The genomic landscape of molecular responses to natural drought stress in Panicum hallii

Lovell, John T.; Jenkins, Jerry; Lowry, David B.; Mamidi, Sujan; Sreedasyam, Avinash; Weng, Xiaoyu; Barry, Kerrie; Bonnette, Jason; Campitelli, Brandon; Daum, Chris; Gordon, Sean P.; Gould, Billie A.; Khasanova, Albina; Lipzen, Anna; MacQueen, Alice; Palacio-Mejía, Juan Diego; Plott, Christopher; Shakirov, Eugene V.; Shu, Shengqiang; Yoshinaga, Yuko; Zane, Matt; Kudrna, Dave; Talag, Jason D.; Rokhsar, Daniel; Grimwood, Jane; Schmutz, Jeremy; Juenger, Thomas E.

doi:10.1038/s41467-018-07669-x

Title: The genomic landscape of molecular responses to natural drought stress in Panicum hallii

Journal Article · 05 December 2018 · Nature Communications

DOI: https://doi.org/10.1038/s41467-018-07669-x · OSTI ID:1506428

Lovell, John T. ^[1];

^[2]; Lowry, David B. ^[3];

^[2];

^[2]; Weng, Xiaoyu ^[4]; Barry, Kerrie ^[5]; Bonnette, Jason ^[4]; Campitelli, Brandon ^[4]; Daum, Chris ^[5];

^[6]; Gould, Billie A. ^[3]; Khasanova, Albina ^[4]; Lipzen, Anna ^[5];

^[4];

^[4]; Plott, Christopher ^[2]; Shakirov, Eugene V. ^[7];

^[5]; Yoshinaga, Yuko ^[5] more »

HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States); The Univ. of Texas, Austin, TX (United States); Genome Sequencing Center, HudsonAlpha Institute for Biotechnology
HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States)
Michigan State Univ., East Lansing, MI (United States)
The Univ. of Texas, Austin, TX (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Zymergen Inc, Emeryville, CA (United States)
The Univ. of Texas, Austin, TX (United States); Kazan Federal University, Kazan (Russia)
Univ. of Arizona, Tucson, AZ (United States)
Univ. of California, Berkeley, CA (United States)
HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Environmental stress is a major driver of ecological community dynamics and agricultural productivity. This is especially true for soil water availability, because drought is the greatest abiotic inhibitor of worldwide crop yields. Here, we test the genetic basis of drought responses in the genetic model for C4 perennial grasses, Panicum hallii, through population genomics, field-scale gene-expression (eQTL) analysis, and comparison of two complete genomes. While gene expression networks are dominated by local cis-regulatory elements, we observe three genomic hotspots of unlinked trans-regulatory loci. These regulatory hubs are four times more drought responsive than the genome-wide average. Additionally, cis- and trans-regulatory networks are more likely to have opposing effects than expected under neutral evolution, supporting a strong influence of compensatory evolution and stabilizing selection. These results implicate trans-regulatory evolution as a driver of drought responses and demonstrate the potential for crop improvement in drought-prone regions through modification of gene regulatory networks.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of Wisconsin, Madison, WI (United States). Great Lakes Bioenergy Research Center

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC02-05CH11231; SC0018409

OSTI ID:: 1506428

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 9; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (94)

Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes Matsukura, Satoko; Mizoi, Junya; Yoshida, Takumi Molecular Genetics and Genomics, Vol. 283, Issue 2 https://doi.org/10.1007/s00438-009-0506-y	journal	January 2010
AP2/ERF family transcription factors in plant abiotic stress responses Mizoi, Junya; Shinozaki, Kazuo; Yamaguchi-Shinozaki, Kazuko Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1819, Issue 2 https://doi.org/10.1016/j.bbagrm.2011.08.004	journal	February 2012
Europe-wide reduction in primary productivity caused by the heat and drought in 2003 Ciais, Ph.; Reichstein, M.; Viovy, N. Nature, Vol. 437, Issue 7058 https://doi.org/10.1038/nature03972	journal	September 2005
Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data Chin, Chen-Shan; Alexander, David H.; Marks, Patrick Nature Methods, Vol. 10, Issue 6 https://doi.org/10.1038/nmeth.2474	journal	May 2013
MECAT: fast mapping, error correction, and de novo assembly for single-molecule sequencing reads Xiao, Chuan-Le; Chen, Ying; Xie, Shang-Qian Nature Methods, Vol. 14, Issue 11 https://doi.org/10.1038/nmeth.4432	journal	September 2017
Targeted introduction of heritable point mutations into the plant mitochondrial genome Forner, Joachim; Kleinschmidt, Dennis; Meyer, Etienne H. Nature Plants, Vol. 8, Issue 3 https://doi.org/10.1038/s41477-022-01108-y	journal	March 2022
Targeted A-to-G base editing of chloroplast DNA in plants Mok, Young Geun; Hong, Sunghyun; Bae, Su-Ji Nature Plants, Vol. 8, Issue 12 https://doi.org/10.1038/s41477-022-01279-8	journal	December 2022
Mating pair stabilization mediates bacterial conjugation species specificity Low, Wen Wen; Wong, Joshua L. C.; Beltran, Leticia C. Nature Microbiology, Vol. 7, Issue 7 https://doi.org/10.1038/s41564-022-01146-4	journal	June 2022
Shared and distinct transcriptomic cell types across neocortical areas Tasic, Bosiljka; Yao, Zizhen; Graybuck, Lucas T. Nature, Vol. 563, Issue 7729 https://doi.org/10.1038/s41586-018-0654-5	journal	October 2018
Evidence for widespread adaptive evolution of gene expression in budding yeast Fraser, H. B.; Moses, A. M.; Schadt, E. E. Proceedings of the National Academy of Sciences, Vol. 107, Issue 7 https://doi.org/10.1073/pnas.0912245107	journal	January 2010
R/qtl: QTL mapping in experimental crosses Broman, K. W.; Wu, H.; Sen, S. Bioinformatics, Vol. 19, Issue 7 https://doi.org/10.1093/bioinformatics/btg112	journal	May 2003
BRAKER1: Unsupervised RNA-Seq-Based Genome Annotation with GeneMark-ET and AUGUSTUS: Table 1. Hoff, Katharina J.; Lange, Simone; Lomsadze, Alexandre Bioinformatics, Vol. 32, Issue 5 https://doi.org/10.1093/bioinformatics/btv661	journal	November 2015
Deleterious mutations, apparent stabilizing selection and the maintenance of quantitative variation. Kondrashov, A. S.; Turelli, M. Genetics, Vol. 132, Issue 2 https://doi.org/10.1093/genetics/132.2.603	journal	October 1992
Monitoring plant and soil water status: established and novel methods revisited and their relevance to studies of drought tolerance Jones, H. G. Journal of Experimental Botany, Vol. 58, Issue 2 https://doi.org/10.1093/jxb/erl118	journal	November 2006
Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies Haas, B. J. Nucleic Acids Research, Vol. 31, Issue 19 https://doi.org/10.1093/nar/gkg770	journal	October 2003
MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity Wang, Y.; Tang, H.; DeBarry, J. D. Nucleic Acids Research, Vol. 40, Issue 7 https://doi.org/10.1093/nar/gkr1293	journal	January 2012
The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote Liao, Yang; Smyth, Gordon K.; Shi, Wei Nucleic Acids Research, Vol. 41, Issue 10 https://doi.org/10.1093/nar/gkt214	journal	April 2013
JASPAR 2016: a major expansion and update of the open-access database of transcription factor binding profiles Mathelier, Anthony; Fornes, Oriol; Arenillas, David J. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1176	journal	November 2015
Ab initio Gene Finding in Drosophila Genomic DNA Salamov, Asaf A.; Solovyev, Victor V. Genome Research, Vol. 10, Issue 4, p. 516-522 https://doi.org/10.1101/gr.10.4.516	journal	April 2000
Natural selection on cis and trans regulation in yeasts Emerson, J. J.; Hsieh, L. -C.; Sung, H. -M. Genome Research, Vol. 20, Issue 6 https://doi.org/10.1101/gr.101576.109	journal	May 2010
Drought responsive gene expression regulatory divergence between upland and lowland ecotypes of a perennial C ₄ grass Lovell, John T.; Schwartz, Scott; Lowry, David B. Genome Research, Vol. 26, Issue 4 https://doi.org/10.1101/gr.198135.115	journal	March 2016
Physiological Genomics of Response to Soil Drying in Diverse Arabidopsis Accessions Des Marais, David L.; McKay, John K.; Richards, James H. The Plant Cell, Vol. 24, Issue 3 https://doi.org/10.1105/tpc.112.096180	journal	March 2012
Asymmetric responses of primary productivity to precipitation extremes: A synthesis of grassland precipitation manipulation experiments Wilcox, Kevin R.; Shi, Zheng; Gherardi, Laureano A. Global Change Biology, Vol. 23, Issue 10 https://doi.org/10.1111/gcb.13706	journal	May 2017
The genetics of divergence and reproductive isolation between ecotypes of Panicum hallii Lowry, David B.; Hernandez, Kyle; Taylor, Samuel H. New Phytologist, Vol. 205, Issue 1 https://doi.org/10.1111/nph.13027	journal	September 2014
Feedstocks for Lignocellulosic Biofuels Somerville, Cris; Youngs, Heather; Taylor, Caroline Science, Vol. 329, Issue 5993, p. 790-792 https://doi.org/10.1126/science.1189268	journal	August 2010
Plant Productivity and Environment Boyer, J. S. Science, Vol. 218, Issue 4571 https://doi.org/10.1126/science.218.4571.443	journal	October 1982
HEAT-SHOCK PROTEINS, MOLECULAR CHAPERONES, AND THE STRESS RESPONSE: Evolutionary and Ecological Physiology Feder, Martin E.; Hofmann, Gretchen E. Annual Review of Physiology, Vol. 61, Issue 1 https://doi.org/10.1146/annurev.physiol.61.1.243	journal	March 1999
Transcriptome and de novo analysis of Rosa xanthina f. spontanea in response to cold stress Zhuang, Defeng; Ma, Ce; Xue, Li BMC Plant Biology, Vol. 21, Issue 1 https://doi.org/10.1186/s12870-021-03246-5	journal	October 2021
TSPmap, a tool making use of traveling salesperson problem solvers in the efficient and accurate construction of high-density genetic linkage maps Monroe, J. Grey; Allen, Zachariah A.; Tanger, Paul BioData Mining, Vol. 10, Issue 1 https://doi.org/10.1186/s13040-017-0158-0	journal	December 2017
OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy Emms, David M.; Kelly, Steven Genome Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s13059-015-0721-2	journal	August 2015
BEAST 2: A Software Platform for Bayesian Evolutionary Analysis Bouckaert, Remco; Heled, Joseph; Kühnert, Denise PLoS Computational Biology, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pcbi.1003537	journal	April 2014
fastSTRUCTURE: Variational Inference of Population Structure in Large SNP Data Sets Raj, Anil; Stephens, Matthew; Pritchard, Jonathan K. Genetics, Vol. 197, Issue 2 https://doi.org/10.1534/genetics.114.164350	journal	April 2014
Resistance and resilience of a grassland ecosystem to climate extremes Hoover, David L.; Knapp, Alan K.; Smith, Melinda D. Ecology, Vol. 95, Issue 9 https://doi.org/10.1890/13-2186.1	journal	September 2014
A population genetic transect of Panicum hallii (Poaceae) Lowry, David B.; Purmal, Colin T.; Juenger, Thomas E. American Journal of Botany, Vol. 100, Issue 3 https://doi.org/10.3732/ajb.1200379	journal	March 2013
Evolution at two levels of gene expression in yeast Artieri, Carlo G.; Fraser, Hunter B. arXiv https://doi.org/10.48550/arxiv.1311.7140	preprint	January 2013
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method Livak, Kenneth J.; Schmittgen, Thomas D. Methods, Vol. 25, Issue 4 https://doi.org/10.1006/meth.2001.1262	journal	December 2001
Clustal Omega, Accurate Alignment of Very Large Numbers of Sequences Sievers, Fabian; Higgins, Desmond G. Multiple Sequence Alignment Methods https://doi.org/10.1007/978-1-62703-646-7_6	book	January 2013
Physiological adaptation and plasticity to water stress of coastal and desert populations of Heliotropium curassavicum L. Roy, J.; Mooney, H. A. Oecologia, Vol. 52, Issue 3 https://doi.org/10.1007/BF00367961	journal	January 1982
Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes Matsukura, Satoko; Mizoi, Junya; Yoshida, Takumi Molecular Genetics and Genomics, Vol. 283, Issue 2 https://doi.org/10.1007/s00438-009-0506-y	journal	January 2010
AP2/ERF family transcription factors in plant abiotic stress responses Mizoi, Junya; Shinozaki, Kazuo; Yamaguchi-Shinozaki, Kazuko Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1819, Issue 2 https://doi.org/10.1016/j.bbagrm.2011.08.004	journal	February 2012
Natural variation and genetic constraints on drought tolerance Juenger, Thomas E. Current Opinion in Plant Biology, Vol. 16, Issue 3 https://doi.org/10.1016/j.pbi.2013.02.001	journal	June 2013
The gene regulatory logic of transcription factor evolution Wagner, Günter P.; Lynch, Vincent J. Trends in Ecology & Evolution, Vol. 23, Issue 7 https://doi.org/10.1016/j.tree.2008.03.006	journal	July 2008
Europe-wide reduction in primary productivity caused by the heat and drought in 2003 Ciais, Ph.; Reichstein, M.; Viovy, N. Nature, Vol. 437, Issue 7058 https://doi.org/10.1038/nature03972	journal	September 2005
Inferring human population size and separation history from multiple genome sequences Schiffels, Stephan; Durbin, Richard Nature Genetics, Vol. 46, Issue 8 https://doi.org/10.1038/ng.3015	journal	June 2014
Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data Chin, Chen-Shan; Alexander, David H.; Marks, Patrick Nature Methods, Vol. 10, Issue 6 https://doi.org/10.1038/nmeth.2474	journal	May 2013
MECAT: fast mapping, error correction, and de novo assembly for single-molecule sequencing reads Xiao, Chuan-Le; Chen, Ying; Xie, Shang-Qian Nature Methods, Vol. 14, Issue 11 https://doi.org/10.1038/nmeth.4432	journal	September 2017
Evidence for widespread adaptive evolution of gene expression in budding yeast Fraser, H. B.; Moses, A. M.; Schadt, E. E. Proceedings of the National Academy of Sciences, Vol. 107, Issue 7 https://doi.org/10.1073/pnas.0912245107	journal	January 2010
Genetic mapping of adaptation reveals fitness tradeoffs in Arabidopsis thaliana Agren, J.; Oakley, C. G.; McKay, J. K. Proceedings of the National Academy of Sciences, Vol. 110, Issue 52 https://doi.org/10.1073/pnas.1316773110	journal	December 2013
Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses van Velzen, Robin; Holmer, Rens; Bu, Fengjiao Proceedings of the National Academy of Sciences, Vol. 115, Issue 20 https://doi.org/10.1073/pnas.1721395115	journal	May 2018
PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses Purcell, Shaun; Neale, Benjamin; Todd-Brown, Kathe The American Journal of Human Genetics, Vol. 81, Issue 3 https://doi.org/10.1086/519795	journal	September 2007
R/qtl: QTL mapping in experimental crosses Broman, K. W.; Wu, H.; Sen, S. Bioinformatics, Vol. 19, Issue 7 https://doi.org/10.1093/bioinformatics/btg112	journal	May 2003
Fast and accurate short read alignment with Burrows-Wheeler transform Li, H.; Durbin, R. Bioinformatics, Vol. 25, Issue 14 https://doi.org/10.1093/bioinformatics/btp324	journal	May 2009
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
STAR: ultrafast universal RNA-seq aligner Dobin, Alexander; Davis, Carrie A.; Schlesinger, Felix Bioinformatics, Vol. 29, Issue 1 https://doi.org/10.1093/bioinformatics/bts635	journal	October 2012
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
BRAKER1: Unsupervised RNA-Seq-Based Genome Annotation with GeneMark-ET and AUGUSTUS: Table 1. Hoff, Katharina J.; Lange, Simone; Lomsadze, Alexandre Bioinformatics, Vol. 32, Issue 5 https://doi.org/10.1093/bioinformatics/btv661	journal	November 2015
Comparative Genomics of an Unusual Biogeographic Disjunction in the Cotton Tribe (Gossypieae) Yields Insights into Genome Downsizing Grover, Corrinne E.; Arick, Mark A.; Conover, Justin L. Genome Biology and Evolution, Vol. 9, Issue 12 https://doi.org/10.1093/gbe/evx248	journal	November 2017
Deleterious mutations, apparent stabilizing selection and the maintenance of quantitative variation. Kondrashov, A. S.; Turelli, M. Genetics, Vol. 132, Issue 2 https://doi.org/10.1093/genetics/132.2.603	journal	October 1992
Monitoring plant and soil water status: established and novel methods revisited and their relevance to studies of drought tolerance Jones, H. G. Journal of Experimental Botany, Vol. 58, Issue 2 https://doi.org/10.1093/jxb/erl118	journal	November 2006
Inheritance of Gene Expression Level and Selective Constraints on Trans- and Cis-Regulatory Changes in Yeast Schaefke, Bernhard; Emerson, J. J.; Wang, Tzi-Yuan Molecular Biology and Evolution, Vol. 30, Issue 9 https://doi.org/10.1093/molbev/mst114	journal	June 2013
Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies Haas, B. J. Nucleic Acids Research, Vol. 31, Issue 19 https://doi.org/10.1093/nar/gkg770	journal	October 2003
MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity Wang, Y.; Tang, H.; DeBarry, J. D. Nucleic Acids Research, Vol. 40, Issue 7 https://doi.org/10.1093/nar/gkr1293	journal	January 2012
The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote Liao, Yang; Smyth, Gordon K.; Shi, Wei Nucleic Acids Research, Vol. 41, Issue 10 https://doi.org/10.1093/nar/gkt214	journal	April 2013
limma powers differential expression analyses for RNA-sequencing and microarray studies Ritchie, Matthew E.; Phipson, Belinda; Wu, Di Nucleic Acids Research, Vol. 43, Issue 7 https://doi.org/10.1093/nar/gkv007	journal	January 2015
JASPAR 2016: a major expansion and update of the open-access database of transcription factor binding profiles Mathelier, Anthony; Fornes, Oriol; Arenillas, David J. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1176	journal	November 2015
Ab initio Gene Finding in Drosophila Genomic DNA Salamov, Asaf A.; Solovyev, Victor V. Genome Research, Vol. 10, Issue 4, p. 516-522 https://doi.org/10.1101/gr.10.4.516	journal	April 2000
Natural selection on cis and trans regulation in yeasts Emerson, J. J.; Hsieh, L. -C.; Sung, H. -M. Genome Research, Vol. 20, Issue 6 https://doi.org/10.1101/gr.101576.109	journal	May 2010
VarScan 2: Somatic mutation and copy number alteration discovery in cancer by exome sequencing Koboldt, D. C.; Zhang, Q.; Larson, D. E. Genome Research, Vol. 22, Issue 3 https://doi.org/10.1101/gr.129684.111	journal	February 2012
Evolution at two levels of gene expression in yeast Artieri, C. G.; Fraser, H. B. Genome Research, Vol. 24, Issue 3 https://doi.org/10.1101/gr.165522.113	journal	December 2013
Computational Inference of Homologous Gene Structures in the Human Genome Yeh, R. -F.; Lim, L. P.; Burge, C. B. Genome Research, Vol. 11, Issue 5 https://doi.org/10.1101/gr.175701	journal	May 2001
Drought responsive gene expression regulatory divergence between upland and lowland ecotypes of a perennial C ₄ grass Lovell, John T.; Schwartz, Scott; Lowry, David B. Genome Research, Vol. 26, Issue 4 https://doi.org/10.1101/gr.198135.115	journal	March 2016
BLAT---The BLAST-Like Alignment Tool Kent, W. J. Genome Research, Vol. 12, Issue 4 https://doi.org/10.1101/gr.229202	journal	March 2002
Physiological Genomics of Response to Soil Drying in Diverse Arabidopsis Accessions Des Marais, David L.; McKay, John K.; Richards, James H. The Plant Cell, Vol. 24, Issue 3 https://doi.org/10.1105/tpc.112.096180	journal	March 2012
A direct approach to false discovery rates Storey, John D. Journal of the Royal Statistical Society: Series B (Statistical Methodology), Vol. 64, Issue 3 https://doi.org/10.1111/1467-9868.00346	journal	August 2002
TESS3: fast inference of spatial population structure and genome scans for selection Caye, Kevin; Deist, Timo M.; Martins, Helena Molecular Ecology Resources, Vol. 16, Issue 2 https://doi.org/10.1111/1755-0998.12471	journal	October 2015
Asymmetric responses of primary productivity to precipitation extremes: A synthesis of grassland precipitation manipulation experiments Wilcox, Kevin R.; Shi, Zheng; Gherardi, Laureano A. Global Change Biology, Vol. 23, Issue 10 https://doi.org/10.1111/gcb.13706	journal	May 2017
ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis: WRKY transcription factor and drought stress Ren, Xiaozhi; Chen, Zhizhong; Liu, Yue The Plant Journal, Vol. 63, Issue 3 https://doi.org/10.1111/j.1365-313X.2010.04248.x	journal	May 2010
A worldwide phylogenetic classification of the Poaceae (Gramineae): Phylogenetic classification of the grasses Soreng, Robert J.; Peterson, Paul M.; Romaschenko, Konstantin Journal of Systematics and Evolution, Vol. 53, Issue 2 https://doi.org/10.1111/jse.12150	journal	March 2015
The genetics of divergence and reproductive isolation between ecotypes of Panicum hallii Lowry, David B.; Hernandez, Kyle; Taylor, Samuel H. New Phytologist, Vol. 205, Issue 1 https://doi.org/10.1111/nph.13027	journal	September 2014
Feedstocks for Lignocellulosic Biofuels Somerville, Cris; Youngs, Heather; Taylor, Caroline Science, Vol. 329, Issue 5993, p. 790-792 https://doi.org/10.1126/science.1189268	journal	August 2010
Plant Productivity and Environment Boyer, J. S. Science, Vol. 218, Issue 4571 https://doi.org/10.1126/science.218.4571.443	journal	October 1982
HEAT-SHOCK PROTEINS, MOLECULAR CHAPERONES, AND THE STRESS RESPONSE: Evolutionary and Ecological Physiology Feder, Martin E.; Hofmann, Gretchen E. Annual Review of Physiology, Vol. 61, Issue 1 https://doi.org/10.1146/annurev.physiol.61.1.243	journal	March 1999
TSPmap, a tool making use of traveling salesperson problem solvers in the efficient and accurate construction of high-density genetic linkage maps Monroe, J. Grey; Allen, Zachariah A.; Tanger, Paul BioData Mining, Vol. 10, Issue 1 https://doi.org/10.1186/s13040-017-0158-0	journal	December 2017
OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy Emms, David M.; Kelly, Steven Genome Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s13059-015-0721-2	journal	August 2015
BEAST 2: A Software Platform for Bayesian Evolutionary Analysis Bouckaert, Remco; Heled, Joseph; Kühnert, Denise PLoS Computational Biology, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pcbi.1003537	journal	April 2014
Dissecting the Genetic Basis of a Complex cis-Regulatory Adaptation Naranjo, Santiago; Smith, Justin D.; Artieri, Carlo G. PLOS Genetics, Vol. 11, Issue 12 https://doi.org/10.1371/journal.pgen.1005751	journal	December 2015
A Gene-Phenotype Network Based on Genetic Variability for Drought Responses Reveals Key Physiological Processes in Controlled and Natural Environments Rengel, David; Arribat, Sandrine; Maury, Pierre PLoS ONE, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pone.0045249	journal	October 2012
fastSTRUCTURE: Variational Inference of Population Structure in Large SNP Data Sets Raj, Anil; Stephens, Matthew; Pritchard, Jonathan K. Genetics, Vol. 197, Issue 2 https://doi.org/10.1534/genetics.114.164350	journal	April 2014
The Dissection of Expression Quantitative Trait Locus Hotspots Tian, Jianan; Keller, Mark P.; Broman, Aimee Teo Genetics, Vol. 202, Issue 4 https://doi.org/10.1534/genetics.115.183624	journal	February 2016
Resistance and resilience of a grassland ecosystem to climate extremes Hoover, David L.; Knapp, Alan K.; Smith, Melinda D. Ecology, Vol. 95, Issue 9 https://doi.org/10.1890/13-2186.1	journal	September 2014
A population genetic transect of Panicum hallii (Poaceae) Lowry, David B.; Purmal, Colin T.; Juenger, Thomas E. American Journal of Botany, Vol. 100, Issue 3 https://doi.org/10.3732/ajb.1200379	journal	March 2013
A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w Cingolani, Pablo; Platts, Adrian; Wang, Le Lily Fly, Vol. 6, Issue 2 https://doi.org/10.4161/fly.19695	journal	April 2012
Resistance and resilience of a grassland ecosystem to climate extremes Hoover, David L.; Knapp, Alan K.; Smith, Melinda D. Figshare https://doi.org/10.6084/m9.figshare.c.3307092.v1	collection	January 2016
TSPmap, a tool making use of traveling salesperson problem solvers in the efficient and accurate construction of high-density genetic linkage maps Monroe, J.; Allen, Zachariah; Tanger, Paul Figshare https://doi.org/10.6084/m9.figshare.c.3958558	collection	January 2017

Cited By (13)

IsoSeq transcriptome assembly of C ₃ panicoid grasses provides tools to study evolutionary change in the Panicoideae Carvalho, Daniel S.; Nishimwe, Aime V.; Schnable, James C. Plant Direct, Vol. 4, Issue 2 https://doi.org/10.1002/pld3.203	journal	February 2020
A high-quality genome of Eragrostis curvula grass provides insights into Poaceae evolution and supports new strategies to enhance forage quality Carballo, J.; Santos, B. A. C. M.; Zappacosta, D. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-46610-0	journal	July 2019
Conservation of Endophyte Bacterial Community Structure Across Two Panicum Grass Species Singer, Esther; Bonnette, Jason; Woyke, Tanja Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02181	journal	September 2019
The Genetic Architecture of Shoot and Root Trait Divergence Between Mesic and Xeric Ecotypes of a Perennial Grass Khasanova, Albina; Lovell, John T.; Bonnette, Jason Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00366	journal	April 2019
Biosynthesis and Emission of Stress-Induced Volatile Terpenes in Roots and Leaves of Switchgrass (Panicum virgatum L.) Muchlinski, Andrew; Chen, Xinlu; Lovell, John T. Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01144	journal	September 2019
Gene Expression and Physiological Differences in Neo-Octoploid Switchgrass Subjected to Drought Stress Chanbusarakum, Lisa; Bragg, Jennifer; Cheng, Prisca BioEnergy Research, Vol. 13, Issue 1 https://doi.org/10.1007/s12155-020-10092-0	journal	February 2020
A high-quality genome of Eragrostis curvula grass provides insights into Poaceae evolution and supports new strategies to enhance forage quality Carballo, J.; Santos, B. A. C. M.; Zappacosta, D. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-46610-0	journal	July 2019
Genome-wide phylogenetic and structural analysis reveals the molecular evolution of the ABA receptor gene family Yang, Jing-Fang; Chen, Mo-Xian; Zhang, Jian-Hua Journal of Experimental Botany, Vol. 71, Issue 4 https://doi.org/10.1093/jxb/erz511	journal	November 2019
Widespread lateral gene transfer among grasses Hibdige, Samuel G. S.; Raimondeau, Pauline; Christin, Pascal‐Antoine New Phytologist, Vol. 230, Issue 6 https://doi.org/10.1111/nph.17328	journal	April 2021
Complex interactions between day length and diurnal patterns of gene expression drive photoperiodic responses in a perennial C ₄ grass Weng, Xiaoyu; Lovell, John T.; Schwartz, Scott L. Plant, Cell & Environment, Vol. 42, Issue 7 https://doi.org/10.1111/pce.13546	journal	April 2019
Integrating transcriptomic network reconstruction and eQTL analyses reveals mechanistic connections between genomic architecture and Brassica rapa development Baker, Robert L.; Leong, Wen Fung; Brock, Marcus T. PLOS Genetics, Vol. 15, Issue 9 https://doi.org/10.1371/journal.pgen.1008367	journal	September 2019
Conservation of Endophyte Bacterial Community Structure Across Two Panicum Grass Species Singer, Esther; Bonnette, Jason; Woyke, Tanja Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02181	journal	September 2019
Characterization of introgression from the teosinte Zea mays ssp. mexicana to Mexican highland maize Gonzalez-Segovia, Eric; Pérez-Limon, Sergio; Cíntora-Martínez, G. Carolina PeerJ, Vol. 7 https://doi.org/10.7717/peerj.6815	journal	January 2019

Similar Records

Drought responsive gene expression regulatory divergence between upland and lowland ecotypes of a perennial C₄ grass

Journal Article · 2016 · Genome Research · OSTI ID:1616046

Lovell, John T.; Schwartz, Scott; Lowry, David B.; +10 more

Evolutionary Analyses of Gene Expression Divergence in Panicum hallii : Exploring Constitutive and Plastic Responses Using Reciprocal Transplants

Journal Article · 2023 · Molecular Biology and Evolution · OSTI ID:2280395

Bhaskara, Govinal Badiger; Haque, Taslima; Bonnette, Jason E.; +5 more

Transcriptome and DNA methylome divergence of inflorescence development between 2 ecotypes in Panicum hallii

Journal Article · 2023 · Plant Physiology (Bethesda) · OSTI ID:2228595

Weng, Xiaoyu; Song, Haili; Sreedasyam, Avinash; +9 more

Related Subjects

54 ENVIRONMENTAL SCIENCES
59 BASIC BIOLOGICAL SCIENCES
GxE
adaptation
cis
compensatory evolution
eQTL
plasticity
trans

Title: The genomic landscape of molecular responses to natural drought stress in Panicum hallii

Citation Formats

References (94)

Cited By (13)

Similar Records

Related Subjects