- We used whole genome sequencing combined with association study of climate to discover the drivers of differentiation in the perennial C4 grass Panicum hallii.. - Results: Sequencing of 89 natural accessions of P.hallii revealed complex population structure across the species range. - Major population genomic separation was found between subspecies P.hallii var. - Conclusions: Both geography and climate adaptation contribute significantly to patterns of genome-wide variation in P.hallii. - Population subgroups within P.hallii may represent early stages in the formation of ecotypes. - While general patterns in the partitioning of plant species across space is well established for many species, an understanding of the extent to which different ecotypes overlap in their ranges and the distribution of locally adapted alleles across those groups is just beginning to emerge [7]. - Hall’s panicgrass, Panicum hallii Vasey, is a perennial C4 grass and a member of the Panicoid grasses, which includes sorghum, maize, and sugarcane [9]. - Full list of author information is available at the end of the article. - 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0. - hallii) and P.hallii var. - hallii is typically found in drier habitats across the range of the species, which stretches from Arizona to central Texas and south into northern Mexico. - Overall, our goals were: 1) To characterize fine- scale population structure and hybridization between and within P.hallii subgroups. - 2) To identify regions of the genome associated with local adaptation to major climate variation in temperature and precipitation. - hallii has revealed that much of the large pericentromeric region of the genome con- sists of a low-recombination region with a high level of repetitive DNA. - Given that an appreciable rate of erroneous variant calls likely still occurs in the data, we estimated that the upper bound for pairwise diversity (π), based on callable sites. - 46% of the genome), as 0.008 within var. - hallii groups than between any of the var. - Interestingly, the degree of divergence between P.hallii var. - If hybridization between subspecies were common through- out history we would expect many individuals to show evidence of mixed ancestry however only a single individ- ual located in the southern part of the var. - All of these mixed individuals were collected from the southern part of the range (Fig. - Geography is correlated with genetic distance across the range of P.hallii (Fig. - However, IBD was strong and statistically significant within three of the. - 1 Population structure of 89 P.hallii individuals. - 2 The average number of pairwise nucleotide differences between P.hallii subgroups . - We hypothesize that genetic diversity across P.hallii is the result of some isolation by distance combined with hierarchical structure that developed as a result of expansion from southern glacial refugia following the last glacial maximum.. - The major contrasting axes of vari- ation in precipitation across the range were most strongly correlated with annual mean precipitation, seasonality of precipitation, and mean precipitation in the warmest quarter (Additional file 1: Figure S3). - Major variation in temperature was characterized most strongly by variation in mean daily temperature range, isothermality, and mini- mum temperature of the coldest month. - In general, climate in the study area varies across a northwest to southeast axis, from the hot dry deserts of Arizona, New Mexico, western Texas, and northern Mexico to the more mesic regions along the Gulf Coast (Additional file 1: Figure S5). - filipes is found only in the coastal part of the range in South Texas, whereas var. - hallii is found throughout the study area with the exception of some parts of the Gulf Coast region (Fig. - Population structure within P. - hallii as a whole was correlated with many of the major climate variables we examined. - precipitation in the warmest quarter, mean daily temperature range, minimum temperature of the coldest month, and aridity (all P <. - Many climate associated SNPs in both analyses fell within genic or 1 kb promoter regions of the genome. - In the analysis of all plants, for at least three climate variables - isothermal- ity, minimum temperature of the coldest month, and arid- ity – associated SNPs were more often found in genes than expected by chance (p <. - Associated SNPs. - BioClim6 minimum temperature of the coldest month (degrees C . - BioClim18 precipitation in the warmest quarter (mm . - Variable site π was similar in climate and non-climate associated genes (π var = 0.163 and 0.161, respectively). - Because there are strong correlations between climate and geography across the study area, we examined more closely how both factors influence variation in the candi- date climate SNPs identified by GWAS. - Variation in minimum temperature of the coldest month (BioClim variable 6) explained the greatest percentage of variation in candidate SNPs (41.9%, n = 12 SNPs). - Geography explained only 5.1% of variation in the same SNP set. - In this study, we were able to characterize genomic vari- ation across geographic space for 89 accessions of the C4 perennial grass species, P. - Population structure analysis of P. - However, just as in this study recent population structure analyses and new collections in the southern US have revealed that other major groups also exist within P. - Overall, the divided population structure of P. - hallii and other plant species suggests that many widespread species exist as subspecies complexes, with groups at different stages of the speciation continuum occurring across their range [25]. - The patterns of population structure of P. - The break is strongly associated with a transition from lower elevation in the east to higher elevation in the west. - To the west of the break are the higher elevation populations of P. - hallii, as these plants have a larger overall size and have the largest seeds of any of the plants in the spe- cies complex. - To the east of the break are all the other ecotypes of P. - This break in Texas corresponds to the transition from the gently rolling Edward/Stockton Plateaus to mountainous Trans-Pecos region in the south and the transition between the rolling lower plains to the high plains further north. - This suggests the possibil- ity that the Mexico subgroup is also distributed through- out the lower elevations of the desert Southwest of the United States.. - We find climate associated SNPs are not often associated with more than one climate variable in P. - We also found little evidence that genes containing climate associated SNPs have been under stronger directional or purifying selection than other genes in the genome. - response to hyperosmosis and salinity (both experienced during drought stress) contained climate associated SNPs.. - hallii is exposed to variable levels of drought stress throughout its range during the summer and becomes dormant in the winter months. - One candidate gene (Pahal.D02753) containing climate-associated variation is likely to be involved broadly with drought recovery through the regulation of the key stress hormone ABA.. - Using population genomic sequencing and analyses we identified multiple population subgroups within the per- ennial C4 grass P.hallii. - These population subgroups were partially overlapping across the species range and may represent early stages in the formation of subspe- cific ecotypes. - Many of the accessions used in this study were collected from field sites as seeds or live plants in the years 2010–. - All accessions that were used in this study were grown from seed in the University of Texas at Austin greenhouses. - Short read data has been archived in the NCBI Short Read Archive (https://www.ncbi.nlm.nih.gov/sra). - Reads were aligned against the v2 draft P.hallii genome (filipes variety. - This masked approxi- mately 5% of the genome. - We also observed unusually high numbers of het- erozygous calls in pericentromeric regions of the genome.. - were annotated using SNPeff v4.1 k [39] and the v2.0 an- notation of the P. - Analysis of population structure and linkage. - Isolation by distance (IBD) was tested using a Mantel test, in the R package vegan, of the matrix of geographic distances between sampling locations vs. - Climate variable values were extracted for a set of 127 P.hallii known sampling locations using the data por- tal at http://dataportal-senckenberg.de/dataExtractTool/.. - First, we determined the principal components of the set of all precipitation variables (bio12-bio19) and identified the individual variables that loaded most heavily on the first three principal components (Additional file 1: Figure S3). - Due to missing data values for a subset of the collection sites, bio15 was later dropped from the analysis. - Second, we determined the principal components of the set of all temperature variables for the study area (bio1-bio11).. - Data for climate variables isothermality, minimum temperature of the coldest month, and precipitation in the warmest quar- ter were transformed to improve normality before analysis.. - We tested whether regions of potentially low-quality alignment and SNP calling in peri-centromeric regions of the genome were likely to generate false positives. - In general, climate associated. - Because this is an indicator that SNP calling errors do not strongly con- tribute to error in the identification of climate associated SNPs, we present here results for SNPs in all regions of the genome.. - To an- notate GO terms, all P.hallii reference proteins were paired with their best Arabidopsis protein matches using BLAST (blastp) at an e-value cutoff of 10 − 3 . - physical distance (bp) between markers in the genome. - Maps of variation in climate variables across the range of P.hallii. - Manhattan plots of SNP association with climate variables for P.hallii. - Candidate genes containing climate associated SNPs. - BioClim: Bioclimatic variables derived from monthly temperature and rainfall values in the WorldClim. - Wrobleski assisted in preparation of the manuscript. - We also thank the following for providing seed collections and/or permission for our collections: The Ladybird Johnson Wildflower Center, The Brackenridge Field Laboratory, The Nature Conservancy of Texas, The State Parks of Texas, The Kika de la Garza Plant Materials Center, members of Christine Hawkes lab, as well as The University of Arizona and Arizona State University Herbaria, Socorro González Director of the Herbarium at the Instituto Politécnico Nacional, Durango, México.. - Funding agencies played no role in the design of the study or collection, analysis, and interpretation of data or writing the manuscript. - Department of Energy Joint Genome Institute is sup- ported by the Office of Science of the U.S. - KB managed the JGI portion of the data collection, interfaced with the collaborators, and provided overall project management for sequencing of the P. - The genotypic response of the plant species to habitat. - Stages in the evolution of plant species. - Ecogeographic isolation and speciation in the genus Mimulus. - Ecotypes and the controversy over stages in the formation of new species. - Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure. - Genomic evidence for the parallel evolution of coastal forms in the Senecio lautus complex. - The ecological relations of the vegetation of western Texas. - Phylogeographic structure and historical demography of the western diamondback rattlesnake (Crotalus atrox): a perspective on North American desert biogeography. - Targeting environmental adaptation in the monocot model Brachypodium distachyon:. - A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118. - Distruct: a program for the graphical display of population structure
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