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Arunkumar, R.

Publications and source records attributed to Arunkumar, R..

9 recordsLinked to original sources

Transgressive gene expression and methylation remodeling in an intraspecific hexaploid wheat hybrid

Intraspecific hybridization in allopolyploid plants can generate additive and nonadditive changes in gene expression through interactions between divergent parental genomes. However, how it simultaneously affects gene expression and the relative expression of homoeologs in higher-order polyploids is less well understood. To study this, we sequenced seedling leaf transcriptomes and profiled gene body methylation in two hexaploid wheat (Triticum aestivum L.) cultivars and their F hybrids. Although only 4.3% of genes differed in expression between the parents, 22.3% deviated from mid-parent expression in the hybrids, with many showing transgressive expression. 32.1% of triads contained at least one homoeolog that deviated from mid-parent expression, and all three homoeologs deviated in 11% of triads, substantially more than expected by chance. Triads in which all three homoeologs were overexpressed also showed reduced differences in expression among homoeologs. Greater parental divergence in relative homoeolog expression was associated with nonadditive expression. Genes lacking gene body methylation were also more likely to show dominant or transgressive expression, whereas gene body methylation was associated with more balanced homoeolog expression and additive or conserved expression. Intraspecific hybridization in hexaploid wheat, even without a change in ploidy, was associated with widespread nonadditive gene expression and altered relative homoeolog expression within triads. These responses were associated with parental differences in homoeolog expression and the absence of gene body methylation.

plant biology↗

Methylomes reveal recent evolutionary changes in populations of two plant species

Plant DNA methylation changes occur hundreds to thousands of times faster than DNA mutations and can be transmitted transgenerationally, making them useful for studying population-scale patterns in clonal or selfing species. However, a state-of-the-art approach to use them for inferring population genetic processes and demographic histories is lacking. To address this, we compare evolutionary signatures extracted from CG methylomes and genomes in Arabidopsis thaliana and Brachypodium distachyon. While methylation variants (SMPs) are less effective than single nucleotide polymorphisms (SNPs) for identifying population differentiation in A. thaliana, they can classify phenotypically divergent B. distachyon subgroups that are otherwise genetically indistinguishable. The site frequency spectra generated using methylation sites from varied genomic locations and evolutionary conservation exhibit an excess of rare alleles. Nucleotide diversity estimates were three orders of magnitude higher for methylation variants than for SNPs in both species, driven by the higher epimutation rate. Correlations between SNPs and SMPs in nucleotide diversity and allele frequencies at gene exons are weak or absent in A. thaliana, possibly because the two sources of variation reflect evolutionary forces acting at different timescales. Linkage disequilibrium quickly decays within 100 bp for methylation variants in both plant species. Finally, we developed a deep learning-based demographic inference approach. We identified recent population expansions in A. thaliana and B. distachyon using methylation variants that were not identified when using SNPs. Our study demonstrates the unique evolutionary insights methylomes provide that SNPs alone cannot reveal.

evolutionary biology↗

Rapid reprogramming and stabilisation of homoeolog expression bias in hexaploid wheat biparental populations

O_LIDifferences in the relative level of expression of homoeologs, known as homoeolog expression bias (HEB), are widely observed in allopolyploids. While the evolution of homoeolog expression bias through hybridisation has been characterised, on shorter timescales the extent to which homoeolog expression bias is preserved or altered between generations remains elusive. C_LIO_LIHere we use biparental mapping populations of hexaploid wheat (Triticum aestivum) with a common Paragon parent to explore the inheritance of homoeolog expression bias in the F5 generation. C_LIO_LIWe found that homoeolog expression bias is inherited for 26-27% of triads in both populations. Most triads ([~]70%) conserved a similar homoeolog expression bias pattern as one or both parents. Inherited patterns were largely driven by changes in the expression of one homoeolog, allowing homoeolog expression bias in subsequent generations to match parental expression. Novel patterns of homoeolog expression bias occurred more frequently in the biparental population from a landrace x elite cross, than in the population with two elite parents. C_LIO_LIThese results demonstrate that there is significant reprogramming and stabilisation of homoeolog expression bias within a small number of generations that differs significantly based on the parental lines used in the crossing. C_LI

plant biology↗

The evolution of constitutively active humoral immune defenses in Drosophila populations under high parasite pressure

Both constitutive and inducible immune mechanisms are employed by hosts for defense against infection. Constitutive immunity allows for a faster response, but it comes with an associated cost that is always present. This trade-off between speed and fitness costs leads to the theoretical prediction that constitutive immunity will be favored where parasite exposure is frequent. We selected populations of Drosophila melanogaster under high parasite pressure from the parasitoid wasp Leptopilina boulardi. With RNA sequencing, we found the evolution of resistance in these populations was associated with them developing constitutively active humoral immunity, mediated by the larval fat body. Furthermore, these evolved populations were also able to induce gene expression in response to infection to a greater level, which indicates an overall more activated humoral immune response to parasitization. The anti-parasitoid immune response also relies on the JAK/STAT signaling pathway being activated in muscles following infection, and this induced response was only seen in populations that had evolved under high parasite pressure. We found that the cytokine Upd3, which induces this JAK/STAT response, is being expressed by immature lamellocytes. Furthermore, these immune cells became constitutively present when populations evolved resistance, potentially explaining why they gained the ability to activate JAK/STAT signaling. Thus, under intense parasitism, populations evolved resistance by increasing both constitutive and induced immune defenses, and there is likely an interplay between these two forms of immunity. Author SummaryImmune defenses can be induced after infection or they may be constitutively active, even in uninfected individuals. As constitutive immunity is a more rapid response, theory predicts that it will be favored when animals frequently encounter parasites. When we subjected populations of Drosophila melanogaster to high rates of parasitization from its natural parasite, Leptopilina boulardi parasitoid wasps, we indeed observed that the immune response became constitutively active. Uninfected insects had an activated humoral immune response and produced cytokine-secreting immune cells that were normally induced after infection. However, we also found that these populations evolved a greater induced response. This included a greatly increased cytokine response after infection, suggesting that the constitutive activation of some aspects of the immune system may allow a greater induced response in other tissues.

evolutionary biology↗

Prenatal Carotenoid Supplementation with Lutein or Zeaxanthin Ameliorates Oxygen-Induced Retinopathy (OIR) in Bco2-/- Macular Pigment Mice

PurposePremature infants at risk of retinopathy of prematurity (ROP) miss placental transfer of carotenoids, lutein (L) and zeaxanthin (Z), during the third trimester. We previously demonstrated that prenatal L and Z supplementation raises carotenoid levels in infants at birth in the Lutein and Zeaxanthin in Pregnancy (L-ZIP) study (NCT03750968). Based on their antioxidant effects and bioavailability, we hypothesized that prenatal maternal supplementation with macular carotenoids would reduce risk of ROP. To test this hypothesis, we utilized "macular pigment mice" genetically engineered to take up L and Z into the retina in a model of oxygen-induced retinopathy (OIR). MethodsPregnant Bco2-/- mice were divided into nine experimental subgroups based on the type of supplementation (L, Z, or placebo) and on maternal supplementation start date corresponding to the three trimesters of human fetal development (E0, E11, and P1). Pups and nursing mothers were exposed to 75% O2 for 5 days (P7-12) and returned to room air for 5 days (P12-17). Pups were sacrificed at P12 and P17, and their retinas were analyzed for vaso-obliteration (VO) and intravitreal neovascularization (INV). ResultsPups of pregnant mice supplemented with L or Z had significant reductions in VO and INV areas compared to placebo. Prenatal carotenoid supplementation starting at E0 or E11 was significantly more protective against OIR than postnatal supplementation starting at P1. ConclusionPrenatal supplementation with L and Z was beneficial in a mouse OIR model. We recommend testing prenatal L and Z supplementation in future human clinical trials to prevent ROP.

biochemistry↗

Recognition of non-self is necessary to activate Drosophila's immune response against an insect parasite

Innate immune responses can be activated by pathogen-associated molecular patterns (PAMPs) or danger signals released by damaged tissues. As PAMPs are typically conserved across broad groups of pathogens but absent from the host, it is unclear whether they allow hosts to recognize parasites that are phylogenetically related to themselves, such as parasitoid wasps infecting insects. Parasitoids must penetrate the cuticle of Drosophila larvae to inject their eggs. In line with previous results, we find that the danger signal of wounding triggers the differentiation of specialized immune cells called lamellocytes. However, using oil droplets to mimic infection by a parasitoid wasp egg, we find that the activation of melanization response that kills parasitoids also requires exposure to a parasitoid wasp molecule that acts as a PAMP. The unidentified factor enhances the transcriptional response in hemocytes and induces a specific response in the fat body that includes Tep1, which is essential for efficient melanization. We conclude that a combination of danger signals and PAMPs are required activate Drosophilas immune response against parasitic insects.

immunology↗

Recurrent loss of an immunity gene that protects Drosophila against a major natural parasite

Polymorphisms in immunity genes can have large effects on susceptibility to infection. To understand the origins of this variation, we investigated the genetic basis of resistance to the parasitoid wasp Leptopilina boulardi in Drosophila melanogaster. A cis-regulatory polymorphism in the gene Lectin-24A abolishes expression after infection, strongly reducing survival. Other null mutations have arisen repeatedly in this gene, with additional loss-of-expression and premature stop codons segregating in nature. The frequency of these alleles varies greatly, and in some populations natural selection has driven them near to fixation. We conclude that there is a pleiotropic cost to Lectin-24A expression, and in some populations this outweighs the benefit of resistance, resulting in natural selection causing the repeated loss of this important immune defense. Significance StatementGenetic differences between individuals can have a large effect on susceptibility to infectious disease. We have identified a gene called Lectin-24A that is important in the immune response that protects fruit flies against one of their main natural enemies--parasitic wasps. However, in nature many flies carry mutated copies of this gene that are no longer functional. We found that the high frequency of these loss-of-function mutations can only be explained if they have a selective advantage in some populations. Therefore, we can conclude that this immune defiance is costly, and genetic variation in susceptibility is maintained because in some locations susceptible flies are fitter than resistant flies.

evolutionary biology↗

Transcription factor retention through multiple polyploidisation steps in wheat

O_LIWhole genome duplication (WGD) is widespread in plant evolutionary history, but the mechanisms of non-random gene loss after WGD are debated. The gene balance hypothesis proposes that dosage-sensitive genes such as regulatory genes are retained in polyploids. To test this hypothesis, we analysed the retention of transcription factors (TFs) in the recent allohexaploid bread wheat (Triticum aestivum). C_LIO_LIWe annotated TFs in hexaploid, tetraploid and diploid wheats; compared the co-expression of homoeologous TF and non-TF triads; and analysed single nucleotide variation in TFs across cultivars. C_LIO_LIWe found that, following each of two hybridisation and WGD events, the proportion of TFs in the genome increased. TFs were preferentially retained over other genes as homoeologous groups in tetraploid and hexaploid wheat. Across cultivars, TF triads contain fewer deleterious missense mutations than non-TFs. C_LIO_LITFs are preferentially retained as three functional homoeologs in hexaploid wheat, in support of the gene balance hypothesis. High co-expression between TF homoeologs suggests that neo- and sub-functionalisation are not major drivers of TF retention in this young polyploid. Knocking out one TF homoeolog to alter gene dosage, using TILLING or CRISPR, could be a way to further test the gene balance hypothesis and generate new phenotypes for wheat breeding. C_LI

plant biology↗

Constitutive activation of cellular immunity underlies the evolution of resistance to infection

Organisms rely on inducible and constitutive immune defences to combat infection. Constitutive immunity enables a rapid response to infection but may carry a cost for uninfected individuals, leading to the prediction that it will be favoured when infection rates are high. When we exposed populations of Drosophila melanogaster to intense parasitism by the parasitoid wasp Leptopilina boulardi, they evolved resistance by developing a more reactive cellular immune response. Using single-cell RNA sequencing, we found that immune-inducible genes had become constitutively upregulated. This was the result of resistant larvae differentiating precursors of specialized immune cells called lamellocytes that were previously only produced after infection. Therefore, populations evolved resistance by genetically hard-wiring an induced immune response to become constitutive.

evolutionary biology↗