Genome-environment associations in sorghum landraces predict adaptive traits

Genome-environment associations and phenotypic analyses may reveal the basis of environmental adaptation. Improving environmental adaptation in crops is essential for food security under global change, but phenotyping adaptive traits remains a major bottleneck. If associations between single-nucleotide polymorphism (SNP) alleles and environment of origin in crop landraces reflect adaptation, then these could be used to predict phenotypic variation for adaptive traits. We tested this proposition in the global food crop Sorghum bicolor, characterizing 1943 georeferenced landraces at 404,627 SNPs and quantifying allelic associations with bioclimatic and soil gradients. Environment explained a substantial portion of SNP variation, independent of geographical distance, and genic SNPs were enriched for environmental associations. Further, environment-associated SNPs predicted genotype-by-environment interactions under experimental drought stress and aluminum toxicity. Our results suggest that genomic signatures of environmental adaptation may be useful for crop improvement, enhancing germplasm identification and marker-assisted selection. Together, genome-environment associations and phenotypic analyses may reveal the basis of environmental adaptation.

[1]  R. Varshney,et al.  Genomic Selection for Crop Improvement , 2017, Springer International Publishing.

[2]  D. Bates,et al.  Linear Mixed-Effects Models using 'Eigen' and S4 , 2015 .

[3]  R. Gates,et al.  Building coral reef resilience through assisted evolution , 2015, Proceedings of the National Academy of Sciences.

[4]  P. Langridge,et al.  Molecular basis of adaptation to high soil boron in wheat landraces and elite cultivars , 2014, Nature.

[5]  A. Fischer,et al.  Senescence, nutrient remobilization, and yield in wheat and barley. , 2014, Journal of experimental botany.

[6]  Gui-Xin Li,et al.  Xyloglucan Endotransglucosylase-Hydrolase17 Interacts with Xyloglucan Endotransglucosylase-Hydrolase31 to Confer Xyloglucan Endotransglucosylase Action and Affect Aluminum Sensitivity in Arabidopsis1[OPEN] , 2014, Plant Physiology.

[7]  Timothy H. Keitt,et al.  Natural Variation in Abiotic Stress Responsive Gene Expression and Local Adaptation to Climate in Arabidopsis thaliana , 2014, Molecular biology and evolution.

[8]  Robert J. Elshire,et al.  TASSEL-GBS: A High Capacity Genotyping by Sequencing Analysis Pipeline , 2014, PloS one.

[9]  S. Pinson,et al.  Genome Wide Association Mapping of Grain Arsenic, Copper, Molybdenum and Zinc in Rice (Oryza sativa L.) Grown at Four International Field Sites , 2014, PloS one.

[10]  N. Young,et al.  Genomic Signature of Adaptation to Climate in Medicago truncatula , 2014, Genetics.

[11]  Thomas E. Juenger,et al.  Genotype-by-Environment Interaction and Plasticity: Exploring Genomic Responses of Plants to the Abiotic Environment , 2013 .

[12]  M. Whitlock,et al.  Assisted Gene Flow to Facilitate Local Adaptation to Climate Change , 2013 .

[13]  Edward S. Buckler,et al.  Dissecting Genome-Wide Association Signals for Loss-of-Function Phenotypes in Sorghum Flavonoid Pigmentation Traits , 2013, G3: Genes, Genomes, Genetics.

[14]  De-quan Li,et al.  A maize calcium-dependent protein kinase gene, ZmCPK4, positively regulated abscisic acid signaling and enhanced drought stress tolerance in transgenic Arabidopsis. , 2013, Plant physiology and biochemistry : PPB.

[15]  Jun Li,et al.  Whole-genome sequencing reveals untapped genetic potential in Africa’s indigenous cereal crop sorghum , 2013, Nature Communications.

[16]  S. Zheng,et al.  Association of specific pectin methylesterases with Al-induced root elongation inhibition in rice. , 2013, Physiologia plantarum.

[17]  B. Mueller‐Roeber,et al.  ORE1 balances leaf senescence against maintenance by antagonizing G2‐like‐mediated transcription , 2013, EMBO reports.

[18]  Y. Fan,et al.  Global Patterns of Groundwater Table Depth , 2013, Science.

[19]  J. Tailleur,et al.  Global Patterns of Groundwater Table Depth , 2013 .

[20]  C. T. Hash,et al.  Population genomic and genome-wide association studies of agroclimatic traits in sorghum , 2012, Proceedings of the National Academy of Sciences.

[21]  P. Langridge,et al.  Can genomics boost productivity of orphan crops? , 2012, Nature Biotechnology.

[22]  Gwendal Latouche,et al.  A new optical leaf-clip meter for simultaneous non-destructive assessment of leaf chlorophyll and epidermal flavonoids , 2012, Physiologia plantarum.

[23]  Jean-Luc Jannink,et al.  Shrinkage Estimation of the Realized Relationship Matrix , 2012, G3: Genes | Genomes | Genetics.

[24]  T. Juenger,et al.  Characterizing genomic variation of Arabidopsis thaliana: the roles of geography and climate , 2012, Molecular ecology.

[25]  P. Traoré,et al.  Breeding Strategies for Adaptation of Pearl Millet and Sorghum to Climate Variability and Change in West Africa. , 2012 .

[26]  Jukon Kim,et al.  The overexpression of OsNAC9 alters the root architecture of rice plants enhancing drought resistance and grain yield under field conditions. , 2012, Plant biotechnology journal.

[27]  P. Pesaresi,et al.  The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency , 2012, Nature.

[28]  Doreen Ware,et al.  ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize , 2012, Proceedings of the National Academy of Sciences.

[29]  Xianran Li,et al.  Presence of tannins in sorghum grains is conditioned by different natural alleles of Tannin1 , 2012, Proceedings of the National Academy of Sciences.

[30]  Bjarni J. Vilhjálmsson,et al.  An efficient multi-locus mixed model approach for genome-wide association studies in structured populations , 2012, Nature Genetics.

[31]  Alex A. Pollen,et al.  The genomic basis of adaptive evolution in threespine sticklebacks , 2012, Nature.

[32]  R. L. Gomide,et al.  Studying the genetic basis of drought tolerance in sorghum by managed stress trials and adjustments for phenological and plant height differences , 2012, Theoretical and Applied Genetics.

[33]  Qian Qian,et al.  Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm , 2011, Nature Genetics.

[34]  David M. Goodstein,et al.  Phytozome: a comparative platform for green plant genomics , 2011, Nucleic Acids Res..

[35]  Jeffrey B. Endelman,et al.  Ridge Regression and Other Kernels for Genomic Selection with R Package rrBLUP , 2011 .

[36]  Joy Bergelson,et al.  References and Notes Supporting Online Material Adaptation to Climate across the Arabidopsis Thaliana Genome , 2022 .

[37]  M. Nordborg,et al.  A Map of Local Adaptation in Arabidopsis thaliana , 2011, Science.

[38]  Diana V. Dugas,et al.  Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum , 2011, Proceedings of the National Academy of Sciences.

[39]  E. Pauw,et al.  Predictive Association between Biotic Stress Traits and Eco-Geographic Data for Wheat and Barley Landraces , 2011 .

[40]  C. Tom Hash,et al.  The Relationship between Population Structure and Aluminum Tolerance in Cultivated Sorghum , 2011, PloS one.

[41]  Robert J. Elshire,et al.  A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species , 2011, PloS one.

[42]  Ky L. Mathews,et al.  Environment characterization as an aid to wheat improvement: interpreting genotype-environment interactions by modelling water-deficit patterns in North-Eastern Australia. , 2011, Journal of experimental botany.

[43]  M. Zanor,et al.  ORS1, an H2O2-Responsive NAC Transcription Factor, Controls Senescence in Arabidopsis thaliana , 2011, Molecular Plant.

[44]  Joy Bergelson,et al.  Towards identifying genes underlying ecologically relevant traits in Arabidopsis thaliana , 2010, Nature Reviews Genetics.

[45]  Abraham Blum,et al.  Plant Breeding for Water-Limited Environments , 2010 .

[46]  P. Legendre,et al.  Common factors drive adaptive genetic variation at different spatial scales in Arabis alpina , 2010, Molecular ecology.

[47]  Tina T. Hu,et al.  Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils , 2010, Nature Genetics.

[48]  Jean-Luc Jannink,et al.  Genomic selection in plant breeding: from theory to practice. , 2010, Briefings in functional genomics.

[49]  M. Stephens,et al.  Bayesian statistical methods for genetic association studies , 2009, Nature Reviews Genetics.

[50]  H. Upadhyaya,et al.  Developing a mini core collection of sorghum for diversified utilization of germplasm. , 2009 .

[51]  Richard Durbin,et al.  Sequence analysis Fast and accurate short read alignment with Burrows – Wheeler transform , 2009 .

[52]  N. Batjes,et al.  The Harmonized World Soil Database , 2009 .

[53]  Mihaela M. Martis,et al.  The Sorghum bicolor genome and the diversification of grasses , 2009, Nature.

[54]  Antonio Trabucco,et al.  Climate change mitigation: a spatial analysis of global land suitability for Clean Development Mechanism afforestation and reforestation , 2008 .

[55]  D. Heckerman,et al.  Efficient Control of Population Structure in Model Organism Association Mapping , 2008, Genetics.

[56]  C. Tebaldi,et al.  Prioritizing Climate Change Adaptation Needs for Food Security in 2030 , 2008, Science.

[57]  William L. Rooney,et al.  Community Resources and Strategies for Association Mapping in Sorghum , 2008 .

[58]  L. Kochian,et al.  A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum , 2007, Nature Genetics.

[59]  H. Nguyen,et al.  Sorghum stay-green QTL individually reduce post-flowering drought-induced leaf senescence. , 2006, Journal of experimental botany.

[60]  S. Rose,et al.  Human-Induced Climate Change: Global agricultural land-use data for integrated assessment modeling , 2007 .

[61]  John M. Reilly,et al.  Human-induced climate change : an interdisciplinary assessment , 2007 .

[62]  Tony O’Hagan Bayes factors , 2006 .

[63]  P. Legendre,et al.  Variation partitioning of species data matrices: estimation and comparison of fractions. , 2006, Ecology.

[64]  J. Bailey-Serres,et al.  Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice , 2006, Nature.

[65]  J. L. Parra,et al.  Very high resolution interpolated climate surfaces for global land areas , 2005 .

[66]  M. Purugganan,et al.  Evolutionary and Ecological Genomics of Arabidopsis1 , 2005, Plant Physiology.

[67]  Cheryl A. Palm,et al.  Fertility capability soil classification: a tool to help assess soil quality in the tropics , 2003 .

[68]  Pierre Legendre,et al.  All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices , 2002 .

[69]  M. Hulme,et al.  A high-resolution data set of surface climate over global land areas , 2002 .

[70]  Cort J. Willmott,et al.  Global Distribution of Plant-Extractable Water Capacity of Soil (Dunne) , 2000 .

[71]  Burt,et al.  Natural selection in the wild. , 2000, Trends in ecology & evolution.

[72]  G. Hammer,et al.  Does maintaining green leaf area in sorghum improve yield under drought? II. Dry matter production and yield. , 2000 .

[73]  C. W. Smith,et al.  Sorghum: origin, history, technology and production. , 2000 .

[74]  D. M. Bates Lost Crops of Africa. Volume I: Grains.Board on Science and Technology for International Development, National Research Council , 1998 .

[75]  L. Perlemuter [From theory to practice]. , 1997, Soins. Psychiatrie.

[76]  Cort J. Willmott,et al.  GLOBAL DISTRIBUTION OF PLANT‐EXTRACTABLE WATER CAPACITY OF SOIL , 1996 .

[77]  F. Miller,et al.  The association of genes controlling caryopsis traits with grain mold resistance in sorghum. , 1993 .

[78]  N. Vavilov Origin and geography of cultivated plants , 1993 .

[79]  R. Lande,et al.  Efficiency of marker-assisted selection in the improvement of quantitative traits. , 1990, Genetics.

[80]  A. L. V. D. Wollenberg Redundancy analysis an alternative for canonical correlation analysis , 1977 .

[81]  Paul R. Lowe,et al.  The Computation of Saturation Vapor Pressure , 1974 .

[82]  H. B. Harris,et al.  Influence of Tannin Content on Preharvest seed Germination in Sorghum> 1 , 1970 .