Abstract
Key message
Comparing populations derived, respectively, from polyploid Sorghum halepense and its progenitors improved knowledge of plant architecture and showed that S. halepense harbors genetic novelty of potential value for sorghum improvement
Vegetative growth and the timing of the vegetative-to-reproductive transition are critical to a plant’s fitness, directly and indirectly determining when and how a plant lives, grows and reproduces. We describe quantitative trait analysis of plant height and flowering time in the naturally occurring tetraploid Sorghum halepense, using two novel BC1F2 populations totaling 246 genotypes derived from backcrossing two tetraploid Sorghum bicolor x S. halepense F1 plants to a tetraploidized S. bicolor. Phenotyping for two years each in Bogart, GA and Salina, KS allowed us to dissect variance into narrow-sense genetic (QTLs) and environmental components. In crosses with a common S. bicolor BTx623 parent, comparison of QTLs in S. halepense, its rhizomatous progenitor S. propinquum and S. bicolor race guinea which is highly divergent from BTx623 permit inferences of loci at which new alleles have been associated with improvement of elite sorghums. The relative abundance of QTLs unique to the S. halepense populations may reflect its polyploidy and subsequent ‘diploidization’ processes often associated with the formation of genetic novelty, a possibility further supported by a high level of QTL polymorphism within sibling lines derived from a common S. halepense parent. An intriguing hypothesis for further investigation is that polyploidy of S. halepense following 96 million years of abstinence, coupled with natural selection during its spread to diverse environments across six continents, may provide a rich collection of novel alleles that offer potential opportunities for sorghum improvement.
Similar content being viewed by others
Availability of data and material
Genotypic data is available at https://www.frontiersin.org/articles/10.3389/fpls.2020.00467/full#supplementary-material. Phenotypic data can be found in the supplementary documents.
References
Aljanabi SM, Forget L, Dookun A (1999) An improved and rapid protocol for the isolation of polysaccharide- and polyphenol-free sugarcane DNA. Plant Mol Biol Rep 17:281
Andolfatto P, Davison D, Erezyilmaz D, Hu TT, Mast J, Sunayama-Morita T, Stern DL (2011) Multiplexed shotgun genotyping for rapid and efficient genetic mapping. Genome Res 21:610–617
Bishop GJ (2003) Brassinosteroid mutants of crops. J Plant Growth Regul 22:325–335
Brady JA (2006) Sorghum Ma5 and Ma6 maturity genes. Texas A&M University
Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890
Brown PJ, Rooney WL, Franks C, Kresovich S (2008) Efficient mapping of plant height quantitative trait loci in a sorghum association population with introgressed dwarfing genes. Genetics 180:629–637
Childs KL, Miller FR, Cordonnier-Pratt MM, Pratt LH, Morgan PW, Mullet JE (1997) The sorghum photoperiod sensitivity gene, Ma3, encodes a phytochrome B. Plant Physiol 113:611–619
Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846
Cuevas HE, Zhou C, Tang H, Khadke PP, Das S, Lin YR, Ge Z, Clemente T, Upadhyaya HD, Hash CT, Paterson AH (2016) The evolution of photoperiod-insensitive flowering in sorghum, a genomic model for panicoid grasses. Mol Biol Evol 33:2417–2428
Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A (2004) Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev 18:926–936
Fernandez MGS, Becraft PW, Yin Y, Lübberstedt T (2009) From dwarves to giants? Plant height manipulation for biomass yield. Trends Plant Sci 14:454–461
Hart GE, Schertz KF, Peng Y, Syed NH (2001) Genetic mapping of Sorghum bicolor (L.) Moench QTLs that control variation in tillering and other morphological characters. Theor Appl Genet 103:1232–1242
Higgins RH, Thurber CS, Assaranurak I, Brown PJ (2014) Multiparental mapping of plant height and flowering time QTL in partially isogenic sorghum families. G3-Genes Genom Genet 4:1593–1602
Hill CB, Li C (2016) Genetic Architecture of Flowering Phenology in Cereals and Opportunities for Crop Improvement. Front Plant Sci 7:1906
Hilley J, Truong S, Olson S, Morishige D, Mullet J (2016) Identification of Dw1, a regulator of sorghum stem internode length. PLoS ONE 11:e0151271
Hilley JL, Weers BD, Truong SK, McCormick RF, Mattison AJ, McKinley BA, Morishige DT, Mullet JE (2017) Sorghum Dw2 encodes a protein kinase regulator of stem internode length. Sci Rep 7:4616
Jung C, Müller AE (2009) Review: flowering time control and applications in plant breeding. Trends Plant Sci 14:563–573
Kong L, Dong J, Hart GE (2000) Characteristics, linkage-map positions, and allelic differentiation of Sorghum bicolor (L.) Moench DNA simple-sequence repeats (SSRs). Theor Appl Genet 101:438–448
Kong W, Jin H, Franks CD, Kim C, Bandopadhyay R, Rana MK, Auckland SA, Goff VH, Rainville LK, Burow GB, Woodfin C, Burke JJ, Paterson AH (2013) Genetic analysis of recombinant inbred lines for Sorghum bicolor × Sorghum propinquum. G3 Genes Genomes Genetics 3:101–108
Kong W, Guo H, Goff V, Lee T-H, Kim C, Paterson A (2014) Genetic analysis of vegetative branching in sorghum. Theor Appl Genet 127:2387–2403
Kong W, Kim C, Zhang D, Guo H, Tan X, Jin H, Zhou C, Shuang LS, Goff V, Sezen U, Pierce G, Compton R, Lemke C, Robertson J, Rainville L, Auckland S, Paterson AH (2018) Genotyping by Sequencing of 393 Sorghum bicolor BTx623 x IS3620C recombinant inbred lines improves sensitivity and resolution of QTL Detection. G3 (Bethesda) 8:2563–2572
Kong W, Nabukalu P, Cox TS, Goff VH, Pierce GJ, Lemke C, Robertson JS, Compton R, Tang H, Paterson AH (2020) Transmission genetics of a Sorghum bicolor × S. halepense backcross populations. Front. Plant Sci 11:467
Ku LX, Zhang LK, Tian ZQ, Guo SL, Su HH, Ren ZZ, Wang ZY, Li GH, Wang XB, Zhu YG, Zhou JL, Chen YH (2015) Dissection of the genetic architecture underlying the plant density response by mapping plant height-related traits in maize (Zea mays L.). Mol Genet Genomics 290:1223–1233
Kutschera U, Wang ZY (2012) Brassinosteroid action in flowering plants: a Darwinian perspective. J Exp Bot 63:3511–3522
Lander ES, Botstein D (1989) Mapping mendelian factors underlying quantitative traits using Rflp linkage maps. Genetics 121:185–199
Li X, Li XR, Fridman E, Tesso TT, Yu JM (2015) Dissecting repulsion linkage in the dwarfing gene Dw3 region for sorghum plant height provides insights into heterosis. Proc Natl Acad Sci USA 112:11823–11828
Lin YR, Schertz KF, Paterson AH (1995) Comparative analysis of QTLs affecting plant height and maturity across the Poaceae, in reference to an interspecific sorghum population. Genetics 141:391–411
McWhorter C (1971) Introduction and spread of johnsongrass in the United States. Weed Sci, pp 496–500
Morris GP, Ramu P, Deshpande SP, Hash CT, Shah T, Upadhyaya HD, Riera-Lizarazu O, Brown PJ, Acharya CB, Mitchell SE, Harriman J, Glaubitz JC, Buckler ES, Kresovich S (2013) Population genomic and genome-wide association studies of agroclimatic traits in sorghum. Proc Natl Acad Sci USA 110:453–458
Multani DS, Briggs SP, Chamberlin MA, Blakeslee JJ, Murphy AS, Johal GS (2003) Loss of an MDR transporter in compact stalks of maize br2 and sorghum dw3 mutants. Science 302:81–84
Murphy RL, Klein RR, Morishige DT, Brady JA, Rooney WL, Miller FR, Dugas DV, Klein PE, Mullet JE (2011) Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum. Proc Natl Acad Sci USA 108:16469–16474
Murphy RL, Morishige DT, Brady JA, Rooney WL, Yang SS, Klein PE, Mullet JE (2014) Ghd7 (Ma(6)) Represses sorghum flowering in long days: Ghd7 alleles enhance biomass accumulation and grain production. Plant Genom 7:1–10
Murray SC, Rooney WL, Mitchell SE, Sharma A, Klein PE, Mullet JE, Kresovich S (2008) Genetic improvement of sorghum as a biofuel feedstock: II. QTL for stem and leaf structural carbohydrates. Crop Sci 48:2180–2193
Murray SC, Rooney WL, Hamblin MT, Mitchell SE, Kresovich S (2009) Sweet sorghum genetic diversity and association mapping for brix and height. Plant Genome-Us 2:48–62
Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142
Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Lyons E, Maher C, Narechania A, Penning B, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein PE, Kresovich S, McCann MC, Ming R, Peterson DG, Ware D, Westhoff P, Mayer KFX, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556
Peiffer JA, Romay MC, Gore MA, Flint-Garcia SA, Zhang ZW, Millard MJ, Gardner CAC, McMullen MD, Holland JB, Bradbury PJ, Buckler ES (2014) The genetic architecture of maize height. Genetics 196:1337
Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F, Sudhakar D, Christou P, Snape JW, Gale MD, Harberd NP (1999) Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261
Quinby J (1966) Fourth maturity gene locus in sorghum. Crop Sci 6:516–518
Quinby J, Karper R (1945) Inheritance of three genes that influence time of floral initiation and maturity date in milo. J Am Soc Agron 37(11):916–936
Quinby JR, Karper RE (1954) Inheritance of Height in Sorghum. Agron J 46:211–216
Quinn LD, Barney JN, McCubbins JS, Endres AB (2013) Navigating the “noxious” and “invasive” regulatory landscape: suggestions for improved regulation. Bioscience 63:124–131
R Core Team (2016) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna
Ritter KB, Jordan DR, Chapman SC, Godwin ID, Mace ES, McIntyre CL (2008) Identification of QTL for sugar-related traits in a sweet x grain sorghum (Sorghum bicolor L. Moench) recombinant inbred population. Mol Breed 22:367–384
Sasaki A, Ashikari M, Ueguchi-Tanaka M, Itoh H, Nishimura A, Swapan D, Ishiyama K, Saito T, Kobayashi M, Khush GS, Kitano H, Matsuoka M (2002) Green revolution: a mutant gibberellin-synthesis gene in rice. Nature 416:701–702
Sezen UU, Barney JN, Atwater DZ, Pederson GA, Pederson JF, Chandler JM, Cox TS, Cox S, Dotray P, Kopec D, Smith SE, Schroeder J, Wright SD, Jiao Y, Kong W, Goff V, Auckland S, Rainville LK, Pierce GJ, Lemke C, Compton R, Phillips C, Kerr A, Mettler M, Paterson AH (2016) Multi-phase US spread and habitat switching of a post-columbian invasive Sorghum halepense. Plos One 11:e0164584
Upadhyaya HD, Wang Y-H, Sharma S, Singh S (2012) Association mapping of height and maturity across five environments using the sorghum mini core collection. Genome 55:471–479
Wang YH, Li JY (2006) Genes controlling plant architecture. Curr Opin Biotech 17:123–129
Wang X, Wang J, Jin D, Guo H, Lee TH, Liu T, Paterson AH (2015) Genome alignment spanning major poaceae lineages reveals heterogeneous evolutionary rates and alters inferred dates for key evolutionary events. Mol Plant 8:885–898
Wang Y, Zhao J, Lu W, Deng D (2017) Gibberellin in plant height control: old player, new story. Plant Cell Rep 36:391–398
Warnes GR, Bolker B, Bonebakker L, Gentleman R, LIaw W, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz M, Venables B (2016) gplots: Various R programming tools for plotting data 2(4):1
Wolabu TW, Zhang F, Niu LF, Kalve S, Bhatnagar-Mathur P, Muszynski MG, Tadege M (2016) Three FLOWERING LOCUS T-like genes function as potential florigens and mediate photoperiod response in sorghum. New Phytol 210:946–959
Yamaguchi M, Fujimoto H, Hirano K, Araki-Nakamura S, Ohmae-Shinohara K, Fujii A, Tsunashima M, Song XJ, Ito Y, Nagae R, Wu J, Mizuno H, Yonemaru J, Matsumoto T, Kitano H, Matsuoka M, Kasuga S, Sazuka T (2016) Sorghum Dw1, an agronomically important gene for lodging resistance, encodes a novel protein involved in cell proliferation. Sci Rep 6:28366
Yang SS, Murphy RL, Morishige DT, Klein PE, Rooney WL, Mullet JE (2014a) Sorghum phytochrome b inhibits flowering in long days by activating expression of SbPRR37 and SbGHD7, Repressors of SbEHD1, SbCN8 and SbCN12. Plos One 9(8):e105352
Yang SS, Weers BD, Morishige DT, Mullet JE (2014b) CONSTANS is a photoperiod regulated activator of flowering in sorghum. BMC Plant Biol 14(1):1–5
Zhang D, Guo H, Kim C, Lee TH, Li JP, Robertson J, Wang XY, Wang ZN, Paterson AH (2013) CSGRqtl, a comparative quantitative trait locus database for saccharinae grasses. Plant Physiol 161:594–599
Zhang D, Kong W, Robertson J, Goff VH, Epps E, Kerr A, Mills G, Cromwell J, Lugin Y, Phillips C, Paterson AH (2015) Genetic analysis of inflorescence and plant height components in sorghum (Panicoidae) and comparative genetics with rice (Oryzoidae). BMC Plant Biol 15:107
Acknowledgments
We appreciate the support of the USDA Biotechnology Risk Assessment Program (2012-01658 to AHP and TSC), USAID Feed The Future (AID-OAA-A-13-00044 to AHP, TSC) program, and NIFA Global Food Security CAP (2015-68004-23492 to AHP, JNB). We thank members of the Plant Genome Mapping Laboratory (PGML) for help with field work.
Funding
We appreciate the support of the USDA Biotechnology Risk Assessment Program (2012-01658 to AHP and TSC), and NIFA Global Food Security CAP (2015-68004-23492 to AHP, JNB). This work was funded in part by the United States Agency for International Development (USAID) Bureau for Resilience and Food Security under Agreement # AID-OAA-A-13-00044 (to AHP, TSC) as part of Feed the Future Innovation Lab for Climate Resilient Sorghum. Any opinions, findings, conclusions, or recommendations expressed here are those of the authors alone.
Author information
Authors and Affiliations
Contributions
WQK conducted the experiment, analyzed the data wrote the manuscript; PN conducted the experiment and collected phenotypic data; TSC designed, supervised the experiment and edited the paper; VHG, JSR, GRP, CL and RC carried out the field experiment and collected the phenotypic data. AHP designed and supervised the experiment, edited the manuscript and recommended analytical suggestions.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Jianbing Yan.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kong, W., Nabukalu, P., Cox, T.S. et al. Quantitative trait mapping of plant architecture in two BC1F2 populations of Sorghum Bicolor × S. halepense and comparisons to two other sorghum populations. Theor Appl Genet 134, 1185–1200 (2021). https://doi.org/10.1007/s00122-020-03763-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-020-03763-1