past. This study hence demonstrates the power of cross-disciplinary crop research to reconstruct aspects of the human past for which historical records may be biased or incomplete. We anticipate that a similar study approach can be applied to other heirloom crops of (Indigenous) communities that may have preserved their history on their farms to reconstruct, acknowledge and honor the past.

genomics↗

Local adaptation of Arabidopsis thaliana in a small geographic region with mild environmental clines

Natural populations of Arabidopsis thaliana provide powerful systems to study adaptation of wild plant species. Previous research has predominantly focused on global populations or accessions collected from regions with diverse climates. However, little is known about the genetics underlying adaptation in regions with mild environmental clines. We have examined a diversity panel consisting of 192 A. thaliana accessions collected from the Netherlands, a region with limited climatic variation. Despite the relatively uniform climate, we identified compelling evidence of local adaptation within this population. Notably, semidwarf accessions, due to mutation of the GIBBERELLIC ACID REQUIRING 5 (GA5) gene, occur at a relatively high frequency near the coast and these displayed enhanced tolerance to high wind velocities. Additionally, we evaluated the performance of the population under iron deficiency conditions and found that allelic variation in the FE SUPEROXIDE DISMUTASE 3 (FSD3) gene affects tolerance to low iron levels. Moreover, we explored patterns of local adaptation to environmental clines in temperature and precipitation, observing that allelic variation at LA RELATED PROTEIN 1C (LARP1c) likely affects drought tolerance. Not only is the genetic variation observed in a diversity panel of A. thaliana collected in a region with mild environmental clines comparable to that in collections sampled over larger geographic ranges, it is also sufficiently rich to elucidate the genetic and environmental factors underlying natural plant adaptation.

plant biology↗

The NDH complex reveals a trade-off that constrains maximising photosynthesis in Arabidopsis thaliana

The Green Revolution has resulted in major improvements in crop productivity, but left photosynthesis largely unimproved. Despite ample variation of photosynthetic performance in crops and their wild relatives, the photosynthetic capacity of elite breeding lines remains well below its theoretical maximum. As yield is often the primary selective trait, current plant breeding approaches result in photosynthetic trade-offs that prevent positive selection for photosynthetic performance itself. Currently, genetic variation for photosynthetic performance is seldomly validated at the genetic level, and as a result these photosynthetic trade-offs remain poorly understood. Here we reveal the physiological nature of a photosynthetic trade-off caused by the NAD(P)H dehydrogenase (NDH) complex. The use of an Arabidopsis thaliana cybrid panel revealed how a natural allele of the chloroplastic gene NAD(P)H-QUINONE OXIDOREDUCTASE SUBUNIT 6 - a subunit of the NDH complex - results in a faster recovery of photosystem II efficiency after a transition from high to low irradiances. This improvement is due to a reduction in NDH activity. Under low-light conditions this reduction in NDH activity has a neutral effect on biomass, while under highly fluctuating light conditions, including high irradiances, more NDH activity is favoured. This shows that while allelic variation in one gene can have beneficial effects on one aspect of photosynthesis, it can, depending on environmental conditions, have negative effects on other aspects of photosynthesis. As environmental conditions are hardly ever stable in agricultural systems, understanding photosynthetic trade-offs allows us to explore shifting photosynthetic performance closer to the theoretical maximum.

plant biology↗

Plethora of QTLs found in Arabidopsis thaliana reveals complexity of genetic variation for photosynthesis in dynamic light conditions

The environments in which plant species evolved are now generally understood to be dynamic rather than static. Photosynthesis has to operate within these dynamic environments, such as sudden changes to light intensities. Plants have evolved photoprotection mechanisms that prevent damage caused by sudden changes to high light intensities. The extent of genetic variation within plants species to deal with these dynamic light conditions remains largely unexplored. Here we show that one accession of A. thaliana has a more efficient photoprotection mechanism in dynamic light conditions, compared to six other accessions. The construction of a doubled haploid population and subsequent phenotyping in a dynamically controlled high-throughput system reveals up to 15 QTLs for photoprotection. Identifying the causal gene underlying one of the major QTLs shows that an allelic variant of cpFtsY results in more efficient photoprotection under high and fluctuating light intensities. Further analyses reveal this allelic variant to be overprotecting, reducing biomass in a range of dynamic environmental conditions. This suggests that within nature, adaptation can occur to more stressful environments and that revealing the causal genes and mechanisms can help improve the general understanding of photosynthetic functioning. The other QTLs possess different photosynthetic properties, and thus together they show how there is ample intraspecific genetic variation for photosynthetic functioning in dynamic environments. With photosynthesis being one of the last unimproved components of crop yield, this amount of genetic variation for photosynthesis forms excellent input for breeding approaches. In these breeding approaches, the interactions with the environmental conditions should however be precisely assessed. Doing so correctly, allows us to tap into natures solution to challenging environmental conditions.

plant biology↗

The genome of Lactuca saligna, a wild relative of lettuce, provides insight into non-host resistance to the downy mildew Bremia lactucae

Lactuca saligna L. is a wild relative of cultivated lettuce (Lactuca sativa L.), with which it is partially interfertile. Hybrid progeny suffer from hybrid incompatibilities (HI), resulting in reduced fertility and distorted transmission ratios. Lactuca saligna displays broad spectrum resistance against lettuce downy mildew caused by Bremia lactucae Regel and is considered a non-host species. This phenomenon of resistance in L. saligna is called non-host resistance (NHR). One possible mechanism behind this NHR is through the plant-pathogen interaction triggered by pathogen-recognition receptors, including nucleotide-binding leucin-rich repeats (NLRs) and receptor-like kinases (RLKs). We report a chromosome-level genome assembly of L. saligna (accession CGN05327), leading to the identification of two large paracentric inversions (>50 Mb) between L. saligna and L. sativa. Genome-wide searches delineated the major resistance clusters as regions enriched in NLRs and RLKs. Three of the enriched regions co-locate with previously identified NHR intervals. RNA-seq analysis of Bremia infected lettuce identified several differentially expressed RLKs in NHR regions. Three tandem wall-associated kinase-encoding genes (WAKs) in the NHR8 interval display particularly high expression changes at an early stage of infection. We propose RLKs as strong candidate(s) for determinants for the NHR phenotype of L. saligna.

genomics↗

The genome sequence of Hirschfeldia incana, a species with high photosynthetic light-use efficiency

Photosynthesis is a biophysical and biochemical process that plays a key role in sustaining plant and human life, being the first step in the production of energy-rich molecules and oxygen in the biosphere. Improving the photosynthetic capacity of agricultural crops is highly desirable to increase their yields. While the core mechanisms of photosynthesis are highly conserved, certainly in higher plants, plants that can maintain a high photosynthetic light-use efficiency at high irradiance are exceptional and may be useful to understand and improve high irradiance photosynthesis of crops. One such exceptional species is Hirschfeldia incana, a member of the well-studied Brassicaceae family that is easy to grow under standard laboratory conditions, providing an excellent resource for studying the genetic and physiological basis of this trait. Here, we present a reference assembly of H. incana and affirm its high photosynthetic efficiency relative to the Brassicaceae species Brassica rapa, Brassica nigra, and Arabidopsis thaliana. We estimate that it diverged from B. rapa and B. nigra 10-11 million years ago and that its genome has diversified from that of the latter two species through large chromosomal rearrangements, species-specific transposon activity, and differential retention of duplicated genes. Genes present at copy numbers different from B. rapa and B. nigra include those involved in photosynthesis and/or abiotic stress, which may mediate the high photosynthetic efficiency of H. incana. We expect the reference assembly of H. incana to be a valuable genomic resource for identifying ways to enhance photosynthetic rates in crop species.

bioinformatics↗

Genetic mapping of genotype-by-ploidy effects in Arabidopsis thaliana

Plants can express different phenotypic responses following polyploidization, but ploidy-dependent phenotypic variation has so far not been assigned to specific genetic factors. To map such effects, segregating populations at different ploidy levels are required. The availability of an efficient haploid-inducer line in Arabidopsis thaliana allows for the rapid development of large populations of segregating haploid offspring. Because Arabidopsis haploids can be self-fertilised to give rise to homozygous doubled haploids, the same genotypes can be phenotyped at both the haploid and diploid ploidy level. Here, we compared the phenotypes of recombinant haploid and diploid offspring derived from a cross between two late flowering accessions to map genotype x ploidy (GxP) interactions. Ploidy-specific quantitative trait loci (QTLs) were detected at both ploidy levels. This implies that mapping power will increase when phenotypic measurements of monoploids are included in QTL analyses. A multi-trait analysis further revealed pleiotropic effects for a number of the ploidy specific QTLs as well as opposite effects at different ploidy levels for general QTLs. Taken together, we provide evidence of genetic variation between different Arabidopsis accessions being causal for dissimilarities in phenotypic responses to altered ploidy levels, revealing a GxP effect. Additionally, by investigating a population derived from late flowering accessions we revealed a major vernalisation specific QTL for variation in flowering time, countering the historical bias of research in early flowering accessions.

genetics↗

Local adaptation shapes metabolic diversity in the global population of Arabidopsis thaliana

The biosynthesis, structure and accumulation of secondary metabolites in plants are largely controlled by genetic factors, which can vary substantially among genotypes within a species. Here we studied a global population of Arabidopsis thaliana accessions for qualitative and quantitative variation in volatile and non-volatile secondary metabolites using essentially untargeted metabolomics. Genome-wide association (GWA) mapping revealed that metabolic variation mainly traces back to genetic variation in dedicated biosynthesis genes. Effect sizes of genetic variants, estimated by a Bayesian procedure, indicate that most of the genetic variation in the accumulation of secondary metabolites is explained by large-effect genes and defined by multiple polymorphisms. The various genetic variants resulted from independent mutation events and combined into distinctive haplotypes, which are representative for specific geographical regions. A strong relationship between the effect-size of regulatory loci, their allele frequencies and fixation index indicates that selection forces discriminate between haplotypes, resulting in different phytochemical profiles. Finally, we demonstrate that haplotype frequencies deviate from neutral theory predictions, suggesting that metabolic profiles are shaped by local adaptation and co-evolution of independent loci.

genetics↗

Braconidae revisited: Bracon brevicornis genome showcases the potential of linked-read sequencing in identifying a putative complementary sex determiner gene

Bracon brevicornis is an ectoparasitoid of a wide range of larval-stage Lepidopterans, including several pests of important crops, such as the corn borer, Ostrinia nubilalis. It is also one of the earliest documented cases of complementary sex determination in Hymenoptera. Here, we present the linked-read genome of B. brevicornis, complete with an ab initio-derived annotation and protein comparisons with fellow braconids, Fopius arisanus and Diachasma alloem. We demonstrate the potential of linked-read assemblies in exploring regions of heterozygosity and search for structural and homology-derived evidence of the complementary sex determiner gene (csd).

genomics↗

Reciprocal cybrids reveal how organellar genomes affect plant phenotypes

Assessing the impact of variation in chloroplast and mitochondrial DNA (collectively termed the plasmotype) on plant phenotypes is challenging due to the difficulty in separating their effect from nuclear derived variation (the nucleotype). Haploid inducer lines can be used as efficient plasmotype donors to generate new plasmotype-nucleotype combinations (cybrids)(Ravi et al., 2014). We generated a panel comprising all possible cybrids of seven Arabidopsis thaliana accessions and extensively phenotyped these lines for 1859 phenotypes under stable and fluctuating conditions. We show that natural variation in the plasmotype results in additive as well as epistatic effects across all phenotypic categories. Plasmotypes which induce more additive phenotypic changes also cause more significant epistatic effects, suggesting a possible common basis for both additive and epistatic effects. On average epistatic interactions explained twice as much of the variance in phenotypes as additive plasmotype effects. The impact of plasmotypic variation was also more pronounced under fluctuating and stressful environmental conditions. Thus, the phenotypic impact of variation in plasmotypes is the outcome of multilevel Nucleotype X Plasmotype X Environment interactions and, as such, the plasmotype is likely to serve as a reservoir of variation which is only exposed under certain conditions. The production of cybrids using haploid inducers is a quick and precise method for assessing the phenotypic effects of natural variation in organellar genomes. It will facilitate efficient screening of unique nucleotype-plasmotype combinations to both improve our understanding of natural variation in nucleotype plasmotype interactions and identify favourable combinations to improve plant performance.

genetics↗