We detected 213 lodging QTLs and demonstrated that drought-induced stem lodging in grain sorghum is substantially associated with stay-green and plant height suggesting a critical role of carbon remobilisation.
Sorghum is generally grown in water limited conditions and often lodges under post-anthesis drought, which reduces yield and quality. Due to its complexity, our understanding on the genetic control of lodging is very limited. We dissected the genetic architecture of lodging in grain sorghum through genome-wide association study (GWAS) on 2308 unique hybrids grown in 17 Australian sorghum trials over 3 years. The GWAS detected 213 QTLs, the majority of which showed a significant association with leaf senescence and plant height (72% and 71%, respectively). Only 16 lodging QTLs were not associated with either leaf senescence or plant height. The high incidence of multi-trait association for the lodging QTLs indicates that lodging in grain sorghum is mainly associated with plant height and traits linked to carbohydrate remobilisation. This result supported the selection for stay-green (delayed leaf senescence) to reduce lodging susceptibility, rather than selection for short stature and lodging resistance per se, which likely reduces yield. Additionally, our data suggested a protective effect of stay-green on weakening the association between lodging susceptibility and plant height. Our study also showed that lodging resistance might be improved by selection for stem composition but was unlikely to be improved by selection for classical resistance to stalk rots.
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Adeyanju A, Little C, Yu J, Tesso T (2015) Genome-wide association study on resistance to stalk rot diseases in grain sorghum. G3 Genes Genomes Genetics 5:1165–1175. https://doi.org/10.1534/g3.114.016394
Bandara YMAY, Weerasooriya DK, Liu S, Little CR (2018) The necrotrophic fungus Macrophomina phaseolina promotes charcoal rot susceptibility in grain sorghum through induced host cell-wall-degrading enzymes. Phytopathology 108:948–956. https://doi.org/10.1094/PHYTO-12-17-0404-R
Bashford LL, Maranville JW, Weeks SA, Campbell R (1976) Mechanical properties affecting lodging of sorghum. Trans ASAE 19:962–966
Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546. https://doi.org/10.1146/annurev.arplant.54.031902.134938
Borrell AK, Douglas ACL (1996) Maintaining green leaf area in grain sorghum increases yield in a water-limited environment. In: Proceedings of the third Australian sorghum conference. Tamworth, NSW, pp 315–322
Borrell AK, Hammer GL (2000) Nitrogen dynamics and the physiological basis of stay-green in Sorghum. Crop Sci 40:1295–1307. https://doi.org/10.2135/cropsci2000.4051295x
Borrell AK, Hammer GL, Douglas ACL (2000) Does maintaining green leaf area in sorghum improve yield under drought? II. Dry matter production and yield. Crop Sci 40:1026–1037. https://doi.org/10.2135/cropsci2000.4041037x
Borrell A, Hammer G, Van Oosterom E (2001) Stay-green: a consequence of the balance between supply and demand for nitrogen during grain filling? Ann Appl Biol 138:91–95. https://doi.org/10.1111/j.1744-7348.2001.tb00088.x
Borrell AK, Mullet JE, George-Jaeggli B et al (2014a) Drought adaptation of stay-green sorghum is associated with canopy development, leaf anatomy, root growth, and water uptake. J Exp Bot 65:6251–6263. https://doi.org/10.1093/jxb/eru232
Borrell AK, van Oosterom EJ, Mullet JE et al (2014b) Stay-green alleles individually enhance grain yield in sorghum under drought by modifying canopy development and water uptake patterns. New Phytol 203:817–830. https://doi.org/10.1111/nph.12869
Bout S, Vermerris W (2003) A candidate-gene approach to clone the sorghum Brown midrib gene encoding caffeic acid O-methyltransferase. Mol Genet Genom 269:205–214. https://doi.org/10.1007/s00438-003-0824-4
Browning BL, Browning SR (2016) Genotype imputation with millions of reference samples. Am J Hum Genet 98:116–126
Butler DG, Cullis BR, Gilmour AR, Gogel BJ (2009) ASReml-R reference manual
Casto AL, McKinley BA, Yu KMJ, Rooney WL, Mullet JE (2018) Sorghum stem aerenchyma formation is regulated by SbNAC_D during internode development. Plant Direct 2(11):e00085. https://doi.org/10.1002/pld3.85
Cha KW, Lee YJ, Koh HJ et al (2002) Isolation, characterization, and mapping of the stay green mutant in rice. Theor Appl Genet 104:526–532. https://doi.org/10.1007/s001220100750
Chapman SC, Cooper M, Hammer GL, Butler DG (2000) Genotype by environment interactions affecting grain sorghum. II. Frequencies of different seasonal patterns of drought stress are related to location effects on hybrid yields. Aust J Agric Res 51:209–221. https://doi.org/10.1071/AR99021
Christopher JT, Manschadi AM, Hammer GL, Borrell AK (2008) Developmental and physiological traits associated with high yield and stay-green phenotype in wheat. Aust J Agric Res 59:354–364. https://doi.org/10.1071/AR07193
Cullis BR, Smith AB, Coombes NE (2006) On the design of early generation variety. J Agric Biol Environ Stat 11:381–393. https://doi.org/10.1198/108571106X154443
Dodd JL (1980) The photosynthetic stress-translocation balance concept of sorghum stalk rots. In: In Sorghum diseases, a world review: Proceedings of the international workshop on sorghum diseases, sponsored jointly by Texas A&M University, USA, and ICRISAT, Patancheru, pp 300–305
Esechie HA, Maranville JW, Ross WM (1977) Relationship of stalk morphology and chemical composition to lodging resistance in sorghum. Crop Sci 17:609–612
Frezzi M, Teyssandier EE (1980) Summay and historical review of sorghum in Argentina. In: Sorghum diseases—a world review. Proceedings of the international workshop on sorghum diseases, pp 11–14
Funnell-Harris DL, Pedersen JF, Sattler SE (2010) Alteration in lignin biosynthesis restricts growth of Fusarium spp. in brown midrib sorghum. Phytopathology 100:671–681
Funnell-Harris DL, Gfbru U, States U (2014) Response of Fusarium thapsinum to sorghum Brown midrib lines and to phenolic metabolites. Plant Dis 98:1300–1308
Funnell-Harris DL, Neill PMO, Gfbru U, States U (2016) Response of sweet sorghum lines to stalk pathogens Fusarium thapsinum and Macrophomina phaseolina. Plant Dis 100:896–903
Funnell-Harris DL, Neill PMO, Sattler SE et al (2017) Response of sorghum stalk pathogens to brown midrib plants and soluble phenolic extracts from near isogenic lines. Eur J Plant Pathol 148:941–953. https://doi.org/10.1007/s10658-017-1148-2
Funnell-Harris DL, Neill PMO, Sattler SE (2018) Field response of near-isogenic brown midrib sorghum lines to fusarium stalk rot, and response of wildtype lines to controlled water deficit. Plant Pathol 67:1474–1482. https://doi.org/10.1111/ppa.12863
Funnell-Harris DL, Sattler SE, Neill PMO et al (2019) Response of sorghum enhanced in monolignol biosynthesis to stalk rot pathogens. Plant Dis 103:2277–2287. https://doi.org/10.1094/PDIS-09-18-1622-RE
George-Jaeggli B, Jordan DR, van Oosterom EJ, Hammer GL (2011) Decrease in sorghum grain yield due to the dw3 dwarfing gene is caused by reduction in shoot biomass. Field Crop Res 124:231–239. https://doi.org/10.1016/j.fcr.2011.07.005
Gomez FE, Muliana AH, Niklas KJ, Rooney WL (2017) Identifying morphological and mechanical traits associated with stem lodging in bioenergy sorghum (Sorghum bicolor). Bioenergy Res 10:635–647. https://doi.org/10.1007/s12155-017-9826-7
Gomez FE, Muliana AH, Rooney WL (2018) Predicting stem strength in diverse bioenergy sorghum genotypes. Crop Sci 58:739–751. https://doi.org/10.2135/cropsci2017.09.0588
Hadebe ST, Modi AT, Mabhaudhi T (2017) Drought tolerance and water use of cereal crops: a focus on sorghum as a food security crop in Sub-Saharan Africa. J Agron Crop Sci 203:177–191. https://doi.org/10.1111/jac.12191
Hennig C (2018) fpc: flexible procedures for clustering. R package version 2.1-11.1
Henzell RG, Hare BW (1996) Sorghum breeding in Austrlaia—public and private endeavours. In: Proceedings of the third Australian sorghum conference, pp 159–171
Henzell RG, Dodman RL, Done AA, et al (1984) Lodging, stalk rot, and root rot in sorghum in Australia. In: Mughogho L, Rosenberg G (eds) Sorghum root and stalk rots, a critical reivew: proceedings of the consultative group discussion on research needs and strategies for control of sorghum root and stalk rot diseases, 27 Nov–2 Dec 1983, Bellagio. Patancheru. ICR. International Crops Research Institute for the Semi-Arid Tropics, Bellagio, pp 225–236
Henzell R, Brengman RL, Fletcher DS, McCosker AN (1992) Relationship between yield and staygreen in some grain sorghum hybrids grown under terminal drought stress. In: Proceedings of the second Australian sorghum conference, pp 355–359
Higuchi T (2006) Look back over the studies of lignin biochemistry. J Wood Sci 52:2–8. https://doi.org/10.1007/s10086-005-0790-z
Johnson JW, Stegmeier WD, Andrews DJ et al (1997) Genetic resistance to lodging. In: Proceedings of the international conference on genetic improvement of sorghum and pearl millet, Lubbock, pp 481–489
Jordan DR, Tao Y, Godwin ID et al (2003) Prediction of hybrid performance in grain sorghum using RFLP markers. Theor Appl Genet 106:559–567. https://doi.org/10.1007/s00122-002-1144-5
Jordan DR, Hunt CH, Cruickshank AW et al (2012) The relationship between the stay-green trait and grain yield in elite sorghum hybrids grown in a range of environments. Crop Sci 52:1153–1161. https://doi.org/10.2135/cropsci2011.06.0326
Jun S-Y, Walker AM, Kim H et al (2017) The enzyme activity and substrate specificity of two major cinnamyl alcohol dehydrogenases in sorghum (Sorghum bicolor), SbCAD2 and SbCAD4. Plant Physiol 174:2128–2145. https://doi.org/10.1104/pp.17.00576
Jun S-Y, Sattler SA, Cortez GS et al (2018) Biochemical and structural analysis of substrate specificity of a phenylalanine ammonia-lyase. Plant Physiol 176:1452–1468. https://doi.org/10.1104/pp.17.01608
Kebede H, Subudhi PK, Rosenow DT, Nguyen HT (2001) Quantitative trait loci influencing drought tolerance in grain sorghum (Sorghum bicolor L. Moench). Theor Appl Genet 103:266–276. https://doi.org/10.1007/s001220100541
Kholová J, Mclean G, Vadez V et al (2013) Drought stress characterization of post-rainy season (rabi) sorghum in India. Field Crop Res 141:38–46. https://doi.org/10.1016/j.fcr.2012.10.020
Kilian A, Wenzl P, Huttner E et al (2012) Diversity arrays technology: a generic genome profiling technology on open platforms. In: Pompanon F, Bonin A (eds) Data production and analysis in population genomics. Methods in molecular biology (methods and protocols), vol 888. Humana Press, Totowa, pp 67–89
Liu X, Huang M, Fan B et al (2016) Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PLoS Genet. https://doi.org/10.1186/1471-2156-13-100
Mace ES, Rami J-FF, Bouchet S et al (2009) A consensus genetic map of sorghum that integrates multiple component maps and high-throughput Diversity Array Technology (DArT) markers. BMC Plant Biol 9:13. https://doi.org/10.1186/1471-2229-9-13
Mace ES, Singh V, Van Oosterom EJ et al (2012) QTL for nodal root angle in sorghum (Sorghum bicolor L. Moench) co-locate with QTL for traits associated with drought adaptation. Theor Appl Genet 124:97–109
Mace ES, Hunt CH, Jordan DR (2013) Supermodels: sorghum and maize provide mutual insight into the genetics of flowering time. Theor Appl Genet 126:1377–1395. https://doi.org/10.1007/s00122-013-2059-z
Murray SC, Rooney WL, Mitchell SE et al (2008) Genetic improvement of sorghum as a biofuel feedstock: II. QTL for stem and leaf structural carbohydrates. Crop Sci 48:2180–2193
Pinthus MJ (1974) Lodging in wheat, barley, and oats: the phenomenom, its causes, and preventive measures. Adv Agron 25:209–263
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
Rosenow DT (1977) Breeding for lodging resistance in sorghum. In: Proceedings of the 32nd annual corn and sorghum research conference, 6–8 Dec, Chicago, pp 171–185
Rosenow DT (1980) Stalk rot resistance breeding in Texas. In: ICRISAT (International Crops Research Institute for the Semi-Arid Tropics) (ed) Sorghum diseases, a wrold review: proceedings of the international workshop on sorghum diseases, Hyderabad, pp 306–314
Rosenow DT (1984) Breeding for resistance to root and stalk rots in Texas. In: Interanational Crops Research Institute for the Semi-Arid Tropics (ed) Sorghum root and stalk rots, a critical reivew: proceedings of the consultative group discussion on research needs and strategies for control of sorghum root and stalk rot diseases, 27 Nov–2 Dec 1983, Bellagio. ICR, Patancheru, pp 209–218
Rosenow DT, Clark LE (1995) Drought and lodging resistance for a quality sorghum crop. In: Fiftieth annual corn and sorghum industry research conference, 6–7 Dec 1995. American Seed Trade Association, Chicago, pp 82–97
Rosenow DT, Quisenberry JE, Wendt CW, Clark LE (1983) Drought tolerant sorghum and cotton germplasm. Agric Water Manag 7:207–222. https://doi.org/10.1016/0378-3774(83)90089-6
Rosenow DT, Ejeta G, Clark LE et al (1997) Breeding for pre- and post-flowering drought stress resistance in sorghum. In: Proceedings of the international conference on genetic improvement of sorghum and pearl millet, pp 400–411
Saballos A, Ejeta G, Sanchez E et al (2009) A genomewide analysis of the cinnamyl alcohol dehydrogenase family in sorghum [Sorghum bicolor (L.) Moench] identifies SbCAD2 as the brown midrib6 gene. Genetics 181:783–795. https://doi.org/10.1534/genetics.108.098996
Saballos A, Sattler SE, Sanchez E et al (2012) Brown midrib2 (Bmr2) encodes the major 4-coumarate: coenzyme A ligase involved in lignin biosynthesis in sorghum (Sorghum bicolor (L.) Moench). Plant J 70:818–830. https://doi.org/10.1111/j.1365-313X.2012.04933.x
Sattler SE, Saathoff AJ, Haas EJ et al (2009) A nonsense mutation in a cinnamyl alcohol dehydrogenase gene is responsible for the sorghum brown midrib6 phenotype. Plant Physiol 150:584–595. https://doi.org/10.1104/pp.109.136408
Sattler SA, Walker AM, Vermerris W et al (2017) Structural and biochemical characterization of cinnamoyl-CoA reductases. Plant Physiol 173:1031–1044. https://doi.org/10.1104/pp.16.01671
Scheideler M, Schlaich NL, Fellenberg K et al (2002) Monitoring the switch from housekeeping to pathogen defense metabolism in Arabidopsis thaliana using cDNA arrays. J Biol Chem 277:10555–10561. https://doi.org/10.1074/jbc.M104863200
Schertz KF, Rosenow DT (1977) Anatomical variation in stalk internodes of sorghum. Crop Sci 17:628–631
Smith A, Cullis B, Thompson R (2001) Analyzing variety by environment data using multiplicative mixed models and adjustments. Biometrics 57:1138–1147. https://doi.org/10.1111/j.0006-341X.2001.01138.x
Srinivasa Reddy P, Fakrudin B, Rajkumar et al (2008) Molecular mapping of genomic regions harboring QTLs for stalk rot resistance in sorghum. Euphytica 159:191–198. https://doi.org/10.1007/s10681-007-9472-9
Sun Q, Liu X, Yang J et al (2018) microRNA528 affects lodging resistance of maize by regulating lignin biosynthesis under nitrogen-luxury conditions. Mol Plant 11:806–814. https://doi.org/10.1016/j.molp.2018.03.013
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78. https://doi.org/10.1093/jhered/93.1.77
Walker AM, Hayes RP, Youn B et al (2013) Elucidation of the structure and reaction mechanism of sorghum hydroxycinnamoyltransferase and its structural relationship to other coenzyme a-dependent transferases and synthases. Plant Physiol 162:640–651. https://doi.org/10.1104/pp.113.217836
Walker AM, Sattler SA, Regner M et al (2016) The structure and catalytic Mechanism of Sorghum bicolor Caffeoyl-CoA O -methyltransferase. Plant Physiol 172:78–92. https://doi.org/10.1104/pp.16.00845
Wang J, Feng J, Jia W et al (2017) Genome-wide identification of Sorghum bicolor laccases reveals potential targets for lignin modification. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00714
Xia J, Zhao Y, Burks P, Pauly M, Brown PJ (2018) A sorghum NAC gene is associated with variation in biomass properties and yield potential. Plant Direct 2(7):1–11. https://doi.org/10.1002/pld3.70
Zhang L-M, Leng C-Y, Luo H et al (2018) Sweet sorghum originated through selection of Dry, a plant-specific NAC transcription factor gene. Plant Cell 30:2286–2307. https://doi.org/10.1105/tpc.18.00313
Zhang J, Fengler KA, Van Hemert JL et al (2019) Identification and characterization of a novel stay-green QTL that increases yield in maize. Plant Biotechnol J 17:2272–2285. https://doi.org/10.1111/pbi.13139
Zhang Z, Zhang X, Lin Z et al (2020) A large transposon insertion in the stiff1 promoter increases stalk strength in maize. Plant Cell 32:152–165. https://doi.org/10.1105/tpc.19.00486
We would like to acknowledge the sorghum pre-breeding team at Hermitage Research Facility for support of the field trials.
XW was financially supported by an Australian Government Research Training Program Scholarship and a Centennial Scholarship from The University of Queensland (UQ). This study was supported by the Department of Agriculture and Fisheries in Queensland (DAF), UQ and the Grains Research and Development Corporation (GRDC) sorghum pre-breeding project (UQ00070).
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Communicated by Hai-Chun Jing.
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Wang, X., Mace, E., Tao, Y. et al. Large-scale genome-wide association study reveals that drought-induced lodging in grain sorghum is associated with plant height and traits linked to carbon remobilisation. Theor Appl Genet 133, 3201–3215 (2020). https://doi.org/10.1007/s00122-020-03665-2