The genetic basis for panicle trait variation in switchgrass (Panicum virgatum)

Zhang, Li; MacQueen, Alice; Weng, Xiaoyu; Behrman, Kathrine D.; Bonnette, Jason; Reilley, John L.; Rouquette, Jr., Francis M.; Fay, Philip A.; Wu, Yanqi; Fritschi, Felix B.; Mitchell, Robert B.; Lowry, David B.; Boe, Arvid R.; Juenger, Thomas E.

doi:10.1007/s00122-022-04096-x

The genetic basis for panicle trait variation in switchgrass (Panicum virgatum)

Journal Article · Sat Jul 02 00:00:00 EDT 2022 · Theoretical and Applied Genetics

DOI:https://doi.org/10.1007/s00122-022-04096-x· OSTI ID:1893936

^[1]; MacQueen, Alice ^[2]; Weng, Xiaoyu ^[2]; Behrman, Kathrine D. ^[2]; Bonnette, Jason ^[2]; Reilley, John L. ^[3]; Rouquette, Jr., Francis M. ^[4]; Fay, Philip A. ^[5]; Wu, Yanqi ^[6]; Fritschi, Felix B. ^[7]; Mitchell, Robert B. ^[8]; Lowry, David B. ^[9]; Boe, Arvid R. ^[10]; ^[2]

Univ. of Texas, Austin, TX (United States); University of Texas at Austin Department of Integrative Biology
Univ. of Texas, Austin, TX (United States)
US Department of Agriculture, Kingsville, TX (United States)
Texas A & M Univ., Overton, TX (United States)
US Dept. of Agriculture, Temple, TX (United States)
Oklahoma State Univ., Stillwater, OK (United States)
Univ. of Missouri, Columbia, MO (United States)
Univ. of Nebraska, Lincoln, NE (United States)
Michigan State Univ., East Lansing, MI (United States)
South Dakota State Univ., Brookings, SD (United States)

Grass species exhibit large diversity in panicle architecture influenced by genes, the environment, and their interaction. The genetic study of panicle architecture in perennial grasses is limited. In this study, we evaluate the genetic basis of panicle architecture including panicle length, primary branching number, and secondary branching number in an outcrossed switchgrass QTL population grown across ten field sites in the central USA through multi-environment mixed QTL analysis. We also evaluate genetic effects in a diversity panel of switchgrass grown at three of the ten field sites using genome-wide association (GWAS) and multivariate adaptive shrinkage. Furthermore, we search for candidate genes underlying panicle traits in both of these independent mapping populations. Overall, 18 QTL were detected in the QTL mapping population for the three panicle traits, and 146 unlinked genomic regions in the diversity panel affected one or more panicle trait. Twelve of the QTL exhibited consistent effects (i.e., no QTL by environment interactions or no QTL × E), and most (four of six) of the effects with QTL × E exhibited site-specific effects. Most (59.3%) significant partially linked diversity panel SNPs had significant effects in all panicle traits and all field sites and showed pervasive pleiotropy and limited environment interactions. Panicle QTL co-localized with significant SNPs found using GWAS, providing additional power to distinguish between true and false associations in the diversity panel.

View Accepted Manuscript (DOE)

Research Organization:: Great Lakes Bioenergy Research Center, Madison, WI (United States); Univ. of Texas, Austin, TX (United States)

Sponsoring Organization:: National Science Foundation Plant Genome Research Program; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: FC02-07ER64494; SC0014156; SC0018409

OSTI ID:: 1893936

Journal Information:: Theoretical and Applied Genetics, Journal Name: Theoretical and Applied Genetics Journal Issue: 8 Vol. 135; ISSN 0040-5752

Publisher:: Springer NatureCopyright Statement

Country of Publication:: United States

Language:: English

References (65)

Switchgrass v5 4-way (AP13 x DAC, WBC x VS16) genetic map Lovell, John; Healey, Adam; Schmutz, Jeremy Dryad https://doi.org/10.5061/dryad.ghx3ffbjv	dataset	January 2019
Inheritance of inflorescence architecture in sorghum Brown, P. J.; Klein, P. E.; Bortiri, E. Theoretical and Applied Genetics, Vol. 113, Issue 5 https://doi.org/10.1007/s00122-006-0352-9	journal	July 2006
Detection of QTLs with additive effects and additive-by-environment interaction effects on panicle number in rice (Oryza sativa L.) with single-segment substitution lines Liu, Guifu; Zhang, Zemin; Zhu, Haitao Theoretical and Applied Genetics, Vol. 116, Issue 7 https://doi.org/10.1007/s00122-008-0724-4	journal	February 2008
Genetic dissection of wheat panicle traits using linkage analysis and a genome-wide association study Liu, Kai; Sun, Xiaoxiao; Ning, Tangyuan Theoretical and Applied Genetics, Vol. 131, Issue 5 https://doi.org/10.1007/s00122-018-3059-9	journal	February 2018
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
Genetic variability and interrelationships of seed yield and yield components in switchgrass Das, Modan K.; Taliaferro, Charles M. Euphytica, Vol. 167, Issue 1 https://doi.org/10.1007/s10681-008-9866-3	journal	January 2009
Genome-wide association study to identify chromosomal regions related to panicle architecture in rice (Oryza sativa) Thapa, Ranjita; Tabien, Rodante E.; Septiningsih, Endang M. Genetic Resources and Crop Evolution, Vol. 68, Issue 7 https://doi.org/10.1007/s10722-021-01159-8	journal	March 2021
The Plant Architecture of Rice (Oryza sativa) Wang, Yonghong; Li, Jiayang Plant Molecular Biology, Vol. 59, Issue 1 https://doi.org/10.1007/s11103-004-4038-x	journal	September 2005
Biomass energy production in the United States: an overview Hohenstein, William G.; Wright, Lynn L. Biomass and Bioenergy, Vol. 6, Issue 3 https://doi.org/10.1016/0961-9534(94)90073-6	journal	January 1994
Grass inflorescence architecture and meristem determinacy Bommert, Peter; Whipple, Clinton Seminars in Cell & Developmental Biology, Vol. 79 https://doi.org/10.1016/j.semcdb.2017.10.004	journal	July 2018
Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling Dai, Cheng; Xue, Hong-Wei The EMBO Journal, Vol. 29, Issue 11 https://doi.org/10.1038/emboj.2010.75	journal	April 2010
The role of barren stalk1 in the architecture of maize Gallavotti, Andrea; Zhao, Qiong; Kyozuka, Junko Nature, Vol. 432, Issue 7017 https://doi.org/10.1038/nature03148	journal	December 2004
Architecture of floral branch systems in maize and related grasses Vollbrecht, Erik; Springer, Patricia S.; Goh, Lindee Nature, Vol. 436, Issue 7054 https://doi.org/10.1038/nature03892	journal	July 2005
Genome-wide association and high-resolution phenotyping link Oryza sativa panicle traits to numerous trait-specific QTL clusters Crowell, Samuel; Korniliev, Pavel; Falcão, Alexandre Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms10527	journal	February 2016
OsSPL14 promotes panicle branching and higher grain productivity in rice Miura, Kotaro; Ikeda, Mayuko; Matsubara, Atsushi Nature Genetics, Vol. 42, Issue 6 https://doi.org/10.1038/ng.592	journal	May 2010
Principal components analysis corrects for stratification in genome-wide association studies Price, Alkes L.; Patterson, Nick J.; Plenge, Robert M. Nature Genetics, Vol. 38, Issue 8 https://doi.org/10.1038/ng1847	journal	July 2006
The effect of artificial selection on phenotypic plasticity in maize Gage, Joseph L.; Jarquin, Diego; Romay, Cinta Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01450-2	journal	November 2017
Genomic mechanisms of climate adaptation in polyploid bioenergy switchgrass Lovell, John T.; MacQueen, Alice H.; Mamidi, Sujan Nature, Vol. 590, Issue 7846 https://doi.org/10.1038/s41586-020-03127-1	journal	January 2021
Flexible statistical methods for estimating and testing effects in genomic studies with multiple conditions Urbut, Sarah M.; Wang, Gao; Carbonetto, Peter Nature Genetics, Vol. 51, Issue 1 https://doi.org/10.1038/s41588-018-0268-8	journal	November 2018
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
Patterns of Phenotypic Plasticity and Their Fitness Consequences in Wild Radish (Raphanus sativus: Brassicaceae) Wolfe, Lorne M.; Mazer, Susan J. International Journal of Plant Sciences, Vol. 166, Issue 4 https://doi.org/10.1086/430194	journal	July 2005
Architectural Evolution and its Implications for Domestication in Grasses Doust, A. Annals of Botany, Vol. 100, Issue 5 https://doi.org/10.1093/aob/mcm040	journal	July 2007
Efficient toolkit implementing best practices for principal component analysis of population genetic data Privé, Florian; Luu, Keurcien; Blum, Michael G. B. Bioinformatics, Vol. 36, Issue 16 https://doi.org/10.1093/bioinformatics/btaa520	journal	May 2020
Efficient analysis of large-scale genome-wide data with two R packages: bigstatsr and bigsnpr Privé, Florian; Aschard, Hugues; Ziyatdinov, Andrey Bioinformatics, Vol. 34, Issue 16 https://doi.org/10.1093/bioinformatics/bty185	journal	March 2018
Modulation of plant architecture by the miR156f–OsSPL7–OsGH3.8 pathway in rice Dai, Zhengyan; Wang, Jiang; Yang, Xiaofang Journal of Experimental Botany, Vol. 69, Issue 21 https://doi.org/10.1093/jxb/ery273	journal	July 2018
FLOR-ID: an interactive database of flowering-time gene networks in Arabidopsis thaliana Bouché, Frédéric; Lobet, Guillaume; Tocquin, Pierre Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1054	journal	October 2015
Branching Out: The ramosa Pathway and the Evolution of Grass Inflorescence Morphology McSteen, Paula The Plant Cell, Vol. 18, Issue 3 https://doi.org/10.1105/tpc.105.040196	journal	March 2006
TEOSINTE BRANCHED1 Regulates Inflorescence Architecture and Development in Bread Wheat (Triticum aestivum) Dixon, Laura E.; Greenwood, Julian R.; Bencivenga, Stefano The Plant Cell, Vol. 30, Issue 3 https://doi.org/10.1105/tpc.17.00961	journal	February 2018
Identifying targets and agents of selection: innovative methods to evaluate the processes that contribute to local adaptation Wadgymar, Susana M.; Lowry, David B.; Gould, Billie A. Methods in Ecology and Evolution, Vol. 8, Issue 6 https://doi.org/10.1111/2041-210X.12777	journal	June 2017
Inflorescence architecture and wind pollination in six grass species Friedman, Jannice; Harder, Lawrence D. Functional Ecology, Vol. 18, Issue 6 https://doi.org/10.1111/j.0269-8463.2004.00921.x	journal	December 2004
Phenotypic plasticity of vegetative and reproductive traits in monoecious and dioecious populations ofSagittaria latifolia(Alismataceae): a clonal aquatic plant Dorken, Marcel E.; Barrett, Spencer C. H. Journal of Ecology, Vol. 92, Issue 1 https://doi.org/10.1111/j.1365-2745.2004.00857.x	journal	January 2004
A comparative view of the evolution of grasses under domestication: Tansley review Glémin, Sylvain; Bataillon, Thomas New Phytologist, Vol. 183, Issue 2 https://doi.org/10.1111/j.1469-8137.2009.02884.x	journal	June 2009
Genome-wide associations with flowering time in switchgrass using exome-capture sequencing data Grabowski, Paul P.; Evans, Joseph; Daum, Chris New Phytologist, Vol. 213, Issue 1 https://doi.org/10.1111/nph.14101	journal	July 2016
Gibberellins orchestrate panicle architecture mediated by DELLA–KNOX signalling in rice Su, Su; Hong, Jun; Chen, Xiaofei Plant Biotechnology Journal, Vol. 19, Issue 11 https://doi.org/10.1111/pbi.13661	journal	August 2021
H d16 , a gene for casein kinase I , is involved in the control of rice flowering time by modulating the day‐length response Hori, Kiyosumi; Ogiso‐Tanaka, Eri; Matsubara, Kazuki The Plant Journal, Vol. 76, Issue 1 https://doi.org/10.1111/tpj.12268	journal	July 2013
Cellulosic biofuel contributions to a sustainable energy future: Choices and outcomes Robertson, G. Philip; Hamilton, Stephen K.; Barham, Bradford L. Science, Vol. 356, Issue 6345 https://doi.org/10.1126/science.aal2324	journal	June 2017
Genotype-by-Environment Interaction and Plasticity: Exploring Genomic Responses of Plants to the Abiotic Environment Des Marais, David L.; Hernandez, Kyle M.; Juenger, Thomas E. Annual Review of Ecology, Evolution, and Systematics, Vol. 44, Issue 1 https://doi.org/10.1146/annurev-ecolsys-110512-135806	journal	November 2013
On estimation of genetic variance within families using genome-wide identity-by-descent sharing Hill, William G. Genetics Selection Evolution, Vol. 45, Issue 1 https://doi.org/10.1186/1297-9686-45-32	journal	September 2013
Rice panicle plasticity in Near Isogenic Lines carrying a QTL for larger panicle is genotype and environment dependent Adriani, Dewi Erika; Dingkuhn, Michael; Dardou, Audrey Rice, Vol. 9, Issue 1 https://doi.org/10.1186/s12284-016-0101-x	journal	June 2016
Uncovering the genetic mechanisms regulating panicle architecture in rice with GPWAS and GWAS Zhong, Hua; Liu, Shuai; Meng, Xiaoxi BMC Genomics, Vol. 22, Issue 1 https://doi.org/10.1186/s12864-021-07391-x	journal	January 2021
A genome-wide association study using a Vietnamese landrace panel of rice (Oryza sativa) reveals new QTLs controlling panicle morphological traits Ta, Kim Nhung; Khong, Ngan Giang; Ha, Thi Loan BMC Plant Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s12870-018-1504-1	journal	November 2018
barren inflorescence2 regulates axillary meristem development in the maize inflorescence McSteen, Paula; Hake, Sarah Development, Vol. 128, Issue 15 https://doi.org/10.1242/dev.128.15.2881	journal	August 2001
Evolution of flowers and inflorescences Coen, Enrico S.; Nugent, Jacqueline M. Development, Vol. 1994, Issue Supplement https://doi.org/10.1242/dev.1994.Supplement.107	journal	January 1994
Linkage and Association Mapping of Arabidopsis thaliana Flowering Time in Nature Brachi, Benjamin; Faure, Nathalie; Horton, Matt PLoS Genetics, Vol. 6, Issue 5 https://doi.org/10.1371/journal.pgen.1000940	journal	May 2010
Genome-Assisted Prediction of Quantitative Traits Using the R Package sommer Covarrubias-Pazaran, Giovanny PLOS ONE, Vol. 11, Issue 6 https://doi.org/10.1371/journal.pone.0156744	journal	June 2016
The Genetic Basis of Upland/Lowland Ecotype Divergence in Switchgrass ( Panicum virgatum) Milano, Elizabeth R.; Lowry, David B.; Juenger, Thomas E. G3: Genes\|Genomes\|Genetics, Vol. 6, Issue 11 https://doi.org/10.1534/g3.116.032763	journal	September 2016
The Genetic Basis for Inflorescence Variation Between Foxtail and Green Millet (Poaceae) Doust, Andrew N.; Devos, Katrien M.; Gadberry, Mike D. Genetics, Vol. 169, Issue 3 https://doi.org/10.1534/genetics.104.035543	journal	January 2005
Selection During Maize Domestication Targeted a Gene Network Controlling Plant and Inflorescence Architecture Studer, Anthony J.; Wang, Huai; Doebley, John F. Genetics, Vol. 207, Issue 2 https://doi.org/10.1534/genetics.117.300071	journal	July 2017
Genotypic Variability and Genotype × Environment Interactions among Switchgrass Accessions from the Midwestern USA Hopkins, Andrew A.; Vogel, K. P.; Moore, K. J. Crop Science, Vol. 35, Issue 2 https://doi.org/10.2135/cropsci1995.0011183X003500020047x	journal	January 1995
Variation between Alamo and Cave‐in‐Rock Switchgrass in Response to Photoperiod Extension van Esbroeck, G. A.; Hussey, M. A.; Sanderson, M. A. Crop Science, Vol. 43, Issue 2 https://doi.org/10.2135/cropsci2003.6390	journal	March 2003
Genetic Diversity, Plant Adaptation Regions, and Gene Pools for Switchgrass Casler, Michael D.; Stendal, Chad A.; Kapich, Ludmila Crop Science, Vol. 47, Issue 6 https://doi.org/10.2135/cropsci2006.12.0797	journal	January 2007
Predictive Relationships between Plant Morphological Traits and Biomass Yield in Switchgrass Price, David L.; Casler, Michael D. Crop Science, Vol. 54, Issue 2 https://doi.org/10.2135/cropsci2013.04.0272	journal	March 2014
An Analysis of Variation Between Upland and Lowland Switchgrass, Panicum Virgatum L., in Central Oklahoma Porter, Clyde L. Ecology, Vol. 47, Issue 6 https://doi.org/10.2307/1935646	journal	November 1966
Floral plasticity in an iteroparous plant: the interactive effects of genotype, environment, and ontogeny in Campanula rapunculoides (Campanulaceae) Vogler, Donna W.; Peretz, Shani; Stephenson, Andrew G. American Journal of Botany, Vol. 86, Issue 4 https://doi.org/10.2307/2656809	journal	April 1999
The statistical analysis of multi-environment data: modeling genotype-by-environment interaction and its genetic basis Malosetti, Marcos; Ribaut, Jean-Marcel; van Eeuwijk, Fred A. Frontiers in Physiology, Vol. 4 https://doi.org/10.3389/fphys.2013.00044	journal	January 2013
Genome-Wide Association Mapping Identifies Novel Panicle Morphology Loci and Candidate Genes in Sorghum Wang, Lihua; Upadhyaya, Hari D.; Zheng, Jian Frontiers in Plant Science, Vol. 12 https://doi.org/10.3389/fpls.2021.743838	journal	October 2021
Hd16, a gene for casein kinase I, is involved in the control of rice flowering time by modulating the day-length response. Hori, K. The Plant Journal: for Cell and Molecular Biology https://doi.org/10.3410/f.718022925.793479306	journal	October 2013
Inflorescence diversification in the panicoid “bristle grass” clade (Paniceae, Poaceae): evidence from molecular phylogenies and developmental morphology Doust, Andrew N.; Kellogg, Elizabeth A. American Journal of Botany, Vol. 89, Issue 8 https://doi.org/10.3732/ajb.89.8.1203	journal	August 2002
Phenotypic plasticity in vegetative and reproductive traits in an invasive weed, Lythrum salicaria (Lythraceae), in response to soil moisture Mal, T. K.; Lovett-Doust, J. American Journal of Botany, Vol. 92, Issue 5 https://doi.org/10.3732/ajb.92.5.819	journal	May 2005
Plasticity of inflorescence traits in Lobelia siphilitica (Lobeliaceae) in response to soil water availability Caruso, C. M. American Journal of Botany, Vol. 93, Issue 4 https://doi.org/10.3732/ajb.93.4.531	journal	April 2006
Genome-Wide Association Study for Nine Plant Architecture Traits in Sorghum Zhao, Jing; Mantilla Perez, Maria B.; Hu, Jieyun The Plant Genome, Vol. 9, Issue 2 https://doi.org/10.3835/plantgenome2015.06.0044	journal	January 2016
Genome‐Wide Association Analysis Reveals Different Genetic Control in Panicle Architecture Between Indica and Japonica Rice Bai, Xufeng; Zhao, Hu; Huang, Yong The Plant Genome, Vol. 9, Issue 2 https://doi.org/10.3835/plantgenome2015.11.0115	journal	July 2016
The feasibility of switchgrass for biofuel production Mitchell, Rob; Vogel, Kenneth P.; Uden, Daniel R. Biofuels, Vol. 3, Issue 1 https://doi.org/10.4155/bfs.11.153	journal	January 2012
QTL × environment interactions underlie adaptive divergence in switchgrass across a large latitudinal gradient Lowry, David; Lovell, John; Zhang, Li Dryad https://doi.org/10.5061/dryad.h70rxwdgj	dataset	January 2020
Rice panicle plasticity in Near Isogenic Lines carrying a QTL for larger panicle is genotype and environment dependent Adriani, Dewi; Dingkuhn, Michael; Dardou, Audrey Figshare https://doi.org/10.6084/m9.figshare.c.3599297	collection	January 2016

Similar Records

Meta-analysis identifies pleiotropic loci controlling phenotypic trade-offs in sorghum

Journal Article · Mon Jun 07 20:00:00 EDT 2021 · Genetics (Online) · OSTI ID:1808016

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

The genetic basis for panicle trait variation in switchgrass (Panicum virgatum)

Citation Formats

References (65)

Similar Records

Related Subjects