A single amino acid change led to structural and functional differentiation of PvHd1 to control flowering in switchgrass

Choi, Soyeon; Prabhakar, Pradeep K.; Chowdhury, Ratul; Pendergast, IV, Thomas H.; Urbanowicz, Breeanna R.; Maranas, Costas; Devos, Katrien M.; Melzer, ed., Rainer

doi:10.1093/jxb/erad255

Title: A single amino acid change led to structural and functional differentiation of PvHd1 to control flowering in switchgrass

Journal Article · 03 July 2023 · Journal of Experimental Botany

DOI: https://doi.org/10.1093/jxb/erad255 · OSTI ID:2007119

;

; Melzer, ed., Rainer

Abstract Switchgrass, a forage and bioenergy crop, occurs as two main ecotypes with different but overlapping ranges of adaptation. The two ecotypes differ in a range of characteristics, including flowering time. Flowering time determines the duration of vegetative development and therefore biomass accumulation, a key trait in bioenergy crops. No causal variants for flowering time differences between switchgrass ecotypes have, as yet, been identified. In this study, we mapped a robust flowering time quantitative trait locus (QTL) on chromosome 4K in a biparental F2 population and characterized the flowering-associated transcription factor gene PvHd1, an ortholog of CONSTANS in Arabidopsis and Heading date 1 in rice, as the underlying causal gene. Protein modeling predicted that a serine to glycine substitution at position 35 (p.S35G) in B-Box domain 1 greatly altered the global structure of the PvHd1 protein. The predicted variation in protein compactness was supported in vitro by a 4 °C shift in denaturation temperature. Overexpressing the PvHd1-p.35S allele in a late-flowering CONSTANS-null Arabidopsis mutant rescued earlier flowering, whereas PvHd1-p.35G had a reduced ability to promote flowering, demonstrating that the structural variation led to functional divergence. Our findings provide us with a tool to manipulate the timing of floral transition in switchgrass cultivars and, potentially, expand their cultivation range.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation (CBI)

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

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 2007119

Journal Information:: Journal of Experimental Botany, Journal Name: Journal of Experimental Botany Journal Issue: 18 Vol. 74; ISSN 0022-0957

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (60)

Transcriptome profiling reveals differentially expressed genes associated with flowering time in contrasting switchgrass genotypes Taylor, Megan; Zhao, Xiongwei; Casler, Michael D. Crop Science, Vol. 60, Issue 3 https://doi.org/10.1002/csc2.20083	journal	April 2020
Scalable molecular dynamics with NAMD Phillips, James C.; Braun, Rosemary; Wang, Wei Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802 https://doi.org/10.1002/jcc.20289	journal	January 2005
CHARMM36 all-atom additive protein force field: Validation based on comparison to NMR data Huang, Jing; MacKerell, Alexander D. Journal of Computational Chemistry, Vol. 34, Issue 25 https://doi.org/10.1002/jcc.23354	journal	July 2013
The Iterative Protein Redesign and Optimization (IPRO) suite of programs Pantazes, Robert J.; Grisewood, Matthew J.; Li, Tong Journal of Computational Chemistry, Vol. 36, Issue 4 https://doi.org/10.1002/jcc.23796	journal	December 2014
A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana Koornneef, M.; Hanhart, C. J.; van der Veen, J. H. Molecular and General Genetics MGG, Vol. 229, Issue 1 https://doi.org/10.1007/BF00264213	journal	September 1991
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 Theoretical and Applied Genetics, Vol. 134, Issue 7 https://doi.org/10.1007/s00122-021-03798-y	journal	March 2021
A maize CONSTANS-like gene, conz1, exhibits distinct diurnal expression patterns in varied photoperiods Miller, Theresa A.; Muslin, Elizabeth H.; Dorweiler, Jane E. Planta, Vol. 227, Issue 6 https://doi.org/10.1007/s00425-008-0709-1	journal	February 2008
Transcriptional Analysis of Flowering Time in Switchgrass Tornqvist, Carl-Erik; Vaillancourt, Brieanne; Kim, Jeongwoon BioEnergy Research, Vol. 10, Issue 3 https://doi.org/10.1007/s12155-017-9832-9	journal	April 2017
Photoperiodic Flowering Regulation in Arabidopsis thaliana Golembeski, Greg S.; Kinmonth-Schultz, Hannah A.; Song, Young Hun The Molecular Genetics of Floral Transition and Flower Development https://doi.org/10.1016/B978-0-12-417162-6.00001-8	book	January 2014
Nonsense-mediated mRNA decay: terminating erroneous gene expression Baker, Kristian E.; Parker, Roy Current Opinion in Cell Biology, Vol. 16, Issue 3 https://doi.org/10.1016/j.ceb.2004.03.003	journal	June 2004
Analysis of promoter activity reveals that GmFTL2 expression differs from that of the known Flowering Locus T genes in soybean Liu, Limin; Zhang, Xiaomei; Chen, Fulu The Crop Journal, Vol. 5, Issue 5 https://doi.org/10.1016/j.cj.2017.03.004	journal	October 2017
Stepwise cis-Regulatory Changes in ZCN8 Contribute to Maize Flowering-Time Adaptation Guo, Li; Wang, Xuehan; Zhao, Min Current Biology, Vol. 28, Issue 18 https://doi.org/10.1016/j.cub.2018.07.029	journal	September 2018
Atomic-Level Protein Structure Refinement Using Fragment-Guided Molecular Dynamics Conformation Sampling Zhang, Jian; Liang, Yu; Zhang, Yang Structure, Vol. 19, Issue 12 https://doi.org/10.1016/j.str.2011.09.022	journal	December 2011
Structure of the MID1 Tandem B-Boxes Reveals an Interaction Reminiscent of Intermolecular Ring Heterodimers^, Tao, Hu; Simmons, Brandi N.; Singireddy, Suryaparkash Biochemistry, Vol. 47, Issue 8 https://doi.org/10.1021/bi7018496	journal	January 2008
CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis Suárez-López, Paula; Wheatley, Kay; Robson, Frances Nature, Vol. 410, Issue 6832 https://doi.org/10.1038/35074138	journal	April 2001
Adaptation of photoperiodic control pathways produces short-day flowering in rice Hayama, Ryosuke; Yokoi, Shuji; Tamaki, Shojiro Nature, Vol. 422, Issue 6933 https://doi.org/10.1038/nature01549	journal	April 2003
The I-TASSER Suite: protein structure and function prediction Yang, Jianyi; Yan, Renxiang; Roy, Ambrish Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3213	journal	December 2014
Quality and quantity control of gene expression by nonsense-mediated mRNA decay Kurosaki, Tatsuaki; Popp, Maximilian W.; Maquat, Lynne E. Nature Reviews Molecular Cell Biology, Vol. 20, Issue 7 https://doi.org/10.1038/s41580-019-0126-2	journal	April 2019
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
Highly accurate protein structure prediction with AlphaFold Jumper, John; Evans, Richard; Pritzel, Alexander Nature https://doi.org/10.1038/s41586-021-03819-2	journal	July 2021
Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype Kim, Daehwan; Paggi, Joseph M.; Park, Chanhee Nature Biotechnology, Vol. 37, Issue 8 https://doi.org/10.1038/s41587-019-0201-4	journal	August 2019
Single-sequence protein structure prediction using a language model and deep learning Chowdhury, Ratul; Bouatta, Nazim; Biswas, Surojit Nature Biotechnology, Vol. 40, Issue 11 https://doi.org/10.1038/s41587-022-01432-w	journal	October 2022
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana Clough, Steven J.; Bent, Andrew F. The Plant Journal, Vol. 16, Issue 6, p. 735-743 https://doi.org/10.1046/j.1365-313x.1998.00343.x	journal	December 1998
GIGANTEA directly activates Flowering Locus T in Arabidopsis thaliana Sawa, Mariko; Kay, Steve A. Proceedings of the National Academy of Sciences, Vol. 108, Issue 28 https://doi.org/10.1073/pnas.1106771108	journal	June 2011
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
A New Method for Quantitative Real-Time Polymerase Chain Reaction Data Analysis Rao, Xiayu; Lai, Dejian; Huang, Xuelin Journal of Computational Biology, Vol. 20, Issue 9 https://doi.org/10.1089/cmb.2012.0279	journal	September 2013
Nonsense-mediated mRNA decay: from mechanistic insights to impacts on human health Palacios, I. M. Briefings in Functional Genomics, Vol. 12, Issue 1 https://doi.org/10.1093/bfgp/els051	journal	November 2012
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
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data Robinson, M. D.; McCarthy, D. J.; Smyth, G. K. Bioinformatics, Vol. 26, Issue 1 https://doi.org/10.1093/bioinformatics/btp616	journal	November 2009
IUPred3: prediction of protein disorder enhanced with unambiguous experimental annotation and visualization of evolutionary conservation Erdős, Gábor; Pajkos, Mátyás; Dosztányi, Zsuzsanna Nucleic Acids Research, Vol. 49, Issue W1 https://doi.org/10.1093/nar/gkab408	journal	May 2021
SWISS-MODEL: homology modelling of protein structures and complexes Waterhouse, Andrew; Bertoni, Martino; Bienert, Stefan Nucleic Acids Research, Vol. 46, Issue W1 https://doi.org/10.1093/nar/gky427	journal	May 2018
Hd3a, a Rice Ortholog of the Arabidopsis FT Gene, Promotes Transition to Flowering Downstream of Hd1 under Short-Day Conditions Kojima, Shoko; Takahashi, Yuji; Kobayashi, Yasushi Plant and Cell Physiology, Vol. 43, Issue 10 https://doi.org/10.1093/pcp/pcf156	journal	October 2002
Structural insights into the multivalent binding of the Arabidopsis FLOWERING LOCUS T promoter by the CO–NF–Y master transcription factor complex Lv, Xinchen; Zeng, Xiaolin; Hu, Hongmiao The Plant Cell, Vol. 33, Issue 4 https://doi.org/10.1093/plcell/koab016	journal	January 2021
Control of Flowering Time: Interacting Pathways as a Basis for Diversity Mouradov, Aidyn; Cremer, Frédéric; Coupland, George The Plant Cell, Vol. 14, Issue suppl 1 https://doi.org/10.1105/tpc.001362	journal	May 2002
CONSTANS and the CCAAT Box Binding Complex Share a Functionally Important Domain and Interact to Regulate Flowering of Arabidopsis Wenkel, Stephan; Turck, Franziska; Singer, Kamy The Plant Cell, Vol. 18, Issue 11 https://doi.org/10.1105/tpc.106.043299	journal	November 2006
The FT -Like ZCN8 Gene Functions as a Floral Activator and Is Involved in Photoperiod Sensitivity in Maize Meng, Xin; Muszynski, Michael G.; Danilevskaya, Olga N. The Plant Cell, Vol. 23, Issue 3 https://doi.org/10.1105/tpc.110.081406	journal	March 2011
A Distal CCAAT/NUCLEAR FACTOR Y Complex Promotes Chromatin Looping at the FLOWERING LOCUS T Promoter and Regulates the Timing of Flowering in Arabidopsis Cao, Shuanghe; Kumimoto, Roderick W.; Gnesutta, Nerina The Plant Cell, Vol. 26, Issue 3 https://doi.org/10.1105/tpc.113.120352	journal	March 2014
Hd1 , a Major Photoperiod Sensitivity Quantitative Trait Locus in Rice, Is Closely Related to the Arabidopsis Flowering Time Gene CONSTANS Yano, Masahiro; Katayose, Yuichi; Ashikari, Motoyuki The Plant Cell, Vol. 12, Issue 12 https://doi.org/10.1105/tpc.12.12.2473	journal	December 2000
Structural Insight into DNA Recognition by CCT/NF-YB/YC Complexes in Plant Photoperiodic Flowering Shen, Cuicui; Liu, Haiyang; Guan, Zeyuan The Plant Cell, Vol. 32, Issue 11 https://doi.org/10.1105/tpc.20.00067	journal	August 2020
Gateway vectors for the production of combinatorially-tagged His ₆ -MBP fusion proteins in the cytoplasm and periplasm of Escherichia coli Nallamsetty, Sreedevi; Austin, Brian P.; Penrose, Kerri J. Protein Science, Vol. 14, Issue 12 https://doi.org/10.1110/ps.051718605	journal	December 2005
The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element Tiwari, Shiv B.; Shen, Yu; Chang, Han-Chang New Phytologist, Vol. 187, Issue 1 https://doi.org/10.1111/j.1469-8137.2010.03251.x	journal	April 2010
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
Control of floral transition in the bioenergy crop switchgrass: Regulation of flowering time in switchgrass Niu, Lifang; Fu, Chunxiang; Lin, Hao Plant, Cell & Environment, Vol. 39, Issue 10 https://doi.org/10.1111/pce.12769	journal	July 2016
Photoreceptor Regulation of CONSTANS Protein in Photoperiodic Flowering Valverde, Federico; Mouradov, Aidyn; Soppe, Wim Science, Vol. 303, Issue 5660 https://doi.org/10.1126/science.1091761	journal	February 2004
FT Protein Movement Contributes to Long-Distance Signaling in Floral Induction of Arabidopsis Corbesier, L.; Vincent, C.; Jang, S. Science, Vol. 316, Issue 5827 https://doi.org/10.1126/science.1141752	journal	May 2007
A Pair of Related Genes with Antagonistic Roles in Mediating Flowering Signals Kobayashi, Y. Science, Vol. 286, Issue 5446 https://doi.org/10.1126/science.286.5446.1960	journal	December 1999
Distinct Roles of CONSTANS Target Genes in Reproductive Development of Arabidopsis Samach, A. Science, Vol. 288, Issue 5471 https://doi.org/10.1126/science.288.5471.1613	journal	June 2000
Accurate prediction of protein structures and interactions using a three-track neural network Baek, Minkyung; DiMaio, Frank; Anishchenko, Ivan Science, Vol. 373, Issue 6557 https://doi.org/10.1126/science.abj8754	journal	July 2021
Computed structures of core eukaryotic protein complexes Humphreys, Ian R.; Pei, Jimin; Baek, Minkyung Science, Vol. 374, Issue 6573 https://doi.org/10.1126/science.abm4805	journal	December 2021
Evolutionary-scale prediction of atomic-level protein structure with a language model Lin, Zeming; Akin, Halil; Rao, Roshan Science, Vol. 379, Issue 6637 https://doi.org/10.1126/science.ade2574	journal	March 2023
Control of gene expression through the nonsense-mediated RNA decay pathway Nickless, Andrew; Bailis, Julie M.; You, Zhongsheng Cell & Bioscience, Vol. 7, Issue 1 https://doi.org/10.1186/s13578-017-0153-7	journal	May 2017
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
Genetic Control of Photoperiod Sensitivity in Maize Revealed by Joint Multiple Population Analysis Coles, Nathan D.; McMullen, Michael D.; Balint-Kurti, Peter J. Genetics, Vol. 184, Issue 3 https://doi.org/10.1534/genetics.109.110304	journal	December 2009
Selection Response and Developmental Basis for Early and Late Panicle Emergence in Alamo Switchgrass Van Esbroeck, G. A.; Hussey, M. A.; Sanderson, M. A. Crop Science, Vol. 38, Issue 2 https://doi.org/10.2135/cropsci1998.0011183X003800020010x	journal	January 1998
Latitudinal Adaptation of Switchgrass Populations Casler, M. D.; Vogel, K. P.; Taliaferro, C. M. Crop Science, Vol. 44, Issue 1 https://doi.org/10.2135/cropsci2004.2930	journal	January 2004
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
The Importance of Being on Time: Regulatory Networks Controlling Photoperiodic Flowering in Cereals Brambilla, Vittoria; Gomez-Ariza, Jorge; Cerise, Martina Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00665	journal	April 2017
Genome-Wide Association Study in Pseudo-F2 Populations of Switchgrass Identifies Genetic Loci Affecting Heading and Anthesis Dates Taylor, Megan; Tornqvist, Carl-Erik; Zhao, Xiongwei Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01250	journal	September 2018
Characterization and Activity Analyses of the FLOWERING LOCUS T Promoter in Gossypium Hirsutum Sang, Na; Cai, Darun; Li, Chao International Journal of Molecular Sciences, Vol. 20, Issue 19 https://doi.org/10.3390/ijms20194769	journal	September 2019
Quantitative Trait Locus Mapping for Flowering Time in a Lowland × Upland Switchgrass Pseudo-F Population Tornqvist, Carl-Erik; Taylor, Megan; Jiang, Yiwei The Plant Genome, Vol. 11, Issue 2 https://doi.org/10.3835/plantgenome2017.10.0093	journal	January 2018

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
CONSTANS (CO)
Heading date 1 (Hd1)
Panicum virgatum
Plant Sciences
QTL
SNP
bioenergy
flowering time
latitudinal adaptation
protein structure and function
quantitative trait locus
single nucleotide polymorphism
switchgrass

Title: A single amino acid change led to structural and functional differentiation of PvHd1 to control flowering in switchgrass

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