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Title: A new reference genome for Sorghum bicolor reveals high levels of sequence similarity between sweet and grain genotypes: implications for the genetics of sugar metabolism

Abstract

BACKGROUND:The process of crop domestication often consists of two stages: initial domestication, where the wild species is first cultivated by humans, followed by diversification, when the domesticated species are subsequently adapted to more environments and specialized uses. Selective pressure to increase sugar accumulation in certain varieties of the cereal crop Sorghum bicolor is an excellent example of the latter; this has resulted in pronounced phenotypic divergence between sweet and grain-type sorghums, but the genetic mechanisms underlying these differences remain poorly understood. RESULTS:Here we present a new reference genome based on an archetypal sweet sorghum line and compare it to the current grain sorghum reference, revealing a high rate of nonsynonymous and potential loss of function mutations, but few changes in gene content or overall genome structure. We also use comparative transcriptomics to highlight changes in gene expression correlated with high stalk sugar content and show that changes in the activity and possibly localization of transporters, along with the timing of sugar metabolism play a critical role in the sweet phenotype. CONCLUSIONS:The high level of genomic similarity between sweet and grain sorghum reflects their historical relatedness, rather than their current phenotypic differences, but we find key changes in signaling molecules andmore » transcriptional regulators that represent new candidates for understanding and improving sugar metabolism in this important crop.« less

Authors:
ORCiD logo [1];  [2];  [2];  [3];  [4];  [3];  [2];  [5];  [2];  [4];  [4];  [4];  [4];  [6];  [2];  [7];  [2]
  1. Clemson Univ., Clemson, SC (United States); Univ. of North Carolina at Charlotte, Charlotte, NC (United States)
  2. Clemson Univ., Clemson, SC (United States)
  3. HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States)
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. Clemson Univ., Clemson, SC (United States); Hunan Agricultural Univ., Changsha (China)
  6. HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  7. Univ. of Florida, Gainesville, FL (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1572011
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Volume: 20; Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Sorghum; Sugar metabolism; Sugar transport; Genomics; Gene expression

Citation Formats

Cooper, Elizabeth A., Brenton, Zachary W., Flinn, Barry S., Jenkins, Jerry, Shu, Shengqiang, Flowers, Dave, Luo, Feng, Wang, Yunsheng, Xia, Penny, Barry, Kerrie, Daum, Chris, Lipzen, Anna, Yoshinaga, Yuko, Schmutz, Jeremy, Saski, Christopher, Vermerris, Wilfred, and Kresovich, Stephen. A new reference genome for Sorghum bicolor reveals high levels of sequence similarity between sweet and grain genotypes: implications for the genetics of sugar metabolism. United States: N. p., 2019. Web. doi:10.1186/s12864-019-5734-x.
Cooper, Elizabeth A., Brenton, Zachary W., Flinn, Barry S., Jenkins, Jerry, Shu, Shengqiang, Flowers, Dave, Luo, Feng, Wang, Yunsheng, Xia, Penny, Barry, Kerrie, Daum, Chris, Lipzen, Anna, Yoshinaga, Yuko, Schmutz, Jeremy, Saski, Christopher, Vermerris, Wilfred, & Kresovich, Stephen. A new reference genome for Sorghum bicolor reveals high levels of sequence similarity between sweet and grain genotypes: implications for the genetics of sugar metabolism. United States. doi:10.1186/s12864-019-5734-x.
Cooper, Elizabeth A., Brenton, Zachary W., Flinn, Barry S., Jenkins, Jerry, Shu, Shengqiang, Flowers, Dave, Luo, Feng, Wang, Yunsheng, Xia, Penny, Barry, Kerrie, Daum, Chris, Lipzen, Anna, Yoshinaga, Yuko, Schmutz, Jeremy, Saski, Christopher, Vermerris, Wilfred, and Kresovich, Stephen. Mon . "A new reference genome for Sorghum bicolor reveals high levels of sequence similarity between sweet and grain genotypes: implications for the genetics of sugar metabolism". United States. doi:10.1186/s12864-019-5734-x. https://www.osti.gov/servlets/purl/1572011.
@article{osti_1572011,
title = {A new reference genome for Sorghum bicolor reveals high levels of sequence similarity between sweet and grain genotypes: implications for the genetics of sugar metabolism},
author = {Cooper, Elizabeth A. and Brenton, Zachary W. and Flinn, Barry S. and Jenkins, Jerry and Shu, Shengqiang and Flowers, Dave and Luo, Feng and Wang, Yunsheng and Xia, Penny and Barry, Kerrie and Daum, Chris and Lipzen, Anna and Yoshinaga, Yuko and Schmutz, Jeremy and Saski, Christopher and Vermerris, Wilfred and Kresovich, Stephen},
abstractNote = {BACKGROUND:The process of crop domestication often consists of two stages: initial domestication, where the wild species is first cultivated by humans, followed by diversification, when the domesticated species are subsequently adapted to more environments and specialized uses. Selective pressure to increase sugar accumulation in certain varieties of the cereal crop Sorghum bicolor is an excellent example of the latter; this has resulted in pronounced phenotypic divergence between sweet and grain-type sorghums, but the genetic mechanisms underlying these differences remain poorly understood. RESULTS:Here we present a new reference genome based on an archetypal sweet sorghum line and compare it to the current grain sorghum reference, revealing a high rate of nonsynonymous and potential loss of function mutations, but few changes in gene content or overall genome structure. We also use comparative transcriptomics to highlight changes in gene expression correlated with high stalk sugar content and show that changes in the activity and possibly localization of transporters, along with the timing of sugar metabolism play a critical role in the sweet phenotype. CONCLUSIONS:The high level of genomic similarity between sweet and grain sorghum reflects their historical relatedness, rather than their current phenotypic differences, but we find key changes in signaling molecules and transcriptional regulators that represent new candidates for understanding and improving sugar metabolism in this important crop.},
doi = {10.1186/s12864-019-5734-x},
journal = {BMC Genomics},
number = 1,
volume = 20,
place = {United States},
year = {2019},
month = {5}
}

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Works referenced in this record:

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Targeted analysis of nucleotide and copy number variation by exon capture in allotetraploid wheat genome
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journal, April 2014


Genetic Diversity among Sorghum Races and Working Groups Based on AFLPs and SSRs
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Thinking outside the F-box: novel ligands for novel receptors
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Tonoplast Sugar Transporters (SbTSTs) putatively control sucrose accumulation in sweet sorghum stems
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Population genomic and genome-wide association studies of agroclimatic traits in sorghum
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Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza
journal, January 2018


Stem sugar accumulation in sweet sorghum – Activity and expression of sucrose metabolizing enzymes and sucrose transporters
journal, April 2012

  • Qazi, Hilal Ahmad; Paranjpe, Sharayu; Bhargava, Sujata
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Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies
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The Sequence Alignment/Map format and SAMtools
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journal, January 2011

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Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
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Community Resources and Strategies for Association Mapping in Sorghum
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Genome-wide copy number variations in Oryza sativa L.
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    Works referencing / citing this record:

    A sorghum NAC gene is associated with variation in biomass properties and yield potential
    journal, July 2018

    • Xia, Jingnu; Zhao, Yunjun; Burks, Payne
    • Plant Direct, Vol. 2, Issue 7
    • DOI: 10.1002/pld3.70

    Assessment of genetic diversity in the sorghum reference set using EST-SSR markers
    journal, May 2013


    Screen of Genes Linked to High-Sugar Content in Stems by Comparative Genomics
    journal, September 2008


    MYB transcription factor genes as regulators for plant responses: an overview
    journal, April 2013

    • Ambawat, Supriya; Sharma, Poonam; Yadav, Neelam R.
    • Physiology and Molecular Biology of Plants, Vol. 19, Issue 3
    • DOI: 10.1007/s12298-013-0179-1

    A general method applicable to the search for similarities in the amino acid sequence of two proteins
    journal, March 1970


    MATH/BTB CRL3 Receptors Target the Homeodomain-Leucine Zipper ATHB6 to Modulate Abscisic Acid Signaling
    journal, December 2011


    Stem sugar accumulation in sweet sorghum – Activity and expression of sucrose metabolizing enzymes and sucrose transporters
    journal, April 2012

    • Qazi, Hilal Ahmad; Paranjpe, Sharayu; Bhargava, Sujata
    • Journal of Plant Physiology, Vol. 169, Issue 6
    • DOI: 10.1016/j.jplph.2012.01.005

    SWEETs, transporters for intracellular and intercellular sugar translocation
    journal, June 2015


    Thinking outside the F-box: novel ligands for novel receptors
    journal, April 2009


    The Sorghum bicolor genome and the diversification of grasses
    journal, January 2009

    • Paterson, Andrew H.; Bowers, John E.; Bruggmann, Rémy
    • Nature, Vol. 457, Issue 7229
    • DOI: 10.1038/nature07723

    Fast gapped-read alignment with Bowtie 2
    journal, March 2012

    • Langmead, Ben; Salzberg, Steven L.
    • Nature Methods, Vol. 9, Issue 4
    • DOI: 10.1038/nmeth.1923

    Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data
    journal, May 2013

    • Chin, Chen-Shan; Alexander, David H.; Marks, Patrick
    • Nature Methods, Vol. 10, Issue 6
    • DOI: 10.1038/nmeth.2474

    Phased diploid genome assembly with single-molecule real-time sequencing
    journal, October 2016

    • Chin, Chen-Shan; Peluso, Paul; Sedlazeck, Fritz J.
    • Nature Methods, Vol. 13, Issue 12
    • DOI: 10.1038/nmeth.4035

    Genome structural variation discovery and genotyping
    journal, March 2011

    • Alkan, Can; Coe, Bradley P.; Eichler, Evan E.
    • Nature Reviews Genetics, Vol. 12, Issue 5
    • DOI: 10.1038/nrg2958

    Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza
    journal, January 2018


    Population genomic and genome-wide association studies of agroclimatic traits in sorghum
    journal, December 2012

    • Morris, G. P.; Ramu, P.; Deshpande, S. P.
    • Proceedings of the National Academy of Sciences, Vol. 110, Issue 2
    • DOI: 10.1073/pnas.1215985110

    Tonoplast Sugar Transporters (SbTSTs) putatively control sucrose accumulation in sweet sorghum stems
    journal, January 2016


    Improved scoring of functional groups from gene expression data by decorrelating GO graph structure
    journal, April 2006


    TopHat: discovering splice junctions with RNA-Seq
    journal, March 2009


    The Sequence Alignment/Map format and SAMtools
    journal, June 2009


    Trimmomatic: a flexible trimmer for Illumina sequence data
    journal, April 2014


    HTSeq--a Python framework to work with high-throughput sequencing data
    journal, September 2014


    EBSeq-HMM: a Bayesian approach for identifying gene-expression changes in ordered RNA-seq experiments
    journal, April 2015


    Assemblytics: a web analytics tool for the detection of variants from an assembly
    journal, June 2016


    Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies
    journal, October 2003


    BLAT---The BLAST-Like Alignment Tool
    journal, March 2002


    Insights into the Maize Pan-Genome and Pan-Transcriptome
    journal, January 2014

    • Hirsch, Candice N.; Foerster, Jillian M.; Johnson, James M.
    • The Plant Cell, Vol. 26, Issue 1
    • DOI: 10.1105/tpc.113.119982

    The Sorghum bicolor reference genome: improved assembly, gene annotations, a transcriptome atlas, and signatures of genome organization
    journal, December 2017

    • McCormick, Ryan F.; Truong, Sandra K.; Sreedasyam, Avinash
    • The Plant Journal, Vol. 93, Issue 2
    • DOI: 10.1111/tpj.13781

    Genome-wide copy number variations in Oryza sativa L.
    journal, January 2013


    Compartmentation of sucrose during radial transfer in mature sorghum culm
    journal, January 2007


    Genome-wide patterns of genetic variation in sweet and grain sorghum (Sorghum bicolor)
    journal, January 2011


    Targeted analysis of nucleotide and copy number variation by exon capture in allotetraploid wheat genome
    journal, January 2011


    The plasticity of NBS resistance genes in sorghum is driven by multiple evolutionary processes
    journal, September 2014


    Sucrose accumulation in sweet sorghum stems occurs by apoplasmic phloem unloading and does not involve differential Sucrose transporter expression
    journal, July 2015


    Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
    journal, December 2014


    The sorghum SWEET gene family: stem sucrose accumulation as revealed through transcriptome profiling
    journal, June 2016

    • Mizuno, Hiroshi; Kasuga, Shigemitsu; Kawahigashi, Hiroyuki
    • Biotechnology for Biofuels, Vol. 9, Issue 1
    • DOI: 10.1186/s13068-016-0546-6

    Cytochromes P450
    journal, January 2011

    • Bak, Søren; Beisson, Fred; Bishop, Gerard
    • The Arabidopsis Book, Vol. 9
    • DOI: 10.1199/tab.0144

    Plant F-Box Protein Evolution Is Determined by Lineage-Specific Timing of Major Gene Family Expansion Waves
    journal, July 2013


    Genetic Diversity among Sorghum Races and Working Groups Based on AFLPs and SSRs
    journal, January 2007


    Community Resources and Strategies for Association Mapping in Sorghum
    journal, January 2008


    Genetic Improvement of Sorghum as a Biofuel Feedstock: I. QTL for Stem Sugar and Grain Nonstructural Carbohydrates
    journal, January 2008


    QTLs for Energy-related Traits in a Sweet × Grain Sorghum [ (L.) Moench] Mapping Population
    journal, January 2012


    Are sucrose transporter expression profiles linked with patterns of biomass partitioning in Sorghum phenotypes?
    journal, January 2013

    • Milne, Ricky J.; Byrt, Caitlin S.; Patrick, John W.
    • Frontiers in Plant Science, Vol. 4
    • DOI: 10.3389/fpls.2013.00223

    Multifunctional Microtubule-Associated Proteins in Plants
    journal, April 2016

    • Krtková, Jana; Benáková, Martina; Schwarzerová, Kateřina
    • Frontiers in Plant Science, Vol. 7
    • DOI: 10.3389/fpls.2016.00474

    Early evolution of bHLH proteins in plants
    journal, July 2010