Quantitative trait locus mapping combined with variant and transcriptome analyses identifies a cluster of gene candidates underlying the variation in leaf wax between upland and lowland switchgrass ecotypes

Qi, Peng; Pendergast, Thomas H.; Johnson, Alex; Bahri, Bochra A.; Choi, Soyeon; Missaoui, Ali; Devos, Katrien M.

doi:10.1007/s00122-021-03798-y

Title: Quantitative trait locus mapping combined with variant and transcriptome analyses identifies a cluster of gene candidates underlying the variation in leaf wax between upland and lowland switchgrass ecotypes

Journal Article · Wed Mar 24 00:00:00 EDT 2021 · Theoretical and Applied Genetics

DOI:https://doi.org/10.1007/s00122-021-03798-y· OSTI ID:1851432

^[1];

^[1]

Univ. of Georgia, Athens, GA (United States)

Switchgrass (Panicum virgatum L.) is a promising warm-season candidate energy crop. It occurs in two ecotypes, upland and lowland, which vary in a number of phenotypic traits, including leaf glaucousness. To initiate trait mapping, two F₂ mapping populations were developed by crossing two different F₁ sibs derived from a cross between the tetraploid lowland genotype AP13 and the tetraploid upland genotype VS16, and high-density linkage maps were generated. Quantitative trait locus (QTL) analyses of visually scored leaf glaucousness and of hydrophobicity of the abaxial leaf surface measured using a drop shape analyzer identified highly significant colocalizing QTL on chromosome 7K (Chr07K). Using a multipronged approach, we identified a cluster of genes including Pavir.7KG077009, which encodes a Type III polyketide synthase-like protein, and Pavir.7KG013754 and Pavir.7KG030500, two highly similar genes that encode putative acyl-acyl carrier protein (ACP) thioesterases, as strong candidates underlying the QTL. The lack of homoeologs for any of the three genes on Chr07N, the relatively low level of identity with other switchgrass KCS proteins and thioesterases, as well as the organization of the surrounding region suggest that Pavir.7KG077009 and Pavir.7KG013754/Pavir.7KG030500 were duplicated into a fast-evolving chromosome region, which led to their neofunctionalization. Furthermore, sequence analyses showed all three genes to be absent in the two upland compared to the two lowland accessions analyzed. This study provides an example of and practical guide for trait mapping and candidate gene identification in a complex genetic system by combining QTL mapping, transcriptomics and variant analysis.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Univ. of Georgia, Athens, GA (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

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

Grant/Contract Number:: SC0010743; AC05-00OR22725

OSTI ID:: 1851432

Journal Information:: Theoretical and Applied Genetics, Vol. 134, Issue 7; ISSN 0040-5752

Publisher:: Springer NatureCopyright Statement

Country of Publication:: United States

Language:: English

References (57)

Switchgrass selection as a “model” bioenergy crop: A history of the process Wright, Lynn; Turhollow, Anthony Biomass and Bioenergy, Vol. 34, Issue 6 https://doi.org/10.1016/j.biombioe.2010.01.030	journal	June 2010
Acyl-lipid thioesterase1–4 from Arabidopsis thaliana form a novel family of fatty acyl–acyl carrier protein thioesterases with divergent expression patterns and substrate specificities Pulsifer, Ian P.; Lowe, Christine; Narayaran, Swara A. Plant Molecular Biology, Vol. 84, Issue 4-5 https://doi.org/10.1007/s11103-013-0151-z	journal	November 2013
Chloroplast DNA and Nuclear DNA Content Variations among Cultivars of Switchgrass, Panicum virgatum L. Hultquist, Sherry J.; Vogel, K. P.; Lee, D. J. Crop Science, Vol. 36, Issue 4 https://doi.org/10.2135/cropsci1996.0011183X003600040039x	journal	January 1996
Enzymatic Functions of Wild Tomato Methylketone Synthases 1 and 2 Yu, Geng; Nguyen, Thuong T. H.; Guo, Yongxia Plant Physiology, Vol. 154, Issue 1 https://doi.org/10.1104/pp.110.157073	journal	July 2010
Epicuticular Wax and White Pine Blister Rust Resistance in Resistant and Susceptible Selections of Eastern White Pine ( Pinus strobus ) Smith, Jason A.; Blanchette, Robert A.; Burnes, Todd A. Phytopathology®, Vol. 96, Issue 2 https://doi.org/10.1094/PHYTO-96-0171	journal	February 2006
Perennial Forages as Second Generation Bioenergy Crops Sanderson, Matt; Adler, Paul International Journal of Molecular Sciences, Vol. 9, Issue 5 https://doi.org/10.3390/ijms9050768	journal	May 2008
Quantitative Trait Loci for Freezing Tolerance in a Lowland x Upland Switchgrass Population Poudel, Hari P.; Sanciangco, Millicent D.; Kaeppler, Shawn M. Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00372	journal	March 2019
Significance of the Expression of the CER6 Condensing Enzyme for Cuticular Wax Production in Arabidopsis Hooker, Tanya S.; Millar, Anthony A.; Kunst, Ljerka Plant Physiology, Vol. 129, Issue 4 https://doi.org/10.1104/pp.003707	journal	August 2002
Latitudinal and Longitudinal Adaptation of Switchgrass Populations Casler, M. D.; Vogel, K. P.; Taliaferro, C. M. Crop Science, Vol. 47, Issue 6 https://doi.org/10.2135/cropsci2006.12.0780	journal	January 2007
Switchgrass Genomic Diversity, Ploidy, and Evolution: Novel Insights from a Network-Based SNP Discovery Protocol Lu, Fei; Lipka, Alexander E.; Glaubitz, Jeff PLoS Genetics, Vol. 9, Issue 1 https://doi.org/10.1371/journal.pgen.1003215	journal	January 2013
A High-Density Simple Sequence Repeat-Based Genetic Linkage Map of Switchgrass Liu, Linglong; Wu, Yanqi; Wang, Yunwen G3: Genes\|Genomes\|Genetics, Vol. 2, Issue 3 https://doi.org/10.1534/g3.111.001503	journal	March 2012
Biomass Production in Switchgrass across the United States: Database Description and Determinants of Yield Wullschleger, S. D.; Davis, E. B.; Borsuk, M. E. Agronomy Journal, Vol. 102, Issue 4 https://doi.org/10.2134/agronj2010.0087	journal	January 2010
Complete Switchgrass Genetic Maps Reveal Subgenome Collinearity, Preferential Pairing and Multilocus Interactions Okada, Miki; Lanzatella, Christina; Saha, Malay C. Genetics, Vol. 185, Issue 3 https://doi.org/10.1534/genetics.110.113910	journal	April 2010
QTL × environment interactions underlie adaptive divergence in switchgrass across a large latitudinal gradient Lowry, David B.; Lovell, John T.; Zhang, Li Proceedings of the National Academy of Sciences, Vol. 116, Issue 26 https://doi.org/10.1073/pnas.1821543116	journal	June 2019
Disruption of the FATB Gene in Arabidopsis Demonstrates an Essential Role of Saturated Fatty Acids in Plant Growth Bonaventure, Gustavo; Salas, Joaquin J.; Pollard, Michael R. The Plant Cell, Vol. 15, Issue 4 https://doi.org/10.1105/tpc.008946	journal	March 2003
A Metabolic Gene Cluster in the Wheat W1 and the Barley Cer-cqu Loci Determines β-Diketone Biosynthesis and Glaucousness Hen-Avivi, Shelly; Savin, Orna; Racovita, Radu C. The Plant Cell, Vol. 28, Issue 6 https://doi.org/10.1105/tpc.16.00197	journal	May 2016
High‐density linkage map reveals QTL underlying growth traits in AP13×VS16 biparental population of switchgrass Ali, Shahjahan; Serba, Desalegn D.; Jenkins, Jerry GCB Bioenergy, Vol. 11, Issue 5 https://doi.org/10.1111/gcbb.12592	journal	January 2019
Cuticular wax variants in a population of switchgrass ( Panicum virgatum L.) Weaver, Joshua M.; Lohrey, Greg; Tomasi, Pernell Industrial Crops and Products, Vol. 117 https://doi.org/10.1016/j.indcrop.2018.02.081	journal	July 2018
Gene Clusters for Secondary Metabolic Pathways: An Emerging Theme in Plant Biology: Figure 1. Osbourn, Anne Plant Physiology, Vol. 154, Issue 2 https://doi.org/10.1104/pp.110.161315	journal	October 2010
Population genomic variation reveals roles of history, adaptation and ploidy in switchgrass Grabowski, Paul P.; Morris, Geoffrey P.; Casler, Michael D. Molecular Ecology, Vol. 23, Issue 16 https://doi.org/10.1111/mec.12845	journal	July 2014
Leaf Epicuticular Waxes of the Eceriferum Mutants in Arabidopsis Jenks, M. A.; Tuttle, H. A.; Eigenbrode, S. D. Plant Physiology, Vol. 108, Issue 1 https://doi.org/10.1104/pp.108.1.369	journal	May 1995
Linkage Maps of Lowland and Upland Tetraploid Switchgrass Ecotypes Serba, Desalegn; Wu, Limin; Daverdin, Guillaume BioEnergy Research, Vol. 6, Issue 3 https://doi.org/10.1007/s12155-013-9315-6	journal	March 2013
Efficient and Accurate Construction of Genetic Linkage Maps from the Minimum Spanning Tree of a Graph Wu, Yonghui; Bhat, Prasanna R.; Close, Timothy J. PLoS Genetics, Vol. 4, Issue 10 https://doi.org/10.1371/journal.pgen.1000212	journal	October 2008
Genetic engineering of grass cell wall polysaccharides for biorefining Bhatia, Rakesh; Gallagher, Joe A.; Gomez, Leonardo D. Plant Biotechnology Journal, Vol. 15, Issue 9 https://doi.org/10.1111/pbi.12764	journal	June 2017
Plants to power: bioenergy to fuel the future Yuan, Joshua S.; Tiller, Kelly H.; Al-Ahmad, Hani Trends in Plant Science, Vol. 13, Issue 8 https://doi.org/10.1016/j.tplants.2008.06.001	journal	August 2008
Rice OsGL1-6 Is Involved in Leaf Cuticular Wax Accumulation and Drought Resistance Zhou, Lingyan; Ni, Erdong; Yang, Jiawei PLoS ONE, Vol. 8, Issue 5 https://doi.org/10.1371/journal.pone.0065139	journal	May 2013
MAPMAKER: An interactive computer package for constructing primary genetic linkage maps of experimental and natural populations Lander, Eric S.; Green, Philip; Abrahamson, Jeff Genomics, Vol. 1, Issue 2 https://doi.org/10.1016/0888-7543(87)90010-3	journal	October 1987
Environmentally responsive QTL controlling surface wax load in switchgrass Bragg, Jennifer; Tomasi, Pernell; Zhang, Li Theoretical and Applied Genetics, Vol. 133, Issue 11 https://doi.org/10.1007/s00122-020-03659-0	journal	August 2020
Physiological Effects of Surface Waxes: I. Light Reflectance for Glaucous and Nonglaucous Picea pungens Reicosky, David A.; Hanover, James W. Plant Physiology, Vol. 62, Issue 1 https://doi.org/10.1104/pp.62.1.101	journal	July 1978
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
β-Diketones in Rhododendron waxes Evans, David; Knights, Brian A.; Math, Veerabhadracharya B. Phytochemistry, Vol. 14, Issue 11 https://doi.org/10.1016/0031-9422(75)80362-1	journal	November 1975
Genomic prediction accuracy for switchgrass traits related to bioenergy within differentiated populations Fiedler, Jason D.; Lanzatella, Christina; Edmé, Serge J. BMC Plant Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s12870-018-1360-z	journal	July 2018
Describing and Quantifying Growth Stages of Perennial Forage Grasses Moore, K. J.; Moser, L. E.; Vogel, K. P. Agronomy Journal, Vol. 83, Issue 6 https://doi.org/10.2134/agronj1991.00021962008300060027x	journal	January 1991
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
The development and current status of perennial rhizomatous grasses as energy crops in the US and Europe Lewandowski, Iris; Scurlock, Jonathan M. O.; Lindvall, Eva Biomass and Bioenergy, Vol. 25, Issue 4 https://doi.org/10.1016/S0961-9534(03)00030-8	journal	October 2003
Comparative Relationships and Chromosome Evolution in Switchgrass (Panicum virgatum) and Its Genomic Model, Foxtail Millet (Setaria italica) Daverdin, Guillaume; Bahri, Bochra A.; Wu, Xiaomei BioEnergy Research, Vol. 8, Issue 1 https://doi.org/10.1007/s12155-014-9508-7	journal	July 2014
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data McKenna, A.; Hanna, M.; Banks, E. Genome Research, Vol. 20, Issue 9 https://doi.org/10.1101/gr.107524.110	journal	July 2010
A β -Ketoacyl-CoA Synthase Is Involved in Rice Leaf Cuticular Wax Synthesis and Requires a CER2-LIKE Protein as a Cofactor Wang, Xiaochen; Guan, Yuanyuan; Zhang, Du Plant Physiology, Vol. 173, Issue 2 https://doi.org/10.1104/pp.16.01527	journal	December 2016
Genetic Linkage Mapping and Transmission Ratio Distortion in a Three-Generation Four-Founder Population of Panicum virgatum (L.) Li, Guifen; Serba, Desalegn D.; Saha, Malay C. G3: Genes\|Genomes\|Genetics, Vol. 4, Issue 5 https://doi.org/10.1534/g3.113.010165	journal	March 2014
QTL Mapping for Reproductive Maturity in Lowland Switchgrass Populations Dong, Hongxu; Thames, Shuiyi; Liu, Linglong BioEnergy Research, Vol. 8, Issue 4 https://doi.org/10.1007/s12155-015-9651-9	journal	July 2015
StringTie enables improved reconstruction of a transcriptome from RNA-seq reads Pertea, Mihaela; Pertea, Geo M.; Antonescu, Corina M. Nature Biotechnology, Vol. 33, Issue 3 https://doi.org/10.1038/nbt.3122	journal	February 2015
UGbS-Flex, a novel bioinformatics pipeline for imputation-free SNP discovery in polyploids without a reference genome: finger millet as a case study Qi, Peng; Gimode, Davis; Saha, Dipnarayan BMC Plant Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s12870-018-1316-3	journal	June 2018
Genome Size Reduction through Illegitimate Recombination Counteracts Genome Expansion in Arabidopsis Devos, K. M. Genome Research, Vol. 12, Issue 7 https://doi.org/10.1101/gr.132102	journal	July 2002
Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown Pertea, Mihaela; Kim, Daehwan; Pertea, Geo M. Nature Protocols, Vol. 11, Issue 9 https://doi.org/10.1038/nprot.2016.095	journal	August 2016
MapChart: Software for the Graphical Presentation of Linkage Maps and QTLs Voorrips, R. E. Journal of Heredity, Vol. 93, Issue 1 https://doi.org/10.1093/jhered/93.1.77	journal	January 2002
Anti-adhesive effects of plant wax coverage on insect attachment Gorb, Elena V.; Gorb, Stanislav N. Journal of Experimental Botany, Vol. 68, Issue 19 https://doi.org/10.1093/jxb/erx271	journal	August 2017
Translational genomics using Arabidopsis as a model enables the characterization of pennycress genes through forward and reverse genetics Chopra, Ratan; Johnson, Evan B.; Daniels, Erin The Plant Journal, Vol. 96, Issue 6 https://doi.org/10.1111/tpj.14147	journal	December 2018
Second generation bioenergy crops and climate change: a review of the effects of elevated atmospheric CO ₂ and drought on water use and the implications for yield Oliver, Rebecca J.; Finch, Jon W.; Taylor, Gail GCB Bioenergy, Vol. 1, Issue 2 https://doi.org/10.1111/j.1757-1707.2009.01011.x	journal	April 2009
Protecting against water loss: analysis of the barrier properties of plant cuticles Riederer, Markus; Schreiber, Lukas Journal of Experimental Botany, Vol. 52, Issue 363 https://doi.org/10.1093/jexbot/52.363.2023	journal	October 2001
Epicuticular wax of Panicum virgatum Tulloch, Alexander P.; Hoffman, Leslie L. Phytochemistry, Vol. 19, Issue 5 https://doi.org/10.1016/0031-9422(80)85122-3	journal	January 1980
Quantitative Trait Loci (QTL) Underlying Biomass Yield and Plant Height in Switchgrass Serba, Desalegn D.; Daverdin, Guillaume; Bouton, Joseph H. BioEnergy Research, Vol. 8, Issue 1 https://doi.org/10.1007/s12155-014-9523-8	journal	August 2014
Answering a four decade-old question on epicuticular wax biosynthesis Kosma, Dylan K.; Rowland, Owen Journal of Experimental Botany, Vol. 67, Issue 9 https://doi.org/10.1093/jxb/erw144	journal	April 2016
HISAT: a fast spliced aligner with low memory requirements Kim, Daehwan; Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 12, Issue 4 https://doi.org/10.1038/nmeth.3317	journal	March 2015
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
Cytological and Morphological Variation in Panicum virgatum L. Brunken, Jere N.; Estes, James R. The Southwestern Naturalist, Vol. 19, Issue 4 https://doi.org/10.2307/3670396	journal	January 1975
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
Cuticular Wax Accumulation Is Associated with Drought Tolerance in Wheat Near-Isogenic Lines Guo, Jun; Xu, Wen; Yu, Xiaocong Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.01809	journal	November 2016

Similar Records

Unraveling the Genetics of Two Key Biomass Traits that Differentiate Upland and Lowland Tetraploid Switchgrass Ecotypes, Colonization by Mycorrhizal Fungi and Frost Tolerance

Technical Report · Mon Dec 14 00:00:00 EST 2020 · OSTI ID:1851432

Devos, Katrien; Bennetzen, Jeff; Lindstrom, Orville; +2 more

Cell Wall Composition and Underlying QTL in an F1 Pseudo-Testcross Population of Switchgrass

Journal Article · Sat Apr 23 00:00:00 EDT 2016 · BioEnergy Research · OSTI ID:1851432

Serba, Desalegn D.; Sykes, Robert W.; Gjersing, Erica L.; +5 more

Quantitative trait loci (QTL) underlying biomass yield and plant height in switchgrass

Journal Article · Sat Aug 30 00:00:00 EDT 2014 · BioEnergy Research · OSTI ID:1851432

Serba, Desalegn D.; Daverdin, Guillaume; Bouton, Joseph H.; +3 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Agriculture
Plant sciences
Genetics & heredity

Title: Quantitative trait locus mapping combined with variant and transcriptome analyses identifies a cluster of gene candidates underlying the variation in leaf wax between upland and lowland switchgrass ecotypes

Citation Formats

References (57)

Similar Records

Related Subjects