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Polyploids contribute substantially to plant evolution and biodiversity; however, the mechanisms by which they succeed are still unclear. According to the polyploid adaptation hypothesis, successful polyploids spread by repeated adaptive responses to new environments. Here, we tested this hypothesis using two tetraploid yellowcresses (Rorippa), the endemic Rorippa elata and the widespread Rorippa palustris, in the temperate biodiversity hotspot of the Hengduan Mountains. Speciation modes were resolved by phylogenetic modeling using 12 low-copy nuclear loci. Phylogeographical patterns were then examined using haplotypes phased from four plastid and ITS markers, coupled with historical niche reconstruction by ecological niche modeling. We inferred the time of hybrid origins for both species as the mid-Pleistocene, with shared glacial refugia within the southern Hengduan Mountains. Phylogeographic and ecological niche reconstruction indicated recurrent northward colonization by both species after speciation, possibly tracking denuded habitats created by glacial retreat during interglacial periods. Common garden experiment involving perennial R. elata conducted over two years revealed significant changes in fitness-related traits across source latitudes or altitudes, including latitudinal increases in survival rate and compactness of plant architecture, suggesting gradual adaptation during range expansion. These findings support the polyploid adaptation hypothesis and suggest that the spread of polyploids was aided by adaptive responses to environmental changes during the Pleistocene. Our results thus provide insight into the evolutionary success of polyploids in high-altitude environments.

Abstract Background Genomic variation is widespread, and both neutral and selective processes can generate similar patterns in the genome. These processes are not mutually exclusive, so it is difficult to infer the evolutionary mechanisms that govern population and species divergence. Boechera stricta is a perennial relative of Arabidopsis thaliana native to largely undisturbed habitats with two geographic and ecologically divergent subspecies. Here, we delineate the evolutionary processes driving the genetic diversity and population differentiation in this species. Results Using whole-genome re-sequencing data from 517 B. stricta accessions, we identify four genetic groups that diverged around 30–180 thousand years ago, with long-term small effective population sizes and recent population expansion after the Last Glacial Maximum. We find three genomic regions with elevated nucleotide diversity, totaling about 10% of the genome. These three regions of elevated nucleotide diversity show excess of intermediate-frequency alleles, higher absolute divergence (d XY ), and lower relative divergence (F ST ) than genomic background, and significant enrichment in immune-related genes, reflecting long-term balancing selection. Scattered across the genome, we also find regions with both high F ST and d XY among the groups, termed F ST -islands. Population genetic signatures indicate that F ST -islands with elevated divergence, which have experienced directional selection, are derived from divergent sorting of ancient polymorphisms. Conclusions Our results suggest that long-term balancing selection on disease resistance genes may have maintained ancestral haplotypes across different geographical lineages, and unequal sorting of balanced polymorphisms may have generated genomic regions with elevated divergence. This study highlights the importance of ancestral balanced polymorphisms as crucial components of genome-wide variation.

The mustard family (Brassicaceae) comprises several dozen monophyletic clades usually ranked as tribes. The tribe Boechereae plays a prominent role in plant research due to the incidence of apomixis and its close relationship to Arabidopsis. This tribe, largely confined to western North America, harbors nine genera and c. 130 species, with >90% of species belonging to the genus Boechera. Hundreds of apomictic diploid and triploid Boechera hybrids have spurred interest in this genus, but the remaining Boechereae genomes remain virtually unstudied. Here we report on comparative genome structure of six genera (Borodinia, Cusickiella, Phoenicaulis, Polyctenium, Nevada, and Sandbergia) and three Boechera species as revealed by comparative chromosome painting (CCP). All analyzed taxa shared the same seven-chromosome genome structure. Comparisons with the sister Halimolobeae tribe (n = 8) showed that the ancestral Boechereae genome (n = 7) was derived from an older n = 8 genome by descending dysploidy followed by the divergence of extant Boechereae taxa. As tribal divergence post-dated the origin of four tribe-specific chromosomes, it is proposed that these chromosomal rearrangements were a key evolutionary innovation underlaying the origin and diversification of the Boechereae in North America. Although most Boechereae genera exhibit genomic conservatism, intra-tribal cladogenesis has occasionally been accompanied by chromosomal rearrangements (particularly inversions). Recently, apomixis was reported in the Boechereae genera Borodinia and Phoenicaulis. Here, we report sexual reproduction in diploid Nevada, diploid Sandbergia, and tetraploid Cusickiella and aposporous apomixis in tetraploids of Polyctenium and Sandbergia. In sum, apomixis is now known to occur in five of the nine Boechereae genera.

Abstract Background Traditional rice (Oryza sativa) varieties are valuable resources for the improvement of drought resistance. qDTY 3.2 is a drought-yield quantitative trait locus that was identified in a population derived from the traditional variety Moroberekan and the drought-susceptible variety Swarna. In this study, our aim was to characterize the physiological mechanisms associated with qDTY 3.2 . Our approach was to phenotype fifteen BC2F3:4 lines for shoot and root drought resistance-related traits as compared to Swarna in the field under well-watered and drought stress conditions. Four BC2F3:4 lines contrasting for yield under drought were selected for detailed characterization of shoot morphology, water use related traits, flowering time and root system architecture in the field as well as in controlled environments (lysimeters in a greenhouse, and gel imaging platform in a growth chamber). Results Across five field experiments, grain yield correlated significantly with root growth along the soil profile, flowering time, and canopy temperature under drought conditions. The four selected BC2F3:4 lines showed earlier flowering time, reduced distribution of root growth to shallow soil layers which resulted in lower water uptake (between 0 and 30 cm) and drought-induced increased distribution of root growth to deep soil layers (between 30 and 60 cm) as compared to Swarna in the field. Root system architecture phenotypes were confirmed in whole root systems in lysimeters, and corresponded to higher numbers of root tips in a gel imaging platform, highlighting the potential stability of some root traits across different growth stages and systems. Conclusions We conclude that earlier flowering time, reduced shallow root growth, and drought-induced increased deep root growth are associated with the presence of qDTY 3.2 since these phenotypes were consistently observed in the selected QTL lines with full introgression of qDTY 3.2 . We hypothesize that the qDTY 3.2 associated RSA phenotypes led to better use of water and metabolic resources which, combined with earlier flowering time, improved yield under drought.

Abstract Balancing selection maintains variation for evolution. A recent study investigated the extent of balancing selection in two Brassicaceae species and highlighted its importance for adaptation.

Laboratory-based studies of the effect of plant genotype on plant microbiome composition often do not consider the influence of environmental heterogeneity. Here, Wagner et al. use a large-scale field experiment to assess the extent of host genetic and environmental factors on the microbiome of Boechera stricta.

Differences in the timing of vegetative-to-reproductive phase transition have evolved independently and repeatedly in different plant species. Due to their specific biological functions and positions in pathways, some genes are important targets of repeated evolution – independent mutations on these genes caused the evolution of similar phenotypes in distantly related organisms. While many studies have investigated these genes, it remains unclear how gene duplications influence repeated phenotypic evolution. Here we characterized the genetic architecture underlying a novel rapid-flowering phenotype in Boechera stricta and investigated the candidate genes BsFLC1 and BsFLC2. The expression patterns of BsFLC1 suggested its function in flowering time suppression, and the deletion of BsFLC1 is associated with rapid flowering and loss of vernalization requirement. In contrast, BsFLC2 did not appear to be associated with flowering and had accumulated multiple amino acid substitutions in the relatively short evolutionary timeframe after gene duplication. These non-synonymous substitutions greatly changed the physicochemical properties of the original amino acids, concentrated non-randomly near a protein-interacting domain, and had greater substitution rate than synonymous changes. Here we suggested that, after recent gene duplication of the FLC gene, the evolution of rapid phenology was made possible by the change of BsFLC2 expression pattern or protein sequences and the deletion of BsFLC1.

Plants employ highly variable chemical defenses against a broad community of herbivores, which vary in their susceptibilities to specific compounds. Variation in chemical defenses within the plant has been found in many species; the ecological and evolutionary influences on this variation, however, are less well-understood. One central theory describing the allocation of defenses in the plant is the Optimal Defense Hypothesis (ODH), which predicts that defenses will be concentrated in tissues that are of high fitness value to the plant. Although the ODH has been repeatedly supported within vegetative tissues, few studies have compared vegetative and reproductive tissues, and the results have not been conclusive. We quantified variation in glucosinolate profile and tissue value between vegetative and reproductive tissues in Boechera stricta, a close relative of Arabidopsis. B. stricta manufactures glucosinolates, a set of defensive compounds that vary genetically and are straightforward to quantify. Genetic diversity in glucosinolate profile has been previously demonstrated to be important to both herbivory and fitness in B. stricta; however, the importance of glucosinolate variation among tissues has not. Here, we investigate whether allocation of glucosinolates within the plant is consistent with the ODH. We used both clipping experiments on endogenous plants and ambient herbivory in a large-scale transplant experiment at three sites to quantify fitness effects of loss of rosette leaves, cauline leaves, and flowers and fruits. We measured glucosinolate concentration in leaves and fruits in the transplant experiment, and asked whether more valuable tissues were more defended. We also investigated within-plant variation in other aspects of the glucosinolate profile. Our results indicated that damage to fruits had a significantly larger effect on overall fitness than damage to leaves, and that fruits had much higher concentrations of glucosinolates, supporting the ODH. This is, to the best of our knowledge, the first study to explicitly compare both tissue value and chemical defense concentrations between vegetative and reproductive tissues under natural conditions.

Following publication of the original article [1], the authors reported that the Availability of data and materials section required updating. The updated text reads as follows:

African rice gall midge (AfRGM) is one of the most destructive pests of irrigated and lowland African ecologies. This study aimed to identify the quantitative trait loci (QTL) associated with AfRGM pest incidence and resistance in three independent bi-parental rice populations (ITA306xBW348-1, ITA306xTOG7106 and ITA306xTOS14519), and to conduct meta QTL (mQTL) analysis to explore whether any genomic regions are conserved across different genetic backgrounds. Composite interval mapping (CIM) conducted on the three populations independently uncovered a total of 28 QTLs associated with pest incidence (12) and pest severity (16). The number of QTLs per population associated with AfRGM resistance varied from three in the ITA306xBW348-1 population to eight in the ITA306xTOG7106 population. Each QTL individually explained 1.3 to 34.1% of the phenotypic variance. The major genomic region for AfRGM resistance had a LOD score and R2 of 60.0 and 34.1% respectively, and mapped at 111 cM on chromosome 4 (qAfrGM4) in the ITA306xTOS14519 population. The meta-analysis reduced the number of QTLs from 28 to 17 mQTLs, each explaining 1.3 to 24.5% of phenotypic variance, and narrowed the confidence intervals by 2.2 cM. There was only one minor effect mQTL on chromosome 1 that was common in the TOS14519 and TOG7106 genetic backgrounds; all other mQTLs were background specific. We are currently fine-mapping and validating the major effect genomic region on chromosome 4 (qAfRGM4). This is the first report in mapping the genomic regions associated with the AfRGM resistance, and will be highly useful for rice breeders.

Coalescent theory is a powerful tool for population geneticists as well as molecular biologists interested in understanding the patterns and levels of DNA variation. Using coalescent Monte Carlo simulations it is possible to obtain the empirical distributions for a number of statistics across a wide range of evolutionary models; these distributions can be used to test evolutionary hypotheses using experimental data. The mlcoalsim application presented here (based on a version of the ms program, Hudson, 2002) adds important new features to improve methodology (uncertainty and conditional methods for mutation and recombination), models (including strong positive selection, finite sites and heterogeneity in mutation and recombination rates) and analyses (calculating a number of statistics used in population genetics and P-values for observed data). One of the most important features of mlcoalsim is the analysis of multilocus data in linked and independent regions. In summary, mlcoalsim is an integrated software application aimed at researchers interested in molecular evolution. mlcoalsim is written in ANSI C and is available at: http://www.ub.es/softevol/mlcoalsim.

Natural populations exhibit substantial variation in quantitative traits. A quantitative trait is typically defined by its mean and variance, and to date most genetic mapping studies focus on loci altering trait means but not (co)variances. For single traits, the control of trait variance across genetic backgrounds is referred to as genetic canalization. With multiple traits, the genetic covariance among different traits in the same environment indicates the magnitude of potential genetic constraint, while genotype-by-environment interaction (GxE) concerns the same trait across different environments. While some have suggested that these three attributes of quantitative traits are different views of similar concepts, it is not yet clear, however, whether they have the same underlying genetic mechanism. Here, we detect quantitative trait loci (QTL) influencing the (co)variance of phenological traits in six distinct environments in Boechera stricta, a close relative of Arabidopsis. We identified nFT as the QTL altering the magnitude of phenological trait canalization, genetic constraint, and GxE. Both the magnitude and direction of nFT's canalization effects depend on the environment, and to our knowledge, this reversibility of canalization across environments has not been reported previously. nFT's effects on trait covariance structure (genetic constraint and GxE) likely result from the variable and reversible canalization effects across different traits and environments, which can be explained by the interaction among nFT, genomic backgrounds, and environmental stimuli. This view is supported by experiments demonstrating significant nFT by genomic background epistatic interactions affecting phenological traits and expression of the candidate gene, FT. In contrast to the well-known canalization gene Hsp90, the case of nFT may exemplify an alternative mechanism: Our results suggest that (at least in traits with major signal integrators such as flowering time) genetic canalization, genetic constraint, and GxE may have related genetic mechanisms resulting from interactions among major QTL, genomic backgrounds, and environments.

Demography impacts the observed standing level of genetic diversity present in populations. Distinguishing the relative impacts of demography from selection requires a baseline of expressed gene variation in naturally occurring populations. Six nuclear genes were sequenced to estimate the patterns and levels of genetic diversity in natural Arabidopsis lyrata subsp. petraea populations that differ in demographic histories since the Pleistocene. As expected, northern European populations have genetic signatures of a strong population bottleneck likely due to glaciation during the Pleistocene. Levels of diversity in the northern populations are about half of that in central European populations. Bayesian estimates of historical population size changes indicate that central European populations also have signatures of population size change since the last glacial maxima, suggesting that these populations are not as stable as previously thought. Time since divergence amongst northern European populations is higher than amongst central European populations, suggesting that the northern European populations were established before the Pleistocene and survived glaciation in small separated refugia. Estimates of demography based on expressed genes are complementary to estimates based on microsatellites and transposable elements, elucidating temporal shifts in population dynamics and confirming the importance of marker selection for tests of demography.

In Arabidopsis thaliana and other crucifers, the glucosinolate-myrosinase system contributes to resistance against herbivory by generalist insects. As yet, it is unclear how crucifers defend themselves against crucifer-specialist insect herbivores.We analyzed natural variation for resistance against two crucifer specialist lepidopteran herbivores, Pieris brassicae and Plutella xylostella, among Arabidopsis thaliana accessions and in a new Arabidopsis recombinant inbred line (RIL) population generated from the parental accessions Da(1)-12 and Ei-2. This RIL population consists of 201 individual F(8) lines genotyped with 84 PCR-based markers. We identified six QTL for resistance against Pieris herbivory, but found only one weak QTL for Plutella resistance. To elucidate potential factors causing these resistance QTL, we investigated leaf hair (trichome) density, glucosinolates and myrosinase activity, traits known to influence herbivory by generalist insects. We identified several previously unknown QTL for these traits, some of which display a complex pattern of epistatic interactions.Although some trichome, glucosinolate or myrosinase QTL co-localize with Pieris QTL, none of these traits explained the resistance QTL convincingly, indicating that resistance against specialist insect herbivores is influenced by other traits than resistance against generalists.

BACKGROUND: Plants defend themselves against herbivorous insects, utilizing both constitutive and inducible defenses. Induced defenses are controlled by several phytohormone-mediated signaling pathways. Here, we analyze transcriptional changes in the North American Arabidopsis relative Boechera divaricarpa in response to larval herbivory by the crucifer specialist lepidopteran Plutella xylostella (diamondback moth) and by the generalist lepidopteran Trichoplusia ni (cabbage semilooper), and compare them to wounding and exogenous phytohormone application. METHODOLOGY/PRINCIPAL FINDINGS: We use a custom macroarray constructed from B. divaricarpa herbivory-regulated cDNAs identified by suppression subtractive hybridization and from known stress-responsive A. thaliana genes for transcript profiling after insect herbivory, wounding and in response to jasmonate, salicylate and ethylene. In addition, we introduce path analysis as a novel approach to analyze transcript profiles. Path analyses reveal that transcriptional responses to the crucifer specialist P. xylostella are primarily determined by direct effects of the ethylene and salicylate pathways, whereas responses to the generalist T. ni are influenced by the ethylene and jasmonate pathways. Wound-induced transcriptional changes are influenced by all three pathways, with jasmonate having the strongest effect. CONCLUSIONS/SIGNIFICANCE: Our results show that insect herbivory is distinct from simple mechanical plant damage, and that different lepidopteran herbivores elicit different transcriptional responses.