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As sessile, photoautotrophic organisms, plants are subjected to fluctuating sunlight that includes potentially detrimental ultraviolet-B radiation (UV-B). Experiments under controlled conditions have shown that the UV-B photoreceptor UV RESISTANCE LOCUS 8 (UVR8) controls acclimation and tolerance to UV-B in Arabidopsis thaliana; however, its long-term impacts on plant fitness remain poorly understood in naturally fluctuating environments. Here we quantified the survival and reproduction of different Arabidopsis mutant genotypes in diverse field and laboratory conditions. We found that uvr8 mutants produced more fruits than wild type when grown in growth chambers under artificial low UV-B conditions but not in natural field conditions, indicating a fitness cost in absence of UV-B stress. Importantly, independent double mutants of UVR8 and the blue-light photoreceptor gene CRYPTOCHROME 1 (CRY1) in two genetic backgrounds showed a drastic reduction in fitness in the field. Experiments with UV-B attenuation experiments in field and with supplemental UV-B in growth chambers demonstrated that UV-B caused the conditional cry1 uvr8 lethality phenotype. Using RNA-seq data of field-grown single and double mutants, we explicitly identified genes showing statistical interaction of UVR8 and CRY1 mutations in the presence of UV-B in the field. They were enriched in Gene Ontology categories related to oxidative stress, photoprotection, and DNA damage repair in addition to UV-B response. Our study demonstrates the functional importance of the UVR8-mediated response across life stages in natura, which is partially redundant with that of cry1. Moreover, these data provide an integral picture of gene expression associated with plant responses under field conditions.

Long-term field monitoring of leaf pigment content is informative for understanding plant responses to environments distinct from regulated chambers but is impractical by conventional destructive measurements. We developed PlantServation, a method incorporating robust image-acquisition hardware and deep learning-based software that extracts leaf color by detecting plant individuals automatically. As a case study, we applied PlantServation to examine environmental and genotypic effects on the pigment anthocyanin content estimated from leaf color. We processed >4 million images of small individuals of four Arabidopsis species in the field, where the plant shape, color, and background vary over months. Past radiation, coldness, and precipitation significantly affected the anthocyanin content. The synthetic allopolyploid A. kamchatica recapitulated the fluctuations of natural polyploids by integrating diploid responses. The data support a long-standing hypothesis stating that allopolyploids can inherit and combine the traits of progenitors. PlantServation facilitates the study of plant responses to complex environments termed “in natura”.

Long-term field monitoring of leaf pigment content is informative for understanding plant responses to environments distinct from regulated chambers but is impractical by conventional destructive measurements. We developed PlantServation, a method incorporating robust image-acquisition hardware and deep learning-based software that extracts leaf color by detecting plant individuals automatically. As a case study, we applied PlantServation to examine environmental and genotypic effects on the pigment anthocyanin content estimated from leaf color. We processed >4 million images of small individuals of four Arabidopsis species in the field, where the plant shape, color, and background vary over months. Past radiation, coldness, and precipitation significantly affected the anthocyanin content. The synthetic allopolyploid A. kamchatica recapitulated the fluctuations of natural polyploids by integrating diploid responses. The data support a long-standing hypothesis stating that allopolyploids can inherit and combine the traits of progenitors. PlantServation facilitates the study of plant responses to complex environments termed "in natura".

Although allopolyploid species are common among natural and crop species, it is not easy to distinguish duplicated genes, known as homeologs, during their genomic analysis. Yet, cost-efficient RNA sequencing (RNA-seq) is to be developed for large-scale transcriptomic studies such as time-series analysis and genome-wide association studies in allopolyploids. In this study, we employed a 3′ RNA-seq utilizing 3′ untranslated regions (UTRs) containing frequent mutations among homeologous genes, compared to coding sequence. Among the 3′ RNA-seq protocols, we examined a low-cost method Lasy-Seq using an allohexaploid bread wheat, Triticum aestivum. HISAT2 showed the best performance for 3′ RNA-seq with the least mapping errors and quick computational time. The number of detected homeologs was further improved by extending 1 kb of the 3′ UTR annotation. Differentially expressed genes in response to mild cold treatment detected by the 3′ RNA-seq were verified with high-coverage conventional RNA-seq, although the latter detected more differentially expressed genes. Finally, downsampling showed that even a 2 million sequencing depth can still detect more than half of expressed homeologs identifiable by the conventional 32 million reads. These data demonstrate that this low-cost 3′ RNA-seq facilitates large-scale transcriptomic studies of allohexaploid wheat and indicate the potential application to other allopolyploid species.

Polyploidization is pervasive in plants, but little is known about the niche divergence of wild allopolyploids (species that harbor polyploid genomes originating from different diploid species) relative to their diploid progenitor species and the gene expression patterns that may underlie such ecological divergence. We conducted a fine-scale empirical study on habitat and gene expression of an allopolyploid and its diploid progenitors. We quantified soil properties and light availability of habitats of an allotetraploid Cardamine flexuosa and its diploid progenitors Cardamine amara and Cardamine hirsuta in two seasons. We analyzed expression patterns of genes and homeologs (homeologous gene copies in allopolyploids) using RNA sequencing. We detected niche divergence between the allopolyploid and its diploid progenitors along water availability gradient at a fine scale: the diploids in opposite extremes and the allopolyploid in a broader range between diploids, with limited overlap with diploids at both ends. Most of the genes whose homeolog expression ratio changed among habitats in C. flexuosa varied spatially and temporally. These findings provide empirical evidence for niche divergence between an allopolyploid and its diploid progenitor species at a fine scale and suggest that divergent expression patterns of homeologs in an allopolyploid may underlie its persistence in diverse habitats.

The timing of germination is a key life-history trait that may strongly influence plant fitness and that sets the stage for selection on traits expressed later in the life cycle. In seasonal environments, the period favourable for germination and the total length of the growing season are limited. The optimal timing of germination may therefore be governed by conflicting selection through survival and fecundity. We conducted a field experiment to examine the effects of timing of germination on survival, fecundity and overall fitness in a natural population of the annual herb Arabidopsis thaliana in north-central Sweden. Seedlings were transplanted at three different times in late summer and in autumn covering the period of seed germination in the study population. Early germination was associated with low seedling survival, but also with high survival and fecundity among established plants. The advantages of germinating early more than balanced the disadvantage and selection favoured early germination. The results suggest that low survival among early germinating seeds is the main force opposing the evolution of earlier germination and that the optimal timing of germination should vary in space and time as a function of the direction and strength of selection acting during different life-history stages.

Herbivore damage can induce the host plant to alter the chemical and physical qualities of its leaves, which is thought to be a plant strategy—termed “induced response”—for avoiding further herbivory. In woody plants, many studies have considered variation in induced response with resource availability, but few studies have examined this variation in relation to growth patterns of woody plants. We studied the phenotypic variability of induced response within successively flushing Quercus serrata seedlings. Q. serrata seedlings were grown under controlled conditions. The controlled factors were herbivore damage (herbivore-damaged and -undamaged) and soil fertility (low and high). At each flush stage, the concentrations of condensed tannin (CT), total phenolics (TP), and nitrogen (N) in leaves were analyzed, and the leaf mass per area (LMA) was measured. CT and TP concentrations in leaves and LMA were higher in herbivore-damaged seedlings. Leaves of the first flushes showed greater sensitivity to herbivore damage and had a higher CT concentration than leaves of the later flushes. Furthermore, seedlings growing in low-fertility soil showed a greater induced response. The results suggest that the induced response of Q. serrata seedlings was related to the contributions of the tissue to current productivity. Leaves of the first flush showed a greater induced response, possibly because they play an important role in subsequent growth. The potential of Q. serrata seedlings to adjust the properties of leaves depending on herbivory and soil fertility in relation to growth patterns may be advantageous on the forest floor, where seedlings grow in soil of heterogeneous fertility and are constantly exposed to herbivory.

Background: The effect of herbivory on plant fitness varies widely. Understanding the causes of this variation is of considerable interest because of its implications for plant population dynamics and trait evolution. We experimentally defoliated the annual herb Arabidopsis thaliana in a natural population in Sweden to test the hypotheses that (a) plant fitness decreases with increasing damage, (b) tolerance to defoliation is lower before flowering than during flowering, and (c) defoliation before flowering reduces number of seeds more strongly than defoliation during flowering, but the opposite is true for effects on seed size. Methodology/Principal Findings: In a first experiment, between 0 and 75% of the leaf area was removed in May from plants that flowered or were about to start flowering. In a second experiment, 0, 25%, or 50% of the leaf area was removed from plants on one of two occasions, in mid April when plants were either in the vegetative rosette or bolting stage, or in mid May when plants were flowering. In the first experiment, seed production was negatively related to leaf area removed, and at the highest damage level, also mean seed size was reduced. In the second experiment, removal of 50% of the leaf area reduced seed production by 60% among plants defoliated early in the season at the vegetative rosettes, and by 22% among plants defoliated early in the season at the bolting stage, but did not reduce seed output of plants defoliated one month later. No seasonal shift in the effect of defoliation on seed size was detected. Conclusions/Significance: The results show that leaf damage may reduce the fitness of A. thaliana, and suggest that in this population leaf herbivores feeding on plants before flowering should exert stronger selection on defence traits than those feeding on plants during flowering, given similar damage levels.