The future of cold‐adapted plants in changing climates: Micranthes (Saxifragaceae) as a case study

Research has shown species undergoing range contractions and/or northward and higher elevational movements as a result of changing climates. Here, we evaluate how the distribution of a group of cold‐adapted plant species with similar evolutionary histories changes in response to warming climates. We selected 29 species of Micranthes (Saxifragaceae) representing the mountain and Arctic biomes of the Northern Hemisphere. For this analysis, 24,755 data points were input into ecological niche models to assess both present fundamental niches and predicted future ranges under climate change scenarios. Comparisons were made across the Northern Hemisphere between all cold‐adapted Micranthes, including Arctic species, montane species, and species defined as narrow endemics. Under future climate change models, 72% of the species would occupy smaller geographical areas than at present. This loss of habitat is most pronounced in Arctic species in general, but is also prevalent in species restricted to higher elevations in mountains. Additionally, narrowly endemic species restricted to high elevations were more susceptible to habitat loss than those species found at lower elevations. Using a large dataset and modeling habitat suitability at a global scale, our results empirically model the threats to cold‐adapted species as a result of warming climates. Although Arctic and alpine biomes share many underlying climate similarities, such as cold and short growing seasons, our results confirm that species in these climates have varied responses to climate change and that key abiotic variables differ between these two habitats.     

Environmental systems biology of cold‐tolerant phenotype in Saccharomyces species adapted to grow at different temperatures

Temperature is one of the leading factors that drive adaptation of organisms and ecosystems. Remarkably, many closely related species share the same habitat because of their different temporal or micro‐spatial thermal adaptation. In this study, we seek to find the underlying molecular mechanisms of the cold‐tolerant phenotype of closely related yeast species adapted to grow at different temperatures, namely S. kudriavzevii CA111 (cryo‐tolerant) and S. cerevisiae 96.2 (thermo‐tolerant). Using two different systems approaches, i. thermodynamic‐based analysis of a genome‐scale metabolic model of S. cerevisiae and ii. large‐scale competition experiment of the yeast heterozygote mutant collection, genes and pathways important for the growth at low temperature were identified. In particular, defects in lipid metabolism, oxidoreductase and vitamin pathways affected yeast fitness at cold. Combining the data from both studies, a list of candidate genes was generated and mutants for two predicted cold‐favouring genes, GUT2 and ADH3, were created in two natural isolates. Compared with the parental strains, these mutants showed lower fitness at cold temperatures, with S. kudriavzevii displaying the strongest defect. Strikingly, in S. kudriavzevii, these mutations also significantly improve the growth at warm temperatures. In addition, overexpression of ADH3 in S. cerevisiae increased its fitness at cold. These results suggest that temperature‐induced redox imbalances could be compensated by increased glycerol accumulation or production of cytosolic acetaldehyde through the deletion of GUT2 or ADH3, respectively.     

Evaluating Tripsacum‐introgressed maize germplasm after infestation with western corn rootworms (Coleoptera: Chrysomelidae)

Maize (Zea mays L.) is a valuable commodity throughout the world, but corn rootworms (Chrysomelidae: Diabrotica spp.) often cause economic damage and increase production costs. Current rootworm management strategies have limitations, and in order to create viable management alternatives, researchers have been developing novel maize lines using Eastern gamagrass (Tripsacum dactyloides L.) germplasm, a wild relative of maize that is resistant to rootworms. Ten maize Tripsacum‐introgressed inbred lines derived from recurrent selection of crosses with gamagrass and teosinte (Zea diploperennis Iltis) recombinants and two public inbred lines were assessed for susceptibility to western corn rootworm (Diabrotica virgifera virgifera LeConte) and yield in a two‐year field study. Two experimental maize inbred lines, SDG11 and SDG20, had mean root damage ratings that were significantly lower than the susceptible public line B73. Two other experimental maize inbred lines, SDG12 and SDG6, appeared tolerant to rootworm damage because they exhibited yield increases after rootworm infestation in both years. In the majority of cases, mean yield per plant of experimental maize lines used in yield analyses was equal to or exceeded that of the public inbred lines B73 and W64A. Our study indicates that there is potential to use Tripsacum‐introgressed maize germplasm in breeding programs to enhance plant resistance and/or tolerance to corn rootworms, although further research on insect resistance and agronomic potential of this germplasm needs to be conducted in F₁ hybrids.     

Cross‐protective effect of acid‐adapted Salmonella enterica on resistance to lethal acid and cold stress conditions

Aims: To evaluate the cross‐protected Salmonella enterica cells under acid and cold stress conditions. Methods and Results: The acid‐adapted S. enterica cells were exposed to pH 4·0 at 4 and 20°C. Recovery of sublethally injured cells was estimated by the difference between the counts obtained on trypticase soy agar (TSA) and xylose lysine desoxycholate (XLD) agar. The survival curves of nonadapted and acid‐adapted S. enterica cells at pH 4·0 were fitted with Weibull distribution model. The recovery behaviour of injured S. enterica cells was estimated by the modified Gompertz parameters. Acid‐adapted S. enterica were more resistant to subsequent acid shock than the nonadapted cells. The numbers of nonadapted S. enterica cells were decreased by 4·57 and 7·55 log CFU ml^?1 at 4 and 20°C after 12‐day acid challenge, respectively. The acid adaptation induced cross‐protection and viable nonculturable (VBNC) state against low acid and cold stresses. The 7‐h adaptation showed the least recovery of injured cells. Conclusion: The results suggest that acid‐adapted S. enterica cells induced acid tolerance response and VBNC state. Significance and Impact of the Study: These results provide useful information for understanding the induction of cross‐protected and VBNC pathogens under various stresses, which might be needed in designing new food preservation strategies.     

A large-scale screen for artificial selection in maize identifies candidate agronomic loci for domestication and crop improvement

Maize (Zea mays subsp mays) was domesticated from teosinte (Z. mays subsp parviglumis) through a single domestication event in southern Mexico between 6000 and 9000 years ago. This domestication event resulted in the original maize landrace varieties, which were spread throughout the Americas by Native Americans and adapted to a wide range of environmental conditions. Starting with landraces, 20th century plant breeders selected inbred lines of maize for use in hybrid maize production. Both domestication and crop improvement involved selection of specific alleles at genes controlling key morphological and agronomic traits, resulting in reduced genetic diversity relative to unselected genes. Here, we sequenced 1095 maize genes from a sample of 14 inbred lines and chose 35 genes with zero sequence diversity as potential targets of selection. These 35 genes were then sequenced in a sample of diverse maize landraces and teosintes and tested for selection. Using two statistical tests, we identified eight candidate genes. Extended gene sequencing of these eight candidate loci confirmed that six were selected throughout the gene, and the remaining two exhibited evidence of selection in the 3' portion of each gene. The selected genes have functions consistent with agronomic selection for nutritional quality, maturity, and productivity. Our large-scale screen for artificial selection allows identification of genes of potential agronomic importance even when gene function and the phenotype of interest are unknown.     

Negative frequency‐dependent selection maintains coexisting genotypes during fluctuating selection

Natural environments are rarely static; rather selection can fluctuate on timescales ranging from hours to centuries. However, it is unclear how adaptation to fluctuating environments differs from adaptation to constant environments at the genetic level. For bacteria, one key axis of environmental variation is selection for planktonic or biofilm modes of growth. We conducted an evolution experiment with Burkholderia cenocepacia, comparing the evolutionary dynamics of populations evolving under constant selection for either biofilm formation or planktonic growth with populations in which selection fluctuated between the two environments on a weekly basis. Populations evolved in the fluctuating environment shared many of the same genetic targets of selection as those evolved in constant biofilm selection, but were genetically distinct from the constant planktonic populations. In the fluctuating environment, mutations in the biofilm‐regulating genes wspA and rpfR rose to high frequency in all replicate populations. A mutation in wspA first rose rapidly and nearly fixed during the initial biofilm phase but was subsequently displaced by a collection of rpfR mutants upon the shift to the planktonic phase. The wspA and rpfR genotypes coexisted via negative frequency‐dependent selection around an equilibrium frequency that shifted between the environments. The maintenance of coexisting genotypes in the fluctuating environment was unexpected. Under temporally fluctuating environments, coexistence of two genotypes is only predicted under a narrow range of conditions, but the frequency‐dependent interactions we observed provide a mechanism that can increase the likelihood of coexistence in fluctuating environments.     

Genome‐wide analysis reveals artificial selection on coat colour and reproductive traits in Chinese domestic pigs

Pigs from Asia and Europe were independently domesticated from c. 9000 years ago. During this period, strong artificial selection has led to dramatic phenotypic changes in domestic pigs. However, the genetic basis underlying these morphological and behavioural adaptations is relatively unknown, particularly for indigenous Chinese pigs. Here, we performed a genome‐wide analysis to screen 196 regions with selective sweep signals in Tongcheng pigs, which are a typical indigenous Chinese breed. Genes located in these regions have been found to be involved in lipid metabolism, melanocyte differentiation, neural development and other biological processes, which coincide with the evolutionary phenotypic changes in this breed. A synonymous substitution, c.669T>C, in ESR1, which colocalizes with a major quantitative trait locus for litter size, shows extreme differences in allele frequency between Tongcheng pigs and wild boars. Notably, the variant C allele in this locus exhibits high allele frequency in most Chinese populations, suggesting a consequence of positive selection. Five genes (PRM1, PRM2, TNP2, GPR149 and JMJD1C) related to reproductive traits were found to have high haplotype similarity in Chinese breeds. Two selected genes, MITF and EDNRB, are implied to shape the two‐end black colour trait in Tongcheng pig. Subsequent SNP microarray studies of five Chinese white‐spotted breeds displayed a concordant signature at both loci, suggesting that these two genes are responsible for colour variations in Chinese breeds. Utilizing massively parallel sequencing, we characterized the candidate sites that adapt to artificial and environmental selections during the Chinese pig domestication. This study provides fundamental proof for further research on the evolutionary adaptation of Chinese pigs.     

Plant defense against fall armyworm in micro‐sympatric maize (Zea mays ssp. mays) and Balsas teosinte (Zea mays ssp. parviglumis)

Maize [Zea mays L. ssp. mays (Poaceae)] was domesticated from Balsas teosinte (Zea mays ssp. parviglumis Iltis & Doebley) in present‐day Mexico. Fall armyworm, Spodoptera frugiperda JE Smith (Lepidoptera: Noctuidae), is among the most important pests of maize in Mexico and Central America. We compared the strength of plant defenses against fall armyworm between micro‐sympatric landrace maize and Balsas teosinte in the field and laboratory. The field comparison, conducted in Mexico, consisted of comparing the frequency of fall armyworm infestation between young maize and Balsas teosinte plants in dryland agricultural fields in which Balsas teosinte grew as a weed. The laboratory comparison contrasted the performance of fall armyworm larvae provided a diet of leaf tissue excised from maize or Balsas teosinte plants that were intact or had been primed by larval feeding. In the field, maize plants were more frequently infested with fall armyworm than Balsas teosinte plants: over 3 years and three fields, maize was infested at a ca. 1.8‐fold greater rate than Balsas teosinte. In the laboratory, larval growth, but not survivorship, was differently affected by feeding on maize vs. Balsas teosinte, and on primed vs. intact plants. Specifically, survivorship was ca. 98%, and did not differ between maize and Balsas teosinte, nor between primed and intact plants. Larvae grew less on intact vs. primed maize, and similarly on intact vs. primed Balsas teosinte; overall, growth was 1.2‐fold greater on maize compared to Balsas teosinte, and on primed compared to intact plants. Parallel observations showed that the differences in growth could not be attributed to the amount of leaf tissue consumed by larvae. We discuss our results in relation to differences in the strength of plant defenses between crops and their ancestors, the relevance of unmanaged Balsas teosinte introgression in the context of fall armyworm defenses in maize, and whether greater growth of larvae on primed vs. intact plants signifies herbivore offense.     

Adaptive phenotypic divergence in an annual grass differs across biotic contexts*

Climate is a powerful force shaping adaptation within species, yet adaptation to climate occurs against a biotic background: species interactions can filter fitness consequences of genetic variation by altering phenotypic expression of genotypes. We investigated this process using populations of teosinte, a wild annual grass related to maize (Zea mays ssp. mexicana), sampling plants from 10 sites along an elevational gradient as well as rhizosphere biota from three of those sites. We grew half‐sibling teosinte families in each biota to test whether trait divergence among teosinte populations reflects adaptation or drift, and whether rhizosphere biota affect expression of diverged traits. We further assayed the influence of rhizosphere biota on contemporary additive genetic variation. We found that adaptation across environment shaped divergence of some traits, particularly flowering time and root biomass. We also observed that different rhizosphere biota shifted expressed values of these traits within teosinte populations and families and altered within‐population genetic variance and covariance. In sum, our results imply that changes in trait expression and covariance elicited by rhizosphere communities could have played a historical role in teosinte adaptation to environments and that they are likely to play a role in the response to future selection.     

Genome-wide association study and scan for signatures of selection point to candidate genes for body temperature maintenance under the cold stress in Siberian cattle populations

Background

Design of new highly productive livestock breeds, well-adapted to local climatic conditions is one of the aims of modern agriculture and breeding. The genetics underlying economically important traits in cattle are widely studied, whereas our knowledge of the genetic mechanisms of adaptation to local environments is still scarce. To address this issue for cold climates we used an integrated approach for detecting genomic intervals related to body temperature maintenance under acute cold stress. Our approach combined genome-wide association studies (GWAS) and scans for signatures of selection applied to a cattle population (Hereford and Kazakh Whiteheaded beef breeds) bred in Siberia. We utilized the GGP HD150K DNA chip containing 139,376 single nucleotide polymorphism markers.

Results

We detected a single candidate region on cattle chromosome (BTA)15 overlapping between the GWAS results and the results of scans for selective sweeps. This region contains two genes, MSANTD4 and GRIA4. Both genes are functional candidates to contribute to the cold-stress resistance phenotype, due to their indirect involvement in the cold shock response (MSANTD4) and body thermoregulation (GRIA4).

Conclusions

Our results point to a novel region on BTA15 which is a candidate region associated with the body temperature maintenance phenotype in Siberian cattle. The results of our research and the follow up studies might be used for the development of cattle breeds better adapted to cold climates of the Russian Federation and other Northern countries with similar climates.

     

Genomewide signatures of selection in Epichloë reveal candidate genes for host specialization

Host specialization is a key process in ecological divergence and speciation of plant‐associated fungi. The underlying determinants of host specialization are generally poorly understood, especially in endophytes, which constitute one of the most abundant components of the plant microbiome. We addressed the genetic basis of host specialization in two sympatric subspecies of grass‐endophytic fungi from the Epichloë typhina complex: subsp. typhina and clarkii. The life cycle of these fungi entails unrestricted dispersal of gametes and sexual reproduction before infection of a new host, implying that the host imposes a selective barrier on viability of the progeny. We aimed to detect genes under divergent selection between subspecies, experiencing restricted gene flow due to adaptation to different hosts. Using pooled whole‐genome sequencing data, we combined F_ST and D_XY population statistics in genome scans and detected 57 outlier genes showing strong differentiation between the two subspecies. Genomewide analyses of nucleotide diversity (π), Tajima's D and dN/dS ratios indicated that these genes have evolved under positive selection. Genes encoding secreted proteins were enriched among the genes showing evidence of positive selection, suggesting that molecular plant–fungus interactions are strong drivers of endophyte divergence. We focused on five genes encoding secreted proteins, which were further sequenced in 28 additional isolates collected across Europe to assess genetic variation in a larger sample size. Signature of positive selection in these isolates and putative identification of pathogenic function supports our findings that these genes represent strong candidates for host specialization determinants in Epichloë endophytes. Our results highlight the role of secreted proteins as key determinants of host specialization.     

The Y-segment of novel cold dehydrin genes is conserved and codons in the PR-10 genes are under positive selection in Oxytropis (Fabaceae) from contrasting climates

While the arctic flora is particularly threatened by climate changes, the molecular aspects allowing colonization of this harsh environment remain largely enigmatic. Genes with a likely functional or evolutive role for arctic Oxytropis (Fabaceae) were previously discovered given a sharp differential expression between arctic and temperate species, but the evolutionary forces in action were unknown within the respective species. Here, we analyze gene duplication patterns and positive and negative selection between genes from species of contrasting environments, which can reveal potential gene functions. Genes were amplified and sequenced from two arctic (Oxytropis arctobia and O. maydelliana) and two temperate (O. campestris subsp. johannensis and O. splendens) species. Detection of codons under positive or negative selection and phylogenetic analyses were used to further elucidate pathogenesis-related class 10 (PR-10), ripening-related proteins, cold dehydrins gene families and light-harvesting complex (lhcaIII and lhcbI) genes from Oxytropis. Overall, results showed that the three gene families duplicated in tandem prior to the Oxytropis genus diversification; that genes overexpressed in arctic species evolve under higher constraints at the sequence level in these species; that evolving novel protein variants in PR-10 genes were required for initial adaptation to the Arctic, and that Oxytropis cold dehydrins are of a novel (K-like–Y₄–K–S) structure, where the Y-segment is under stringent evolutive constraints in the arctic species. This suggests a scenario not previously described for arctic plants, where tandem duplications precede gene recruitment that later become both highly expressed and under stringent constraints in the arctic species.     

Genomic screening for artificial selection during domestication and improvement in maize

BACKGROUND: Artificial selection results in phenotypic evolution. Maize (Zea mays L. ssp. mays) was domesticated from its wild progenitor teosinte (Zea mays subspecies parviglumis) through a single domestication event in southern Mexico between 6000 and 9000 years ago. This domestication event resulted in the original maize landrace varieties. The landraces provided the genetic material for modern plant breeders to select improved varieties and inbred lines by enhancing traits controlling agricultural productivity and performance. Artificial selection during domestication and crop improvement involved selection of specific alleles at genes controlling key morphological and agronomic traits, resulting in reduced genetic diversity relative to unselected genes. SCOPE: This review is a summary of research on the identification and characterization by population genetics approaches of genes affected by artificial selection in maize. CONCLUSIONS: Analysis of DNA sequence diversity at a large number of genes in a sample of teosintes and maize inbred lines indicated that approx. 2 % of maize genes exhibit evidence of artificial selection. The remaining genes give evidence of a population bottleneck associated with domestication and crop improvement. In a second study to efficiently identify selected genes, the genes with zero sequence diversity in maize inbreds were chosen as potential targets of selection and sequenced in diverse maize landraces and teosintes, resulting in about half of candidate genes exhibiting evidence for artificial selection. Extended gene sequencing demonstrated a low false-positive rate in the approach. The selected genes have functions consistent with agronomic selection for plant growth, nutritional quality and maturity. Large-scale screening for artificial selection allows identification of genes of potential agronomic importance even when gene function and the phenotype of interest are unknown. These approaches should also be applicable to other domesticated species if specific demographic conditions during domestication exist.     

A genome scan of diversifying selection in Ophiocordyceps zombie‐ant fungi suggests a role for enterotoxins in co‐evolution and host specificity

Identification of the genes underlying adaptation sheds light on the biological functions targeted by natural selection. Searches for footprints of positive selection, in the form of rapid amino acid substitutions, and the identification of species‐specific genes have proved to be powerful approaches to identifying the genes involved in host specialization in plant‐pathogenic fungi. We used an evolutionary comparative genomic approach to identify genes underlying host adaptation in the ant‐infecting genus Ophiocordyceps, which manipulates ant behaviour. A comparison of the predicted genes in the genomes of species from three species complexes—O. unilateralis, O. australis and O. subramanianii—revealed an enrichment in pathogenesis‐associated functions, including heat‐labile enterotoxins, among species‐specific genes. Furthermore, these genes were overrepresented among those displaying significant footprints of positive selection. Other categories of genes suspected to be important for virulence and pathogenicity in entomopathogenic fungi (e.g., chitinases, lipases, proteases, core secondary metabolism genes) were much less represented, although a few candidate genes were found to evolve under positive selection. An analysis including orthologs from other entomopathogenic fungi in a broader context showed that positive selection on enterotoxins was specific to the ant‐infecting genus Ophiocordyceps. Together with previous studies reporting the overexpression of an enterotoxin during behavioural manipulation in diseased ants, our findings suggest that heat‐labile enterotoxins are important effectors in host adaptation and co‐evolution in the Ophiocordyceps entomopathogenic fungi.