Biology subjects

Toivainen, T.

Publications and source records attributed to Toivainen, T..

9 recordsLinked to original sources

bioRxiv2026

FvTFL1 reverses the function of FvGI-FvCO-FvFT1 pathway in the photoperiodic flowering of woodland strawberry

O_LIPhotoperiod is a stable seasonal signal. Although the photoperiodic flowering is well understood in short-day (SD) and long-day (LD) annual plants, regulatory mechanisms in perennials remain elusive. In a perennial woodland strawberry (Fragaria vesca L.), flowering is induced in SDs in autumn and plants flower following spring, while in plants with mutated FvTERMINAL FLOWER1 (FvTFL1), LDs induce flowering. C_LIO_LIWe investigated photoperiodic flowering of F. vesca through phenotypic and molecular characterization of transgenic lines and their crosses. We studied natural variation in flowering time and gene expression in European accessions, and explored their correlations with climatic, geographical and genetic origins. C_LIO_LIWe showed that FvGIGANTEA (FvGI) and FvCONSTANS (FvCO) activate FvFLOWERING LOCUS T1 (FvFT1) in LDs resulting in early flowering in fvtfl1 mutant, while in SD F. vesca, activation of FvTFL1 by FvFT1 reverses the photoperiodic requirement of flowering. In natural accessions, decreasing expression of FvFT1 and FvTFL1 towards colder climates in the east and north correlated with earlier flowering. C_LIO_LIWe define a photoperiodic flowering mechanism controlling floral transition of perennial F. vesca in autumn that differs from known mechanisms in annual and perennial plants. Our findings open new avenues to understand how perennial plants cope with changing seasons across climatic and geographical ranges. C_LI

plant biology↗

bioRxiv2025

Uncovering the genetic basis of fruit volatiles in Fragaria vesca through GWAS reveals FvJMT2 as a methyl benzoate biosynthesis gene with insect-repellent function

Strawberry aroma is a key component of fruit quality, influencing consumer preferences and playing important ecological roles, including plant defense. However, the genetic basis of volatile organic compound (VOC) biosynthesis remains only partially understood, particularly in the wild woodland strawberry Fragaria vesca, which has enormous potential to uncover genetic diversity within the genus for improving the commercial strawberries. Here, we performed Genome-Wide Association Studies (GWAS) across a diverse European collection of F. vesca accessions. We identified multiple novel candidate genes involved in the biosynthesis of diverse volatile esters, lactones, terpenoids, and methyl ketones. Among them, we characterized FvJMT2, a SABATH family methyltransferase which we found associated with natural variation in benzenoid esters content. Transient expression in Nicotiana benthamiana and strawberry fruit confirmed its role in methyl benzoate biosynthesis, while enzymatic assays demonstrated that FvJMT2 encodes a promiscuous enzyme capable of methylating not only benzoic acid, but also cinnamic, salicylic, and jasmonic acids. Behavioral assays revealed that methyl benzoate at physiologically relevant concentrations significantly reduced the attraction of Drosophila suzukii flies, supporting a dual role of this VOC in both flavor and pest deterrence. Finally, natural variation analyses in wild Fragaria species and F. x ananassa cultivars showed that benzenoid esters have been largely lost in modern cultivars but retained in ancient and wild accessions. Altogether, this study provides novel insights into the genetics and ecological relevance of strawberry volatiles and identifies candidate loci and alleles for future studies.

genomics↗

bioRxiv2025

FvFT1-FvTFL1 epistasis drives flowering time adaptation in woodland strawberry

Floral transition and flower bud development during autumn and winter are common in plants inhabiting temperate and cold climates. However, our understanding of the natural variation and underlying molecular mechanisms of such life-history strategy remain largely limited to Brassicaceae model species. To address this gap, we investigated flowering time variation across a broad geographical and bioclimatic range in Fragaria vesca (woodland strawberry), a perennial herb from the Rosaceae family. We found that the timing of floral transition and subsequent flowering in F. vesca populations is primarily shaped by population structure, reflecting postglacial colonization patterns from distinct refugia, and is further modulated by adaptations to winter temperatures. The association of increasing expression of FvFT1, the strawberry ortholog of FLOWERING LOCUS T, with delayed flowering in accessions from diverse climatic and genetic backgrounds suggested FvFT1 as a major candidate gene regulating flowering time variation. We further demonstrated how distinct florigen and antiflorigen roles of FvFT1 are dependent on functional alleles of F. vesca TERMINAL FLOWER1 (FvTFL1) and how the epistatic relationship between FvFT1 and FvTFL1 controls adaptive flowering time variation by adjusting sensitivity to floral inductive photoperiod and vernalization. Our findings reveal a major molecular basis of how timing of floral transition has adapted to temperature in a Rosaceae model inhabiting multiple climatic zones and highlight lineage-specific adaptive mechanisms underlying convergent life-history strategy. Significance statementMolecular mechanisms underlying flowering time adaptation have been primarily investigated in annual plants that transit to flowering in spring. However, many perennial plant species in temperate climates form flower buds in autumn and winter to flower in the following spring. We uncover wide geographical and climatic patterns of flowering time adaptation in the perennial model species woodland strawberry. We report that natural variation in the expression of strawberry FLOWERING LOCUS T (FvFT1) gene originating ice ages ago and further driven by local temperature adaptations control flowering time variation in this species. Finally, we show how FvFT1 may function as both flowering promoter and repressor depending on the genetic background, thus revealing a novel mechanism of flowering time adaptation.

plant biology↗

bioRxiv2025

Naturally occurring variation in gene-associated transposable elements impacts gene expression and phenotypic diversity in woodland strawberry

Transposable elements (TEs) are major components of plant genomes and powerful drivers of regulatory and phenotypic diversity, yet their mechanistic contributions to gene regulation in non-model crops remain poorly understood. Here, we generate a comprehensive and curated TE annotation for woodland strawberry (Fragaria vesca), revealing that TEs comprise [~]30% of the genome and uncovering an exceptional enrichment of gene-proximal miniature inverted-repeat transposable elements (MITEs) and short inverted repeats (IRs). Integrating small RNA, DNA methylation and transcriptomic data across tissues and fruit developmental stages, we show that most gene-associated MITEs and IRs are epigenetically active, producing 24-nt siRNAs and displaying dynamic CHH methylation patterns during fruit ripening. Genome-wide analyses reveal that MITE- and IR-proximal genes occupy a distinct regulatory landscape compared to genes associated with other TE classes, consistent with a role in context-dependent transcriptional regulation. As a mechanistic proof of concept, we demonstrate that a Mutator-like MITE located near FvAAT1, encoding a key alcohol acyltransferase required for aroma ester biosynthesis, modulates gene expression through siRNA-dependent DNA methylation and ripening-stage-specific chromatin reorganization. Transient perturbation of this MITE epigenetic state alters FvAAT1 expression, and chromatin conformation capture reveals MITE-associated looping at this locus. Notably, this regulatory MITE is conserved in commercial strawberry species, suggesting an evolutionarily preserved function in fruit quality traits. Extending these findings to natural variation, we characterize thousands of TE insertion and deletion polymorphisms across 210 European F. vesca accessions and show that TE-based variation recapitulates population structure. A TE-informed genome-wide association analysis identifies significant associations between MITE and IR polymorphisms and fruit volatile compounds, including key aroma determinants. Together, our results establish MITEs and short IRs as widespread, epigenetically active regulatory elements that shape gene expression, chromatin architecture and phenotypic diversity in strawberry. This work provides a conceptual and methodological framework to integrate TE-driven regulatory variation into population genomics, breeding and genome-editing strategies aimed at improving fruit quality.

genomics↗

bioRxiv2024

Late Quaternary climatic impact on the woodland strawberry genome: a perennial herb's tale

Exploring a species paleohistory is crucial for understanding its responsiveness to climatic events, identifying drivers of adaptation, and developing effective biodiversity conservation strategies in the face of ongoing climate change. We analyzed 200 genomes of the perennial herb woodland strawberry (Fragaria vesca L.) from across Europe and investigated the population structure and demographic history of the species during past geoclimatic events. We found a clear division of populations into western and eastern genetic clusters, indicative of distinct glacial refugia and adaptations to variation in temperature seasonality. The eastern core populations were several times larger (defined as effective population size, NE) than populations in other regions, showed no evidence of inbreeding, and were resilient to several glacial maxima. However, we observed decreasing NE and higher inbreeding in populations toward range edges, particularly in the north, where these individuals went through bottlenecks during glaciations. Population divergence suggested that western and eastern Europe were colonized from separate refugia in multiple waves during the Holocene, while the largest current populations from the northern Mediterranean to southern regions of the Nordic countries formed a connected population chain with gene flow between eastern core populations and western Europe, primarily occurring through Central Europe. Similar patterns of colonization and hybridization may have occurred during past interglacial periods, contributing to the present-day population structure of woodland strawberry. We suggest that the unprecedented resolution of the species climatic history across six glacial-interglacial cycles presented here holds the promise of transforming the general understanding of species paleohistory through geoclimatically tracing ancestral haplotypes.

plant biology↗

bioRxiv2022

Temperature-induced methylome changes during asexual reproduction trigger transcriptomic and phenotypic changes in Fragaria vesca

Plants must quickly adapt to a changing environment in order to maintain their fitness. One rapid adaptation mechanism that promotes plasticity is epigenetic memory, which may provide long-lived organisms the precious time needed to adapt to climate change. In this study, we used the perennial plant Fragaria vesca as a model to determine how the methylome and transcriptome adapt to elevated temperatures (28 vs. 18 {degrees}C) over three asexual generations. Changes in flowering time, stolon number, and petiole length were induced in responses to temperature treatment in one or more ecotypes after three asexual generations in a manner indicative of an epigenetic memory. Induced methylome changes differed between four different ecotypes from Norway, Iceland, Italy, and Spain, but there were also some shared responses. Elevated temperature conditions induced significant phenotypic and methylation changes, particularly in the Norwegian ecotype. Most of the differentially methylated regions (DMRs) were in the CHG context, and most CHG and CHH DMRs were hypermethylated. Notably, the four ecotypes shared only eight CHG DMR peaks. Several differentially methylated genes (DMGs) also showed a change in gene expression. Ecotype-specific methylation and expression patterns were observed for genes related to gibberellin metabolism, flowering time, epigenetics. Furthermore, when repetitive elements (REs) were found near ({+/-}2 kb) or inside a gene, they showed a negative correlation with gene expression. In conclusion, phenotypic changes induced by elevated temperatures during asexual reproduction were accompanied by changes in DNA methylation patterns. Also, positional influences of REs impacted gene expression, indicating that DNA methylation may be involved in both general and ecotype-specific phenotypic plasticity in F. vesca.

genomics↗

bioRxiv2021

Standing covariation between genomic and epigenomic patterns as source for natural selection in wild strawberry plants

Adaptive evolution is generally thought to be the result of natural selection predominantly acting upon pre-existing DNA sequence polymorphisms through gene-environment interactions. Epigenetic inheritance is, however, recently considered an additional molecular force driving adaptive evolution independent of DNA sequence variation. Through comparative analyses of genome-wide genetic (SNPs) and epigenetic (DMCs) variation of wild strawberry plants raised under distinct drought settings, we demonstrate intermediate levels of genome-wide covariation between SNPs and DMCs. Cases of high SNP-DMC covariation were significantly associated with (i) applied stress, (ii) non-adaptive SNPs, and (iii) solitary DMCs (as opposed to DMC islands). We also found that DMCs, drought-responsive DMCs in particular, typically co-vary with hundreds of SNPs, indicating high genomic redundancy as a basis for polygenic adaptation. Our findings suggest that stress-responsive DMCs initially co-vary with many associated SNPs under increased environmental stress (cfr. co-gradient plasticity), and that natural selection acting upon these SNPs subsequently reduce standing covariation with stress-responsive DMCs. In addition, the degree of covariation between SNPs and DMCs appears independent of their respective genomic distance, indicating that trans-acting associations between SNPs and DMCs are as likely as cis-acting associations. Our study is in favor of DNA methylation profiles representing complex quantitative traits rather than independent evolutionary forces, but further research is required to fully rule out SNP-independence of genome-wide DMCs. We provide a conceptual framework for polygenic regulation and adaptation shaping genome-wide methylation patterns.

evolutionary biology↗

bioRxiv2020

Allelic Variation of MYB10 is the Major Force Controlling Natural Variation of Skin and Flesh Color in Strawberry (Fragaria spp.) fruit

Anthocyanins are the principal color-producing compounds synthesized in developing fruits of strawberry (Fragaria spp.). Substantial natural variation in color have been observed in fruits of diploid and octoploid accessions, resulting from distinct accumulation and distribution of anthocyanins in fruits. Anthocyanin biosynthesis is controlled by a clade of R2R3 MYB transcription factors, among which MYB10 has been shown as the main activator in strawberry fruit. Here, we show that MYB10 mutations cause most of the anthocyanin variation observed in diploid woodland strawberry (F. vesca) and octoploid cultivated strawberry (F. xananassa). Using a mapping-by-sequencing approach, we identified a gypsy-transposon insertion in MYB10 that truncates the protein and knocks out anthocyanin biosynthesis in a white-fruited F. vesca ecotype. Two additional loss-of-function MYB10 mutations were identified among geographically diverse white-fruited F. vesca ecotypes. Genetic and transcriptomic analyses in octoploid Fragaria spp. revealed that FaMYB10-2, one of three MYB10 homoeologs identified, residing in the F. iinumae-derived subgenome, regulates the biosynthesis of anthocyanins in developing fruit. Furthermore, independent mutations in MYB10-2 are the underlying cause of natural variation in fruit skin and flesh color in octoploid strawberry. We identified a CACTA-like transposon (FaEnSpm-2) insertion in the MYB10-2 promoter of red-fleshed accessions that was associated with enhanced expression and anthocyanin accumulation. Our findings suggest that putative cis regulatory elements provided by FaEnSpm-2 are required for high and ectopic MYB10-2 expression and induction of anthocyanin biosynthesis in fruit flesh. We developed MYB10-2 (sub-genome) specific DNA markers for marker-assisted selection that accurately predicted anthocyanin phenotypes in octoploid segregating populations.

plant biology↗

bioRxiv2019

Evolutionary genomics of structural variation in Asian rice (Oryza sativa) and its wild progenitor (O. rufipogon)

Structural variants (SVs) are a largely unstudied feature of plant genome evolution, despite the fact that SVs contribute substantially to phenotypes. In this study, we discovered structural variants (SVs) across a population sample of 358 high-coverage, resequenced genomes of Asian rice (Oryza sativa) and its wild ancestor (O. rufipogon). In addition to this short-read dataset, we also inferred SVs from whole-genome assemblies and long-read data. Comparisons among datasets revealed different features of genome variability. For example, genome alignment identified a large (~4.3 Mb) inversion in indica rice varieties relative to an outgroup, and long-read analyses suggest that ~9% of genes from this outgroup are hemizygous. We focused, however, on the resequencing sample to investigate the population genomics of SVs. Clustering analyses with SVs recapitulated the rice cultivar groups that were also inferred from SNPs. However, the site-frequency spectrum of each SV type -- which included inversions, duplications, deletions, translocations and mobile element insertions -- was skewed toward lower frequency variants than synonymous SNPs, suggesting that SVs are predominantly deleterious. The strength of these deleterious effects varied among SV types, with inversions especially deleterious, and across transposable element (TE) families. Among TEs SINE and mariner insertions were especially deleterious, due to stronger selection against their insertions. We also used SVs to study domestication by contrasting between rice and O. rufipogon. Cultivated genomes contained ~25% more derived SVs than O. rufipogon, suggesting these deleterious SVs contribute to the cost of domestication. We also used SVs to study the effects of positive selection on the rice genome. Generally, the search for domestication genes were enriched for known candidates, suggesting some utility for SVs towards this purpose. More importantly, we detected hundreds to thousands of genes gained and lost during domestication, many of which are predicted to contribute to traits of agronomic interest.

evolutionary biology↗