Biology subjects

Wicker, T.

Publications and source records attributed to Wicker, T..

At least 19 recordsLinked to original sources

bioRxiv2026

Reduction of Pollen Number and Anther Length in Bread Wheat Studied by a Nested Association Mapping Population

The number of pollen grains, which carry male gametes in seed plants, has attracted interest in genetics, evolution, and breeding. Rapid evolutionary reductions in pollen number and anther length were reported in selfing species as well as domesticated species, although this poses a challenge for hybrid breeding. Here, we studied the variation of pollen number and anther length of the hexaploid bread wheat (Triticum aestivum) by employing a quick pollen counting method. Pollen numbers in cultivars were lower than those in landraces among 54 lines of diverse geographic origins. Using the year of registration of traditional and modern cultivars, we found a reduction in pollen number over the past 150 years. We detected high heritability and variation among Asian landraces and cultivars. Thus, we conducted QTL mapping of pollen number as well as of anther length using nested association mapping lines in which Norin 61 was the common parent. Genomic loci encompassing Green Revolution genes (Rht-B1, Rht-D1, and Ppd-D1) showed significant effects on pollen number and anther length, but their contributions were relatively minor. Although anther length has often been used as a proxy for pollen number in bread wheat, our data showed that their correlations are not necessarily high. Interestingly, we identified a new QTL of pollen number that was not detected by measuring anther length, and, vice versa, a new QTL specific to anther length. These data suggest that pollen number has reduced rapidly in bread wheat but can be modified using the genetic diversity of landraces. Significance statementWe found that modern cultivars of bread wheat have reduced pollen number and shorter anther length, which are common in domesticated species but can be a challenge for hybrid breeding. Using underutilized Asian landraces and cultivars, we reported that new quantitative trait loci as well as loci used in the Green Revolution, are responsible for the traits, which can be employed to increase pollen numbers.

plant biology↗

bioRxiv2026

Tracing the origin of non-brittle rachis alleles in wheat

The evolution of non-brittle rachises, controlled by the TtBTR1 genes, was a key step during wheat domestication. Here, using k-mer-based approaches applied to a large diversity panel, we refine previous estimates of the geographical and temporal origins of the three known Ttbtr1 loss-of-function alleles and show that they emerged in distinct wild emmer subpopulations. For this, we generated a chromosome-scale dika wheat assembly carrying the recently discovered Ttbtr1-Ab allele. Our analyses reveal that the Ttbtr1-A alleles reside on an introgression from the southern judaicum wild emmer population into northern wild emmer wheat, providing an explanation for the long-standing debate about the Ttbtr1-A origin. We further demonstrate that the Ttbtr1-Aa and Ttbtr1-B alleles are already present in wild emmer wheat, with evidence indicating that they arose prior to the advent of agriculture. Together, these findings support a model in which key domestication genes in domesticated crops were selected and combined from standing genetic variation in wild relatives.

genomics↗

bioRxiv2025

Dual recognition of structurally unrelated mildew effectors underlies the broad-spectrum resistance of Pm3e in wheat

Broad-spectrum resistance genes are highly valuable for sustainable crop protection, yet the molecular basis of their activity is often unknown. The Pm3 allelic series in wheat encodes NLR receptors that recognize avirulence (AVR) effectors of wheat powdery mildew. Here, we show that near-identical Pm3 alleles vary greatly in resistance efficacy and broadness against a global mildew isolate collection and subsequently use this model system to study the mechanisms underlying broad-spectrum resistance. We demonstrate that two alleles, Pm3d and Pm3e, provide resistance against the majority of isolates worldwide, by each recognizing two AVR effectors from powdery mildew, thereby lowering the risk of resistance breakdown. While Pm3d recognizes two closely related RNase-like AVR effectors, Pm3e detects two structurally diverse AVRs, including an effector belonging to a large, uncharacterized protein family with a novel structural fold. Using chimeric Pm3 NLRs, we identify specificity-defining polymorphisms of Pm3d and Pm3e against their diverse effector targets. Lastly, we demonstrate that Pm3d and Pm3e activities can be combined in engineered Pm3 NLRs, thereby further extending their recognition spectrum. Our findings highlight the potential of Pm3 immune receptors for long-lasting wheat protection by demonstrating their versatility in recognizing structurally diverse effectors and their amenability to NLR engineering.

plant biology↗

bioRxiv2025

An HMA-like integrated domain in the wheat tandem kinase WTK4 recognises an RNase-like pathogen effector

Proteins with a tandem kinase structure have recently emerged as new players in race-specific resistance in cereal crops. However, the molecular understanding of these novel immune receptors resistance mechanisms is limited by the lack of knowledge about the pathogen effectors that they recognise. In this work, we identify AvrWTK4, the wheat powdery mildew RNase-like effector recognised by the wheat tandem kinase immune receptor WTK4, through a combination of bi-parental genetic mapping and mutagenesis. We demonstrate that mutations in the AvrWTK4 gene or a reduction of its expression lead to virulence on WTK4. Transfection of AvrWTK4 specifically induced cell death in WTK4-containing Aegilops tauschii protoplasts. The avirulent AvrWTK4 variant interacts more strongly than the virulent variant with the N-terminal heavy metal-associated (HMA)-like domain of WTK4. These findings further highlight that integrated domains in tandem kinase proteins serve as decoys for pathogen effectors, which could be leveraged to design novel recognition specificities.

molecular biology↗

bioRxiv2025

Virulence on Pm4 kinase-based resistance is determined by two divergent wheat powdery mildew effectors

The wheat resistance gene Pm4 encodes a kinase fusion protein and has gained particular attention as it confers race-specific resistance against two major wheat pathogens: powdery mildew and blast. Here, we describe the identification of AvrPm4, the mildew avirulence effector recognised by Pm4, using UV- mutagenesis, and its functional validation in wheat protoplasts. We show that AvrPm4 directly interacts with and is phosphorylated by Pm4. Using genetic association and QTL mapping, we furthermore demonstrate that evasion of Pm4 resistance by virulent mildew isolates relies on a second fungal component, SvrPm4, which suppresses AvrPm4-induced cell death. Surprisingly, SvrPm4 was previously described as AvrPm1a. We show that SvrPm4, but not its inactive variant svrPm4, is recognised by the NLR immune receptor Pm1a. These multiple roles of a single effector provide a new perspective on fungal (a)virulence proteins and their combinatorial interactions with different types of immune receptors.

genetics↗

bioRxiv2025

The CATION CALCIUM EXCHANGER 4 (CCX4) regulates LRX1-related root hair development through Ca2+ homeostasis

Calcium, as a cellular second messenger, is essential for plant growth. A tip-focused Ca2+ gradient in polarized cells is considered to drive cell expansion. The cell wall polysaccharide pectin is a major Ca2+ binding structure and Ca2+ homeostasis is influenced by the cell wall architecture. LRR-extensin (LRX) proteins are extracellular regulators of cell wall development that are anchored in the cell wall by their extensin domain. The extensin-less LRX1{Delta}E14 variant of the root hair-expressed LRX1 of Arabidopsis induces a dominant-negative effect resulting in aberrant root hairs. In an effort to identify the underlying mechanism of the root hair defect caused by LRX1{Delta}E14, we isolated a suppressor of dominant-negative effect mutant, sune42. It codes for the CATION CALCIUM EXCHANGER 4 (CCX4) that localizes to the Golgi apparatus and was shown to have Ca2+ transport activity. A detailed investigation of the Ca2+ dynamics revealed that LRX1{Delta}E14 coincides with a defect in tip-focused cytoplasmic Ca2+ oscillation, and this effect is alleviated by the sune42 mutation. Additionally, reducing Ca2+ availability influences the LRX1{Delta}E14-induced root hair defect. We conclude that sune42 suppresses the root hair defect in LRX1{Delta}E14 through modulating cytoplasmic Ca2+ dynamics, pointing at the importance of the Golgi apparatus for cellular Ca2+ homeostasis.

plant biology↗

bioRxiv2025

Combining pangenomics and population genetics finds chromosomal re-arrangements, accessory-like chromosome segments, copy number variations and transposon polymorphisms in wheat and rye powdery mildew

Grass powdery mildews (Blumeria spp.) include economically important fungal crop pathogens with complex and highly repetitive genomes. To investigate the diversity and genome evolution in Blumeria graminis, we combined population genetic and pangenomic analyses using a worldwide sample of 399 wheat powdery mildew isolates. Additionally, we produced high-quality genome assemblies for seven isolates from wheat and one from rye powdery mildew. Using these, we compiled the first grass powdery mildew pangenome comprising 11 Blumeria graminis isolates. We found multiple chromosomal rearrangements between the isolates that grow on wheat, rye and/or triticale hosts. Interestingly, chr-11 showed some characteristics of accessory chromosomes such as presence/absence of large chromosomal segments and higher sequence diversity. Additionally, we identified nearly 67,000 cases of copy number variations (CNVs), which were highly enriched within effector gene families. Furthermore, we found evidence for recent and high transposable element (TE) activity, such as high numbers of TE insertion polymorphisms. Analyses of TE families showed enrichment 1 kb to 2 kb up- and downstream of effector genes, and we also found high levels of TE insertion polymorphisms between populations. Our results demonstrate that chromosomal variations, gene family expansions and contractions, and TE activity are important sources of genome diversification and diversity in grass powdery mildews. Our findings indicate that a combination of pangenomic and population genetics analyses is needed to understand drivers of evolution in plant pathogenic fungi in a comprehensive way. Author SummaryFungi are a diverse group of organisms, with some of them (e.g. powdery mildews) having at times a devastating impact on important crops like wheat. Studying the genomes of these grass powdery mildew fungi can improve our understanding the pathogens patterns of genome evolution and virulence in order to find more efficient ways to protect crops. Using high quality genomes of a worldwide dataset of wheat and rye powdery mildews, we found multiple re-arrangements in chromosomes, as well as presence and absence of large chromosomal segments in different mildew strains. Along with some genes, important for making these pathogens infectious on various crop lines, some genomic regions may be deleted or duplicated, potentially affecting how the fungus survives and spreads. Additionally, we found that transposable elements are highly active in powdery mildews and that they are enriched near so-called effector genes, which are associated with fungal virulence. Our study shows how powdery mildew genomes have diversified during recent evolution, which has implications for future breeding of crops toward better resistance to fungal diseases.

genomics↗

bioRxiv2025

Comparative analysis of centromeres of oat (Avena sativa) and its tetraploid and diploid relatives reveals rapid evolution of centromere composition and architecture

BackgroundRecent advances in assemblies of nearly gap-free, high-quality genomes have enabled detailed analysis of centromeres in large and highly repetitive crop genomes. Here, we analyse the hexaploid Avena sativa genome and its tetraploid (A. insularis) and diploid relatives (A. longiglumis, A. atlantica and A. eriantha). ResultsAvena centromeres are largely composed of retrotransposons belonging to three families, RLG_Ava, RLG_Cereba and RLG_Beth. Analysis of retrotransposon populations revealed striking differences in the centromere architecture between the A, C and D genome lineages. We identified distinct profiles of transposable element bursts for these lineages which include the emergence and disappearance of retrotransposon families and subfamilies. We identified multiple centromere shifts which occurred in the C genome lineage within the past [~] 4 myrs and retraced species divergences and polyploidization events in the Avena genus. Although the studied species are closely related, our data show that their centromeres have rapidly evolved different and distinct centromere architectures, for example through the spread of novel satellite repeats or activity bursts of different retrotransposon families and subfamilies. Additionally, we found that RLG_Ava and RLG_Cereba retrotransposons have been coexisting while simultaneously competing for the centromeric "niche" since the emergence of the Poaceae (grasses). ConclusionsOur comparative analyses provided detailed insight into centromere evolution across the Avena genus and revealed that composition and architecture of centromeres can vary greatly even between closely related species and different ploidy levels. Our findings emphasize the need for extended analyses of large genome species to improve our understanding of centromere evolution.

plant biology↗

bioRxiv2024

A reference metagenome sequence of the lichen Cladonia rangiformis

[bullet] Lichens are an ancient symbiosis comprising the thalli of lichen-forming fungi, their photoautotrophic partners and their microbiome. So far, they were poorly studied at the genome sequence level. Here, we present a reference metagenome for the holobiont of Cladonia rangiformis. [bullet]Using long read sequences from an entire symbiotic complex, plus short read libraries from 28 additional diverse European lichen samples, we were able to separate genome sequences of 20 individual species. [bullet]We constructed chromosome-scale assemblies of the C. rangiformis fungus and its trebouxioid green algal photobiont Asterochloris mediterranea. The genome of the fungus comprises [~]22% transposable elements and is highly compartmentalized into genic regions and large TE-derived segments which show extensive signatures of repeat-induced point mutations (RIP). We found that A. mediterranea centromeres are predominantly derived from two interacting retrotransposon families. We also identified strong candidates for genes that were horizontally transferred from bacteria to both alga and fungus. Furthermore, we isolated 18 near-complete bacterial genomes, of which 13 are enriched in the lichen compared to surrounding soil. [bullet]Our study revealed that the thalli of C. rangiformis have a highly complex microbiome, comprising a mix of species that may include opportunists, ecologically obligate symbionts and possibly even lichen-beneficial bacteria.

evolutionary biology↗

bioRxiv2024

The phosphatase PP2C12 is a negative player in LRX-RALF-FER-mediated cell wall integrity sensing

Plants have evolved an elaborate cell wall integrity (CWI) sensing system to monitor and modify cell wall formation. LRR-extensins (LRXs) are cell wall-anchored proteins that bind RAPID ALKALINIZATION FACTOR (RALF) peptide hormones and induce compaction of cell wall structures. At the same time, LRXs form a signaling platform with RALFs and the transmembrane receptor kinase FERONIA (FER) as a means to relay changes in CWI to the protoplast. LRX1 of Arabidopsis thaliana is predominantly expressed in root hairs and lrx1 mutants develop defective root hairs. Here, we identify a regulator of LRX1-RALF-FER signaling as a suppressor of the lrx1 root hair phenotype. The repressor of lrx1_23 (rol23) gene encodes PP2C12, a type 2C phosphatase of clade H that interacts with FER and dephosphorylates Thr696 in the FER activation loop in vitro. The LRX1-related function of PP2Cs appears clade H-specific and was not observed for other PP2Cs investigated. Collectively, our data suggest that LRX1 acts upstream of the RALF1-FER signaling module and PP2C12 has an inhibitory activity via modulating FER activity to fine-tune CWI signaling.

plant biology↗

bioRxiv2024

Histidine limitation causes alteration in the TOR network and plant development

Plant growth depends on growth regulators, nutrient availability, and amino acids levels. The TOR (Target of Rapamycin) network senses these parameters and influences cell wall formation and expansion accordingly. Cell wall integrity and structures are surveyed and modified by a complex array of cell wall integrity sensors, including LRR-extensins (LRXs), that function as hormone receptors and help to compact cell walls. Expressing the Arabidopsis root-hair specific LRX1 without the extensin domain, which anchors the protein to the cell wall, has a negative effect on root hair development. The mechanism of this negative effect was investigated by a suppressor screen, which led to the identification of a sune (suppressor of dominant-negative LRX1) mutant collection. The sune82 mutant was identified as an allele of HISN2 which encodes an enzyme essential for histidine biosynthesis. The sune82 mutation leads to reduced accumulation of histidine, and this influences the TOR network. The sune82 mutant reflects the impact of the TOR network on cell wall formation processes involving LRX proteins. It also represents an excellent tool to study the effects of reduced histidine levels on plant development, as it is a rare example of a viable partial loss-of-function allele in an essential biosynthetic pathway. HighlightPartial loss of function of HISN2 in sune82 results in a significant reduction in histidine content, which subsequently alters the TOR network.

cell biology↗

bioRxiv2024

Analysis of a diverse wheat germplasm panel reveals a highly diverse introgression landscape and provides evidence for inter-homoeolog chromosomal recombination

Agriculturally important genes are often introgressed into crops from closely related donor species or landraces. The gene pool of hexaploid bread wheat (Triticum aestivum) is known to contain numerous such "alien" introgressions. Recently established high-quality reference genome sequences allow prediction of the size, frequency, and identity of introgressed chromosome regions. Here, we characterise chromosomal introgressions in bread wheat using exome capture data from the WHEALBI collection. We identified 26,664 putative introgression segments of at least 2 Mb across 434 wheat accessions. Detailed study of the most frequent introgressions identified T. timophevii or its close relatives as a frequent donor species. Importantly, 118 introgressions of at least 10 Mb were exclusive to single wheat accessions, revealing that large populations need to be studied to assess the total diversity of the wheat pangenome. In one case, a 14 Mb introgression in chromosome 7D, exclusive to cultivar Pamukale, was shown by QTL mapping to harbor a recessive powdery mildew resistance gene. We identified multiple events where distal chromosomal segments of one subgenome were duplicated in the genome and replaced the homoeologous segment in another subgenome. We propose that these examples are the results of inter-homoeolog recombination. Our study produced an extensive catalogue of the wheat introgression landscape, providing a resource for wheat breeding. Of note, the finding that the wheat gene pool contains numerous rare, but potentially important introgressions and chromosomal rearrangements has implications for future breeding. Key messageThis study highlights the potential of rare introgressions, as demonstrated by a major QTL for powdery mildew resistance on chromosome 7D. It further shows evidence for inter-homoeolog recombination in wheat.

plant biology↗

bioRxiv2023

Replicators, genes, and the C-value enigma: High-quality genome assembly of barley provides directevidence that self-replicating DNA forms 'cooperative' associations with genes in arms races

The C-value enigma--the apparent disjunction between the complexity of organisms and the sizes of their genomes--could be in part resolved if it were definitively shown that tolerance of self-copying DNA elements incurred an occasional selective advantage. We leverage the power of the latest genome assembly of the exceptionally repetitive and well-studied cereal crop barley (Hordeum vulgare L.) to explicitly test the hypothesis that the population of genes that have been repeatedly replicated by the action of replication-inducing sequences has undergone selection, favouring genes involved in co-evolutionary arms races (such as genes implicated in pathogen resistance). This was achieved by algorithmically identifying 1,999 genomic stretches that are locally rich in long repeated units. In these loci, we identified 554 geanes, belonging to 42 gene families. These gene families strongly overlap with a test set of pathogen resistance and other likely evolutionary arms-race genes compiled independently from the literature. By statistically demonstrating that selection has systematically influenced the composition of replicator-associated genes at a genome-wide scale we provide evidence that tolerance of repeat-inducing DNA sequences is an adaptive strategy that may contribute to enigmatically inflated C-values, and invite more detailed research on how particular genes become prone to duplication, to the organisms advantage. To this end, we examined the genomic sequences surrounding several of the candidate gene families, and find a repeated pattern of genomic disperse-and-expand dynamics, but where the repeated genomic unit itself varies between sites of expansion. This suggests that genes effectively form opportunistic relationships with replication-inducing DNA elements. We mention implications for agriculture.

evolutionary biology↗

bioRxiv2023

Growth-inhibiting effects of the unconventional plant APYRASE 7 of Arabidopsis thaliana influences the LRX1/FER/RALF growth regulatory module

Plant cell growth involves coordination of numerous processes and signaling cascades among the different cellular compartments to concomitantly enlarge the protoplast and the surrounding cell wall. In Arabidopsis thaliana, the cell wall integrity-sensing process involves the extracellular LRX (LRR-Extensin) proteins that bind RALF (Rapid ALkalinization Factor) peptide hormones and, in vegetative tissues, interact with the transmembrane receptor kinase FERONIA (FER). This LRX/RALF/FER signaling module influences cell wall composition and regulates cell growth. The numerous proteins involved in or influenced by this module are beginning to be characterized. In a genetic screen, mutations in Apyrase 7 (APY7) were identified to suppress growth defects observed in lrx1 and fer mutants. APY7 encodes a Golgi-localized NTP-diphosphohydrolase, but opposed to other apyrases of Arabidopsis, APY7 revealed to be a negative regulator of cell growth. APY7 modulates the growth-inhibiting effect of RALF1, influences the cell wall architecture, and alters the pH of the extracellular matrix, all of which affect cell growth. Together, this study reveals a function of APY7 in cell wall formation and cell growth that is connected to growth processes influenced by the LRX/FER/RALF signaling module.

plant biology↗

bioRxiv2022

A survey of lineage-specific genes in Triticeae reveals de novo gene evolution from genomic raw material

Plant genomes typically contain [~]35,000 genes, almost all belonging to highly-conserved gene families. Only a small fraction are lineage-specific, which are found in only one or few closely related species. Little is known about how genes arise de novo in plant genomes and how often this occurs, however they are believed to be important for plants diversification and adaptation. We developed a pipeline to identify lineage-specific genes in Triticeae, using newly available genome assemblies of wheat, barley and rye. Applying a set of stringent criteria, we identified 5,942 candidate Triticeae-specific genes (TSGs), of which 2,337 were validated as protein-coding genes in wheat. Differential gene expression analyses revealed that stress-induced wheat TSGs are strongly enriched in secreted proteins. Some were previously described to be involved in Triticeae non-host resistance and cold adaptation. Additionally, we show that 1,079 TSGs have sequence homology to transposable elements (TEs), [~]68% of them deriving from regulatory non-coding regions of Gypsy retrotransposons. Most importantly, we demonstrate that these TSGs are enriched in transmembrane domains and are among the most highly expressed wheat genes overall. To summarize, we conclude that de novo gene formation is relatively rare and that Triticeae probably possess [~]779 lineage-specific genes per haploid genome. TSGs which respond to pathogen and environmental stresses, may be interesting candidates for future targeted resistance breeding in Triticeae. Finally, we propose that non-coding regions of TEs might provide important genetic raw material for the functional innovation of TM domains and the evolution of novel secreted proteins.

evolutionary biology↗

bioRxiv2021

Standing genetic variation of the AvrPm17 avirulence gene in powdery mildew limits the effectiveness of an introgressed rye resistance gene in wheat

Introgressions of chromosomal segments from related species into wheat are important sources of resistance against fungal diseases. The durability and effectiveness of introgressed resistance genes upon agricultural deployment is highly variable - a phenomenon that remains poorly understood as the corresponding fungal avirulence genes are largely unknown. Until its breakdown, the Pm17 resistance gene introgressed from rye to wheat provided broad resistance against powdery mildew (Blumeria graminis). Here, we used QTL mapping to identify the corresponding wheat mildew avirulence effector AvrPm17. It is encoded by two paralogous genes that exhibit signatures of re-occurring gene conversion events and are members of a mildew sub-lineage specific effector cluster. Extensive haplovariant mining in wheat mildew and related sub-lineages identified several ancient virulent AvrPm17 variants that were present as standing genetic variation in wheat powdery mildew prior to the Pm17 introgression, thereby paving the way for the rapid breakdown of the Pm17 resistance. QTL mapping in mildew identified a second genetic component likely corresponding to an additional resistance gene present on the 1AL.1RS translocation carrying Pm17. This gene remained previously undetected due to suppressed recombination within the introgressed rye chromosomal segment. We conclude that the initial effectiveness of 1AL.1RS was based on simultaneous introgression of two genetically linked resistance genes. Our results demonstrate the relevance of pathogen-based genetic approaches to disentangle complex resistance loci in wheat. We propose that identification and monitoring of avirulence gene diversity in pathogen populations becomes an integral part of introgression breeding to ensure effective and durable resistance in wheat. Significance StatementDomesticated and wild wheat relatives provide an important source of new immune receptors for wheat resistance breeding against fungal pathogens. The durability of these resistance genes is variable and difficult to predict, yet it is crucial for effective resistance breeding. We identified a fungal effector protein recognised by an immune receptor introgressed from rye to wheat. We found that variants of the effector allowing the fungus to overcome the resistance are ancient. They were already present in the wheat powdery mildew gene pool before the introgression of the immune receptor and are therefore responsible for the rapid resistance breakdown. Our study demonstrates that the effort to identify new resistance genes should be accompanied by studies of avirulence genes on the pathogen side.

plant biology↗

bioRxiv2020

Fonio millet genome unlocks African orphan crop diversity for agriculture in a changing climate

Sustainable food production in the context of climate change necessitates diversification of agriculture and a more efficient utilization of plant genetic resources. Fonio millet (Digitaria exilis) is an orphan African cereal crop with a great potential for dryland agriculture. Here, we established high-quality genomic resources to facilitate fonio improvement through molecular breeding. These include a chromosome-scale reference assembly and deep re-sequencing of 183 cultivated and wild Digitaria accessions, enabling insights into genetic diversity, population structure, and domestication. Fonio diversity is shaped by climatic, geographic, and ethnolinguistic factors. Two genes associated with seed size and shattering showed signatures of selection. Most known domestication genes from other cereal models however have not experienced strong selection in fonio, providing direct targets to rapidly improve this crop for agriculture in hot and dry environments.

plant biology↗

bioRxiv2020

A population-level invasion by transposable elements in a fungal pathogen

AO_SCPLOWBSTRACTC_SCPLOWGenome evolution is driven by the activity of transposable elements (TEs). The spread of TEs can have deleterious effects including the destabilization of genome integrity and expansions. However, the precise triggers of genome expansions remain poorly understood because genome size evolution is typically investigated only among deeply divergent lineages. Here, we use a large population genomics dataset of 284 individuals from populations across the globe of Zymoseptoria tritici, a major fungal wheat pathogen. We built a robust map of genome-wide TE insertions and deletions to track a total of 2,456 polymorphic loci within the species. We show that purifying selection substantially depressed TE frequencies in most populations but some rare TEs have recently risen in frequency and likely confer benefits. We found that specific TE families have undergone a substantial genome-wide expansion from the pathogens center of origin to more recently founded populations. The most dramatic increase in TE insertions occurred between a pair of North American populations collected in the same field at an interval of 25 years. We find that both genome-wide counts of TE insertions and genome size have increased with colonization bottlenecks. Hence, the demographic history likely played a major role in shaping genome evolution within the species. We show that both the activation of specific TEs and relaxed purifying selection underpin this incipient expansion of the genome. Our study establishes a model to recapitulate TE-driven genome evolution over deeper evolutionary timescales.

genomics↗