Transposable elements (TEs) are mobile genetic elements with very high mutation rates that play important roles in shaping genome architecture and regulating phenotypic variation. However, the extent to which TEs influence the adaptation of organisms in their natural habitats is largely unknown. Here, we scanned 201 representative resequenced genomes from the model plant Arabidopsis thaliana and identified 2,311 polymorphic TEs from noncentromeric regions. We found expansion and contraction of different types of TEs in different A. thaliana populations. More importantly, we identified two TE insertions that are likely candidates to play a role in adaptive evolution. Our results highlight the importance of variations in TEs for the adaptation of plants in general in the context of rapid global climate change.

Background In addition to genetic variation, epigenetic variation plays an important role in determining various biological processes. The importance of natural genetic variation to crop domestication and improvement has been widely investigated. However, the contribution of epigenetic variation in crop domestication at population level has rarely been explored. Results To understand the impact of epigenetics on crop domestication, we investigate the variation of DNA methylation during soybean domestication and improvement by whole-genome bisulfite sequencing of 45 soybean accessions, including wild soybeans, landraces, and cultivars. Through methylomic analysis, we identify 5412 differentially methylated regions (DMRs). These DMRs exhibit characters distinct from those of genetically selected regions. In particular, they have significantly higher genetic diversity. Association analyses suggest only 22.54% of DMRs can be explained by local genetic variations. Intriguingly, genes in the DMRs that are not associated with any genetic variation are enriched in carbohydrate metabolism pathways. Conclusions This study provides a valuable map of DNA methylation across diverse accessions and dissects the relationship between DNA methylation variation and genetic variation during soybean domestication, thus expanding our understanding of soybean domestication and improvement.

Flowering time is an adaptive life history trait. Capsella rubella, a close relative of Arabidopsis thaliana and a young species, displays extensive variation for flowering time but low standing genetic variation due to an extreme bottleneck event, providing an excellent opportunity to understand how phenotypic diversity can occur with a limited initial gene pool. Here, we demonstrate that common allelic variation and parallel evolution at the FLC locus confer variation in flowering time in C. rubella. We show that two overlapping deletions in the 5′ untranslated region (UTR) of C. rubella FLC, which are associated with local changes in chromatin conformation and histone modifications, reduce its expression levels and promote flowering. We further show that these two pervasive variants originated independently in natural C. rubella populations after speciation and spread to an intermediate frequency, suggesting a role of this parallel cis-regulatory change in adaptive evolution. Our results provide an example of how parallel mutations in the same 5′ UTR region can shape phenotypic evolution in plants.

Rice (Oryza sativa L.) is a chilling-sensitive staple crop that originated in subtropical regions of Asia. Introduction of the chilling tolerance trait enables the expansion of rice cultivation to temperate regions. Here we report the cloning and characterization of HAN1, a quantitative trait locus (QTL) that confers chilling tolerance on temperate japonica rice. HAN1 encodes an oxidase that catalyzes the conversion of biologically active jasmonoyl-L-isoleucine (JA-Ile) to the inactive form 12-hydroxy-JA-Ile (12OH-JA-Ile) and fine-tunes the JA-mediated chilling response. Natural variants in HAN1 diverged between indica and japonica rice during domestication. A specific allele from temperate japonica rice, which gained a putative MYB cis-element in the promoter of HAN1 during the divergence of the two japonica ecotypes, enhances the chilling tolerance of temperate japonica rice and allows it to adapt to a temperate climate. The results of this study extend our understanding of the northward expansion of rice cultivation and provide a target gene for the improvement of chilling tolerance in rice.

Background and Aims Plant elemental composition is of fundamental importance for plant growth and metabolic functions. However, knowledge of how multi-elemental stoichiometry responds to varying nitrogen (N) and phosphorus (P) availabilities remains limited. Methods We conducted experimental manipulations with nine repeat experiments to investigate the effects of N and P supply on the concentrations and variability of six elements, carbon (C), N, P, potassium (K), calcium (Ca) and magnesium (Mg), in leaves of Arabidopsis thaliana. Key Results N supply increased the concentrations of N, K and Mg, decreased the concentration of P, but exerted little influence on the concentrations of C and Ca in green leaves. P supply increased the concentrations of P and Ca, decreased the concentration of C, initially increased and then decreased the concentration of K, but showed little influence on the concentrations of N and Mg in green leaves. Multivariate patterns among the concentrations of these six elements in green leaves was influenced by the type of nutrient supply (i.e. N or P). Elemental variability decreased with increasing elemental concentrations in green leaves at the intraspecific level, supporting the Stability of Limiting Elements Hypothesis that was originally proposed from a meta-analysis of pooled data across species or communities. Compared with green leaves, the senesced leaves showed greater variability in C, N, P, K and Mg concentrations but lower variability in Ca concentration. Conclusions N and P supplies exerted differential influences on the concentrations of C, N, P, K, Ca and Mg in green leaves. The specific C content should be considered when assessing C cycling under global nutrient changes. Stage-dependent patterns of leaf stoichiometric homeostasis differed among elements with various chemical characteristics. These findings can help to improve our understanding of plant eco-physiological responses and acclimation under global nutrient changes from the stoichiometric perspective of multiple elements.

The occurrence of parallel speciation strongly implies the action of natural selection. However, it is unclear how general a phenomena parallel speciation is since it was only shown in a small number of animal species. In particular, the adaptive process and mechanisms underlying the process of parallel speciation remain elusive. Here, we used an integrative approach incorporating population genomics, common garden, and crossing experiments to investigate parallel speciation of the wild rice species Oryza nivara from O. rufipogon. We demonstrated that O. nivara originated multiple times from different O. rufipogon populations and revealed that different O. nivara populations have evolved similar phenotypes under divergent selection, a reflection of recurrent local adaptation of ancient O. rufipogon populations to dry habitats. Almost completed premating isolation was detected between O. nivara and O. rufipogon in the absence of any postmating barriers between and within these species. These results suggest that flowering time is a “magic” trait that contributes to both local adaptation and reproductive isolation in the origin of wild rice species. Our study thus demonstrates a convincing case of parallel ecological speciation as a consequence of adaptation to new environments.

Chlorophyll biosynthesis plays essential roles in photosynthesis and plant growth in response to environmental conditions. The accumulation of excess chlorophyll biosynthesis intermediates under light results in the production of reactive oxygen species and oxidative stress. In this study, we identified a rice (Oryza sativa) mutant, oxidation under photoperiod (oxp), that displayed photobleached lesions on its leaves, reduced growth and decreased chlorophyll content during light/dark cycles or following a dark-to-light transition. The oxp mutant accumulated more chlorophyll precursors (5-aminolevulinic acid and protochlorophyllide) than the wild type in the dark, and more singlet oxygen following light exposure. Several singlet-oxygen-responsive genes were greatly upregulated in oxp, whereas the expression patterns of OsPORA and OsPORB, two genes encoding the chlorophyll biosynthesis enzyme NADPH:protochlorop hyllide oxidoreductase, were altered in de-etiolated oxp seedlings. Molecular and complementation studies revealed that oxp is a loss-of-function mutant in LOC_Os01g32730, a homolog of FLUORESCENT (FLU) in Arabidopsis thaliana. Rice PHYTOCHROME-INTERACTING FACTOR-LIKE14 (OsPIL14) transcription factor directly bound to the OsFLU1 promoter and activated its expression. Dark-grown transgenic rice seedlings overexpressing OsPIL14 accumulated more chlorophyll and turned green faster than the wild type upon light illumination. Thus, OsFLU1 is an important regulator of chlorophyll biosynthesis in rice.

According to the less-is-more hypothesis, gene loss is an engine for evolutionary change. Loss-of-function (LoF) mutations resulting in the natural knockout of protein-coding genes not only provide information about gene function but also play important roles in adaptation and phenotypic diversification. Although the less-is-more hypothesis was proposed two decades ago, it remains to be explored on a large scale. In this study, we identified 60,819 LoF variants in 1071 Arabidopsis (Arabidopsis thaliana) genomes and found that 34% of Arabidopsis protein-coding genes annotated in the Columbia-0 genome do not have any LoF variants. We found that nucleotide diversity, transposable element density, and gene family size are strongly correlated with the presence of LoF variants. Intriguingly, 0.9% of LoF variants with minor allele frequency larger than 0.5% are associated with climate change. In addition, in the Yangtze River basin population, 1% of genes with LoF mutations were under positive selection, providing important insights into the contribution of LoF mutations to adaptation. In particular, our results demonstrate that LoF mutations shape diverse phenotypic traits. Overall, our results highlight the importance of the LoF variants for the adaptation and phenotypic diversification of plants.

Reproductive isolation is a prerequisite for speciation. Failure of communication between female tissues of the pistil and paternal pollen tubes imposes hybridization barriers in flowering plants. Arabidopsis thaliana LURE1 (AtLURE1) peptides and their male receptor PRK6 aid attraction of the growing pollen tube to the ovule. Here, we report that the knockout of the entire AtLURE1 gene family did not affect fertility, indicating that AtLURE1-PRK6–mediated signaling is not required for successful fertilization within one Arabidopsis species. AtLURE1s instead function as pollen tube emergence accelerators that favor conspecific pollen over pollen from other species and thus promote reproductive isolation. We also identified maternal peptides XIUQIU1 to -4, which attract pollen tubes regardless of species. Cooperation between ovule attraction and pollen tube growth acceleration favors conspecific fertilization and promotes reproductive isolation.

Rapid phenotypic changes in traits of adaptive significance are crucial for organisms to thrive in changing environments. How such phenotypic variation is achieved rapidly, despite limited genetic variation in species that experience a genetic bottleneck is unknown. Capsella rubella, an annual and inbreeding forb (Brassicaceae), is a great system for studying this basic question. Its distribution is wider than those of its congeneric species, despite an extreme genetic bottleneck event that severely diminished its genetic variation. Here, we demonstrate that transposable elements (TEs) are an important source of genetic variation that could account for its high phenotypic diversity. TEs are (i) highly enriched in C. rubella compared with its outcrossing sister species Capsella grandiflora, and (ii) 4.2% of polymorphic TEs in C. rubella are associated with variation in the expression levels of their adjacent genes. Furthermore, we show that frequent TE insertions at FLOWERING LOCUS C (FLC) in natural populations of C. rubella could explain 12.5% of the natural variation in flowering time, a key life history trait correlated with fitness and adaptation. In particular, we show that a recent TE insertion at the 3′ UTR of FLC affects mRNA stability, which results in reducing its steady-state expression levels, to promote the onset of flowering. Our results highlight that TE insertions can drive rapid phenotypic variation, which could potentially help with adaptation to changing environments in a species with limited standing genetic variation.