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Aarts, M. G. M.

Publications and source records attributed to Aarts, M. G. M..

14 recordsLinked to original sources

Multi-environment GWAS analysis for photosynthetic light use efficiency in Arabidopsis thaliana

Photosynthesis is acknowledged as a potential target to increase crop yield. Improved photosynthesis may be achieved by conventional breeding, exploiting the available natural genetic variation for photosynthesis traits. This approach is challenging for crops due to limitations in high-throughput photosynthesis phenotyping, the highly polygenic nature of photosynthesis, and its strongly dynamic response to environmental changes. Recent advancements in phenomics make accurate and detailed photosynthesis phenotyping more feasible, with the model species Arabidopsis thaliana paving the way for applications in crops. In this study, we examined photosynthesis parameters over time in the global Arabidopsis HapMap diversity panel exposed to three conditions: optimal nutrient supply, low phosphorus supply and low nitrogen supply. Combined with two previous studies on photosynthesis in response to low temperature, and to a one-step change in irradiance from low light to high light, five high-quality datasets were systematically analysed using the same approach (with one million-maker set, uni- and multi-variate analyses). Our findings emphasize the genetic complexity of photosynthesis, detecting hundreds of significant quantitative trait loci, only a small number of which are robust, and of which most are condition specific. Robust loci, found in multiple conditions, exemplify those suited for conferring higher all-round photosynthesis, and targets for marker-assisted selection, contributing to environmental resilience, while the multitude of small-effect conditional loci suggest that genomic selection approaches may be more suited to improve crop photosynthesis.

genetics↗

The Lettuce Expression Browser: from lab to LEB

Lettuce (Lactuca sativa L.) is an economically important leafy vegetable within the Asteraceae family, cultivated worldwide across diverse agricultural systems. Recent advances in genomic and transcriptomic resources have positioned lettuce as a promising model system for functional genomics in the Asteraceae. However, currently available gene expression datasets lack comprehensive tissue-specific resolution, primarily focus on a single cultivar and are not visualised in an interpretable manner, limiting their utility for broader genetic and physiological studies. To bridge this gap, we developed the Lettuce Expression Browser (LEB), a publicly available platform providing high-resolution gene expression maps across various organs, tissues and developmental stages in both cultivated and wild lettuce species. The LEB integrates transcriptomic data from finely dissected seedlings, shoot tissues at various developmental stages and seedlings subjected to abiotic stresses (salt and far-red), visualised using the ggPlantmap R package. This platform offers an intuitive interface for exploring gene expression patterns and serves as a valuable resource for those studying lettuce development, stress responses, and evolutionary genomics. The LEB is hosted on the LettuceKnow Web Portal (https://lettuce.bioinformatics.nl) and can be expanded to include additional datasets, enhancing its role as a key tool for lettuce research and crop improvement. Significance statementThe Lettuce Expression Browser (LEB) provides the first high-resolution gene expression atlas for both cultivated and wild lettuce species. This open-access resource enables detailed exploration of gene activity across development stages and stress conditions, advancing functional genomics in the Asteraceae family.

plant biology↗

Gain and loss of gene function shaped the nickel hyperaccumulation trait in Noccaea caerulescens

Nickel hyperaccumulation is an extreme adaptation to ultramafic soils observed in more than 500 plant species. However, our understanding of the molecular mechanisms underlying the evolution of this trait remains limited. To shed light on these mechanisms, we have generated a high-quality genome assembly of the metal hyperaccumulator Noccaea caerulescens. We then used this genome as reference to conduct comparative intraspecific and interspecific transcriptomic analyses using various accessions of N. caerulescens and the non-accumulating relative Microthlaspi perfoliatum, to identify genes associated with nickel hyperaccumulation. Our results suggest a correlation between nickel hyperaccumulation and a decrease in the expression of genes involved in defense responses and the regulation of membrane trafficking. Surprisingly, these analyses did not reveal a significant enrichment of genes involved in the regulation of metal homeostasis. However, we found that the expression levels of selected metal transporters, namely NcHMA3, NcHMA4 and NcIREG2, is consistently elevated in N. caerulescens accessions hyperaccumulating nickel. Furthermore, our analyses identified frameshift mutations in NcIRT1 associated with the loss of nickel hyperaccumulation in a few accessions. We further showed that the expression of a functional NcIRT1 in roots of the La Calamine accession increases nickel accumulation in shoots. Our results demonstrate that NcIRT1 participate in nickel hyperaccumulation in N. caerulescens. They also suggest that nickel hyperaccumulation is an ancient trait in N. caerulescens that has evolved from the high and constitutive expression of few metal transporters including NcIREG2 and that the trait was subsequently lost in a few accessions due to mutations in NcIRT1.

plant biology↗

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↗

Response of photosynthetic efficiency to short-term fluctuating light and cold in tomato

Climate-resilient crops are crucial for meeting global food demand and increasing crop productivity. Photosynthesis, a crucial process, is impacted by environmental changes such as temperature and irradiance. Photosynthesis and stomatal opening often lag behind these changes, resulting in a loss in Light Use Efficiency (LUE). Temperature variations also affect photosynthesis, with a decrease below the optimal threshold resulting in a decrease in photosynthetic efficiency. To enhance photosynthetic LUE, understanding plant responses to environmental changes is essential. This study examines the short-term responses of four tomato genotypes to irradiance fluctuations using chlorophyll fluorescence and the effects of transient cold stress. The results show genotype-to-genotype variation in the maximum quantum efficiency of PSII, the kinetics of the quantum efficiency of PSIIs response to step changes in irradiance, and steady-state values of {Phi}PSII, which is used as a stand-in for photosynthetic efficiency. The control conditions were measured at 24{degrees}C and the cold stress conditions at 14{degrees}C. The fact that {Phi}PSII responds dynamically to step decrease and increase in irradiance and how cold impacts these responses illustrates the way tomato genotypes are impacted by cold stress. It also reveals how the genotypes adapt to cold exposure and recover once the cold stress is reversed. HighlightThis study investigates the adaptation and recovery of four tomato genotypes to irradiance fluctuations and transient cold stress, highlighting the importance of climate-resilient crops for food demand.

biophysics↗

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↗

Steep logarithmic increase of genetic variation in natural Arabidopsis thaliana accessions across geographic scales

Arabidopsis thalianas large native range across Eurasia and display of considerable genetic variation is key to its increasing use in eco-evolutionary studies. The structure and amount of this genetic variation has been studied on various geographic scales. On a continental scale, the genetic variation was postulated to follow an isolation by distance model, implying less genetic variation at smaller geographic distances. However, recent studies showed that the genetic variation is already high on small geographic scales, yet direct comparisons of the genetic variation across different geographic scales are rare. Here, we present a new local diversity panel covering 19 km2 with accessions of the Veluwe, the Netherlands. We compared the genetic variation of this local diversity panel to a national and a continental A. thaliana diversity panel. Direct comparison of these three geographic scales showed that local accessions harbour already 41.8% of the genetic variation found on a continental scale despite the substantial difference in geographic surface area covered. Moreover, a rapidly ascending logarithmic relationship between genetic and geographic distances was observed at continental, national and local scale and thus irrespective of the geographic scale considered. The high level of local genetic variation reported here poses new questions on which evolutionary forces are driving and maintaining this, and how much this constrains experimental design when using local A. thaliana populations in future eco-evolutionary studies.

genetics↗

Comparative transcriptomics of Hirschfeldia incana and relatives highlights differences in photosynthetic pathways

Photosynthesis is the only yield-related trait that has not yet been substantially improved by plant breeding. The limited results of previous attempts to increase yield via improvement of photosynthetic pathways suggest that more knowledge is still needed to achieve this goal. To learn more about the genetic and physiological basis of high photosynthetic light-use efficiency (LUE) at high irradiance, we study Hirschfeldia incana. Here, we compare the transcriptomic response to high light of H. incana with that of three other members of the Brassicaceae, Arabidopsis thaliana, Brassica rapa, and Brassica nigra, which have a lower photosynthetic LUE. First, we built a high-light, high-uniformity growing environment in a climate-controlled room. Plants grown in this system developed normally and showed no signs of stress during the whole growth period. Then we compared gene expression in low and high-light conditions across the four species, utilizing a panproteome to group homologous proteins efficiently. As expected, all species actively regulate genes related to the photosynthetic process. An in-depth analysis on the expression of genes involved in three key photosynthetic pathways revealed a general trend of lower gene expression in high-light conditions. However, H. incana distinguishes itself from the other species through higher expression of certain genes in these pathways, either through constitutive higher expression, as for LHCB8, ordinary differential expression, as for PSBE, or cumulative higher expression obtained by simultaneous expression of multiple gene copies, as seen for LHCA6. These differentially expressed genes in photosynthetic path-ways are interesting leads to further investigate the exact relationship between gene expression, protein abundance and turnover, and ultimately the LUE phenotype. In addition, we can also exclude thousands of genes from "explaining" the phenotype, because they do not show differential expression between both light conditions. Finally, we deliver a transcriptomic resource of plant species fully grown under, rather than briefly exposed to, a very high irradiance, supporting efforts to develop highly efficient photosynthesis in crop plants.

bioinformatics↗

Functional copy number variation in SQUALENE EPOXIDASE-LIKE genes affects photosystem II efficiency in Arabidopsis

In this study, we found a single quantitative trait locus for photosystem II efficiency ({Phi}PSII) in the Arabidopsis Ler-0 x Col-0 recombinant inbred line population. This locus on chromosome 5 is caused by genetic variation in a cluster of tandemly repeated SQUALENE EPOXIDASE-LIKE (SQE-like) genes, with unknown function. We show the QTL is caused by variation in the SQE5, SQE6 and SQE7 genes affecting {Phi}PSII in a dose-dependent manner, due to a combination of functional copies. Col-0 carries only one functional copy, SQE5, while Ler-0 carries functional copies of SQE6 and SQE7. Overexpression of a functional copy of SQE6 enhances {Phi}PSII to exceed that of the Ler-0 parent in Arabidopsis, but does not affect {Phi}PSII in tobacco. Phylogenetic analysis of the SQE and SQE-likes in 135 plant species revealed that the SQE-likes are evolutionary confined to two sister families, the Cleomaceae and Brassicaceae, and diversified independently. The tandem cluster of four SQE-like genes in Arabidopsis is likely the result of two recent gene duplication events, one generating SQE5 from SQE4, the next one generating SQE6 and SQE7 from SQE5. The involvement of SQE-like genes in photosynthesis will open up new avenues to determine the function of these novel genes.

plant biology↗

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 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↗

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↗