Abstract
Key message
GWAS analysis revealed variations at loci harboring seed storage, late embryogenesis abundant protein, and a tannin biosynthesis gene associated with sorghum grain mold resistance.
Abstract
Grain mold is the most important disease of sorghum [Sorghum bicolor (L.) Moench]. It starts at the early stages of grain development due to concurrent infection by multiple fungal species. The genetic architecture of resistance to grain mold is poorly understood. Using a diverse set of 635 Ethiopian sorghum accessions, we conducted a multi-stage disease rating for resistance to grain mold under natural infestation in the field. Through genome-wide association analyses with 173,666 SNPs and multiple models, two novel loci were identified that were consistently associated with grain mold resistance across environments. Sequence variation at new loci containing sorghum KAFIRIN gene encoding a seed storage protein affecting seed texture and LATE EMBRYOGENESIS ABUNDANT 3 (LEA3) gene encoding a protein that accumulates in seeds, previously implicated in stress tolerance, were significantly associated with grain mold resistance. The KAFIRIN and LEA3 loci were also significant factors in grain mold resistance in accessions with non-pigmented grains. Moreover, we consistently detected the known SNP (S4_62316425) in TAN1 gene, a regulator of tannin accumulation in sorghum grain to be significantly associated with grain mold resistance. Identification of loci associated with new mechanisms of resistance provides fresh insight into genetic control of the trait, while the highly resistant accessions can serve as sources of resistance genes for breeding. Overall, our association data suggest the critical role of loci harboring seed protein genes and implicate grain chemical and physical properties in sorghum grain mold resistance.
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Abbreviations
- ANOVA:
-
Analysis of variance
- BLINK:
-
Bayesian-information and linkage-disequilibrium iteratively nested keyway
- CMLM:
-
Compressed mixed liner model
- DTF:
-
Days to flowering
- FarmCPU:
-
Fixed and random model circulating probability unification
- FGMR:
-
Field (plot) grain mold rating
- GLM:
-
Generalized linear model
- GWAS:
-
Genome-wide association study
- LEA:
-
Late embryogenesis abundant
- MLM:
-
Mixed linear model
- PCA:
-
Principal components analysis
- PGMR:
-
Panicle grain mold rating
- PHT:
-
Plant height
- SNP:
-
Single nucleotide polymorphism
- TGMR:
-
Threshed grain mold rating
References
Audilakshmi S, Stenhouse JW, Reddy TP, Prasad MVR (1999) Grain mould resistance and associated characters of sorghum genotypes. Euphytica 107(2):91–103. https://doi.org/10.1023/a:1026410913896
Awika JM, Rooney LW (2004) Sorghum phytochemicals and their potential impact on human health. Phytochemistry 65(9):1199–1221. https://doi.org/10.1016/j.phytochem.2004.04.001
Awika JM, Rooney LW, Waniska RD (2004) Properties of 3-deoxyanthocyanins from sorghum. J Agric Food Chem 52(14):4388–4394. https://doi.org/10.1021/jf049653f
Bates D, Machler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48. https://doi.org/10.18637/jss.v067.i01
Baudry A, Heim MA, Dubreucq B, Caboche M, Weisshaar B, Lepiniec L (2004) TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana. Plant J 39(3):366–380. https://doi.org/10.1111/j.1365-313X.2004.02138.x
Belton PS, Delgadillo I, Halford NG, Shewry PR (2006) Kafirin structure and functionality. J Cereal Sci 44:272–286
Boddu J, Svabek C, Sekhon R, Gevens A, Nicholson RL, Jones AD, Pedersen JF, Gustine DL, Chopra S (2004) Expression of a putative flavonoid 3′-hydroxylase in sorghum mesocotyls synthesizing 3-deoxyanthocyanidin phytoalexins. Physiol Mol Plant Pathol 65(2):101–113
Boddu J, Svabek C, Ibraheem F, Jones AD, Chopra S (2005) Characterization of a deletion allele of a sorghum Myb gene, yellow seed1 showing loss of 3-deoxyflavonoids. Plant Sci 169(3):542–552. https://doi.org/10.1016/j.plantsci.2005.05.007
Bouchet S, Olatoye MO, Marla SR, Perumal R, Tesso T, Yu J, Tuinstra M, Morris GP (2017) Increased power to dissect adaptive traits in global sorghum diversity using a nested association mapping population. Genetics 206(2):573–585. https://doi.org/10.1534/genetics.116.198499
Breia R, Conde A, Pimentel D, Conde C, Fortes AM, Granell A, Gerós H (2019) VvSWEET7 is a mono- and disaccharide transporter up-regulated in response to Botrytis cinerea infection in grape berries. Front Plant Sci. https://doi.org/10.3389/fpls.2019.01753
Chala A, Taye W, Ayalew A, Krska R, Sulyok M, Logrieco A (2014) Multimycotoxin analysis of sorghum (Sorghum bicolor L. Moench) and finger millet (Eleusine coracana L. Garten) from Ethiopia. Food Control 45:29–35. https://doi.org/10.1016/j.foodcont.2014.04.018
Chen LQ (2014) SWEET sugar transporters for phloem transport and pathogen nutrition. New Phytol 201(4):1150–1155
Chen ZY, Brown RL, Damann KE, Cleveland TE (2002) Identification of unique or elevated levels of kernel proteins in aflatoxin-resistant maize genotypes through proteome analysis. Phytopathology 92(10):1084–1094. https://doi.org/10.1094/PHYTO.2002.92.10.1084
Chen ZY, Brown RL, Damann KE, Cleveland TE (2007) Identification of maize kernel endosperm proteins associated with resistance to aflatoxin contamination by Aspergillus flavusz. Phytopathology 97(9):1094–1103. https://doi.org/10.1094/phyto-97-9-1094
Cuevas HE, Fermin-Perez RA, Prom LK, Cooper EA, Bean S, Rooney WL (2019) Genome-wide association mapping of grain mold resistance in the US Sorghum Association Panel. Plant Genome 12(2):180070. https://doi.org/10.3835/plantgenome2018.09.0070
da Silva JB, Pozzi CR, Mallozzi MAB, Ortega EM, Corrêa B (2000) Mycoflora and occurrence of aflatoxin B1 and fumonisin B1 during storage of Brazilian sorghum. J Agric Food Chem 48(9):4352–4356. https://doi.org/10.1021/jf990054w
Eckardt NA (2011) Induction of phytoalexin biosynthesis: WRKY33 is a target of MAPK signaling. Plant Cell 23(4):1190
Emmambux NM, Taylor JRN (2003) Sorghum kafirin interaction with various phenolic compounds. J Sci Food Agric 83(5):402–407
Esele JP, Frederiksen RA, Miller FR (1993) The association of genes controlling caryopsis traits with grain mold resistance in sorghum. Phytopathology 83(5):490–495. https://doi.org/10.1094/Phyto-83-490
Esen AA (1987) Proposed nomenclature for the alcohol-soluble proteins (zeins) of maize (Zea mays L.). J Cereal Sci 5:117–128
Gebauer P, Korn M, Engelsdorf T, Sonnewald U, Koch C, Voll LM (2017) Sugar accumulation in leaves of Arabidopsis sweet11/sweet12 double mutants enhances priming of the salicylic acid-mediated defense response. Front Plant Sci. https://doi.org/10.3389/fpls.2017.01378
Girma G, Nida H, Seyoum A, Mekonen M, Nega A, Lule D, Dessalegn K, Bekele A, Gebreyohannes A, Adeyanju A, Tirfessa A, Ayana G, Taddese T, Mekbib F, Belete K, Tesso T, Ejeta G, Mengiste T (2019) A large-scale genome-wide association analyses of Ethiopian sorghum landrace collection reveal loci associated with important traits. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00691
Girma G, Nida H, Tirfessa A, Lule D, Bejiga T, Seyoum A, Mekonen M, Nega A, Dessalegn K, Birhanu C, Bekele A, Gebreyohannes A, Ayana G, Tesso T, Ejeta G, Mengiste T (2020) A comprehensive phenotypic and genomic characterization of Ethiopian sorghum germplasm defines core collection and reveals rich genetic potential in adaptive traits. Plant Genome 13(3):e20055. https://doi.org/10.1002/tpg2.20055
Glaubitz JC, Casstevens TM, Lu F, Harriman J, Elshire RJ, Sun Q, Buckler ES (2014) TASSEL-GBS: a high capacity genotyping by sequencing analysis pipeline. PLoS ONE 9(2):e90346. https://doi.org/10.1371/journal.pone.0090346
Gonzalez A, Zhao M, Leavitt JM, Lloyd AM (2008) Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J 53(5):814–827. https://doi.org/10.1111/j.1365-313X.2007.03373.x
Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186. https://doi.org/10.1093/nar/gkr944
Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388(Pt 1):151–157. https://doi.org/10.1042/bj20041931
Haas BJ, Salzberg SL, Zhu W, Pertea M, Allen JE, Orvis J, White O, Buell CR, Wortman JR (2008) Automated eukaryotic gene structure annotation using EVidenceModeler and the program to assemble spliced alignments. Genome Biol 9(1):R7. https://doi.org/10.1186/gb-2008-9-1-r7
Hamaker BR, Mohamed AA, Habben JE, Huang CP, Larkins BA (1995) Efficient procedure for extracting maize and sorghum kernel proteins reveals higher prolamin contents than the conventional method. Cereal Chem 72:583–588
Hilley J, Truong S, Olson S, Morishige D, Mullet J (2016) Identification of Dw1, a regulator of sorghum stem internode length. PLoS ONE 11(3):e0151271. https://doi.org/10.1371/journal.pone.0151271
Hipskind JD, Hanau R, Leite B, Nicholson RL (1990) Phytoalexin accumulation in sorghum—identification of an apigeninidin acyl ester. Physiol Mol Plant Pathol 36(5):381–396
Huang Y, Li L, Smith KP, Muehlbauer GJ (2016) Differential transcriptomic responses to Fusarium graminearum infection in two barley quantitative trait loci associated with Fusarium head blight resistance. BMC Genomics 17:387. https://doi.org/10.1186/s12864-016-2716-0
Huang M, Liu X, Zhou Y, Summers RM, Zhang Z (2019) BLINK: a package for the next level of genome-wide association studies with both individuals and markers in the millions. Gigascience. https://doi.org/10.1093/gigascience/giy154
Hundertmark M, Hincha DK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9:118. https://doi.org/10.1186/1471-2164-9-118
Ibraheem F, Gaffoor I, Chopra S (2010) Flavonoid phytoalexin-dependent resistance to anthracnose leaf blight requires a functional yellow seed1 in sorghum bicolor. Genetics 184(4):915–926. https://doi.org/10.1534/genetics.109.111831
Ibraheem F, Gaffoor I, Tan QX, Shyu CR, Chopra S (2015) A sorghum MYB transcription factor induces 3-deoxyanthocyanidins and enhances resistance against leaf blights in maize. Molecules 20(2):2388–2404. https://doi.org/10.3390/molecules20022388
Kishi-Kaboshi M, Takahashi A, Hirochika H (2010) MAMP-responsive MAPK cascades regulate phytoalexin biosynthesis. Plant Signal Behav 5(12):1653–1656. https://doi.org/10.4161/psb.5.12.13982
Klein RR, Rodriguez-Herrera R, Schlueter JA, Klein PE, Yu ZH, Rooney WL (2001) Identification of genomic regions that affect grain-mould incidence and other traits of agronomic importance in sorghum. Theor Appl Genet 102(2–3):307–319. https://doi.org/10.1007/s001220051647
Klemens PA, Patzke K, Deitmer J, Spinner L, Le Hir R, Bellini C, Bedu M, Chardon F, Krapp A, Neuhaus HE (2013) Overexpression of the vacuolar sugar carrier AtSWEET16 modifies germination, growth, and stress tolerance in Arabidopsis. Plant Physiol 163(3):1338–1352. https://doi.org/10.1104/pp.113.224972
Leslie JF (2014) Mycotoxins in the sorghum grain chain. In: Leslie JF, Logerico AF (eds) Mycotoxin reduction in grain chains. Wiley, New York, pp 282–296
Li S, Chakraborty N, Borcar A, Menze MA, Toner M, Hand SC (2012) Late embryogenesis abundant proteins protect human hepatoma cells during acute desiccation. Proc Natl Acad Sci USA 109(51):20859–20864. https://doi.org/10.1073/pnas.1214893109
Li X, Fridman E, Tesso TT, Yu J (2015) Dissecting repulsion linkage in the dwarfing gene Dw3 region for sorghum plant height provides insights into heterosis. Proc Natl Acad Sci USA 112(38):11823–11828. https://doi.org/10.1073/pnas.1509229112
Li S, Wang W, Gao J, Yin K, Wang R, Wang C, Petersen M, Mundy J, Qiu JL (2016) MYB75 phosphorylation by MPK4 is required for light-induced anthocyanin accumulation in arabidopsis [OPEN]. Plant Cell 28(11):2866–2883. https://doi.org/10.1105/tpc.16.00130
Liu Y, Chakrabortee S, Li R, Zheng Y, Tunnacliffe A (2011) Both plant and animal LEA proteins act as kinetic stabilisers of polyglutamine-dependent protein aggregation. FEBS Lett 585(4):630–634. https://doi.org/10.1016/j.febslet.2011.01.020
Liu Y, Wang L, Xing X, Sun L, Pan J, Kong X, Zhang M, Li D (2013) ZmLEA3, a multifunctional group 3 LEA protein from maize (Zea mays L.), is involved in biotic and abiotic stresses. Plant Cell Physiol. 54(6):944–959
Liu X, Huang M, Fan B, Buckler ES, Zhang Z (2016) Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PLoS Genet. https://doi.org/10.1371/journal.pgen.1005767
Liu J, Li L, Foroud NA, Gong X, Li C, Li T (2019) Proteomics of bulked rachides combined with documented QTL uncovers genotype nonspecific players of the fusarium head blight responses in wheat. Phytopathology 109(1):111–119
Lo SC, Nicholson RL (1998) Reduction of light induced anthocyanin accumulation in inoculated sorghum mesocotyls. Plant Physiol 116:979–989
Lo SCC, De Verdier K, Nicholson RL (1999) Accumulation of 3-deoxyanthocyanidin phytoalexins and resistance to Colletotrichum sublineolum in sorghum. Physiol Mol Plant Pathol 55(5):263–273. https://doi.org/10.1006/pmpp.1999.0231
Mace ES, Jordan DR (2010) Location of major effect genes in sorghum (Sorghum bicolor (L.) Moench). Theor Appl Genet 121:1339–1356
Mace ES, Innes D, Hunt C, Wang X, Tao Y, Baxter J, Hassall M, Hathorn A, Jordan DR (2018) The sorghum QTL atlas: a powerful tool for trait dissection, comparative genomics and crop improvement. Theor Appl Genet 132(3):751–766. https://doi.org/10.1007/s00122-018-3212-5
Magwanga RO, Lu P, Kirungu JN, Lu H, Wang X, Cai X, Zhou Z, Zhang Z, Salih H, Wang K, Liu F (2018) Characterization of the late embryogenesis abundant (LEA) proteins family and their role in drought stress tolerance in upland cotton. BMC Genet. https://doi.org/10.1186/s12863-017-0596-1
McCormick RF, Truong SK, Sreedasyam A, Jenkins J, Shu SQ, Sims D, Kennedy M, Amirebrahimi M, Weers BD, McKinley B, Mattison A, Morishige DT, Grimwood J, Schmutz J, Mullet JE (2018) The sorghum bicolor reference genome: improved assembly, gene annotations, a transcriptome atlas, and signatures of genome organization. Plant J 93(2):338–354. https://doi.org/10.1111/tpj.13781
Meckenstock DH, Gomez F, Rosenow DT, Guiragossian V (1993) Registration of ‘sureno’ sorghum. Crop Sci 33:213
MelakeBerhan A, Butler LG, Ejeta G, Menkir A (1996) Grain mold resistance and polyphenol accumulation in sorghum. J Agric Food Chem 44(8):2428–2434. https://doi.org/10.1021/jf950580x
Mengistu G, Shimelis H, Laing M, Lule D, Mathew I (2020) Genetic variability among Ethiopian sorghum landrace accessions for major agro-morphological traits and anthracnose resistance. Euphytica 216:1–15
Menkir A, Ejeta G, Butler L, Melakeberhan A (1996) Physical and chemical kernel properties associated with resistance to grain mold in sorghum. Cereal Chem 73(5):613–617
Mizuno H, Yazawa T, Kasuga S, Sawada Y, Ogata J, Ando T, Kanamori H, Yonemaru J, Wu J, Hirai MY, Matsumoto T, Kawahigashi H (2014) Expression level of a flavonoid 3′-hydroxylase gene determines pathogen-induced color variation in sorghum. BMC Res Notes. https://doi.org/10.1186/1756-0500-7-761
Morris GP, Rhodes DH, Brenton Z, Ramu P, Thayil VM, Deshpande S, Hash CT, Acharya C, Mitchell SE, Buckler ES, Yu JM, Kresovich S (2013) Dissecting genome-wide association signals for loss-of-function phenotypes in sorghum flavonoid pigmentation traits. G3-Genes Genomes Genet 3(11):2085–2094. https://doi.org/10.1534/g3.113.008417
Navi SS, Bandyopadhyay R, Hall AJ, Bramel-Cox PJ (1999) A pictorial guide for the identification of mold fungi on sorghum grain. Information bulletin no. 59 (In En. Summaries in En, Fr). International Crops Research Institute for the Semi-Arid Tropics, Patancheru 502 324, Andhra Pradesh, India
Nida H, Girma G, Mekonen M, Lee S, Seyoum A, Dessalegn K, Tadesse T, Ayana G, Senbetay T, Tess T, Ejeta G, Mengiste T (2019) Identification of sorghum grain mold resistance loci through genome wide association mapping. J Cereal Sci 85:295–304
Prom LK, Cuevas HE, Ahn E, Isakeit T, Rooney WL, Magill C (2020) Genome-wide association study of grain mold resistance in sorghum association panel as affected by inoculation with Alternaria alternate alone and Alternaria alternata, Fusarium thapsinum, and Curvularia lunata combined. Eur J Plant Pathol 157:783–798
Quinby JR, Karper RE (1954) Inheritance of height in sorghum. Agron J 46(5):211–216
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ren D, Liu Y, Yang KY, Han L, Mao G, Glazebrook J, Zhang S (2008) A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proc Natl Acad Sci USA 105(14):5638–5643. https://doi.org/10.1073/pnas.0711301105
Revelle W (2019) Psych: procedures for psychological, psychometric, and personality research. Northwestern University, Evanston. R package version 1.9.12. https://CRAN.R-project.org/package=psych
Rhodes DH, Hoffmann L Jr, Rooney WL, Ramu P, Morris GP, Kresovich S (2014) Genome-wide association study of grain polyphenol concentrations in global sorghum [Sorghum bicolor (L.) Moench] germplasm. J Agric Food Chem 62(45):10916–10927. https://doi.org/10.1021/jf503651t
Shull JM, Watterson JJ, Kirleis AW (1991) Proposed nomenclature for the alcohol-soluble proteins (kafirins) of sorghum bicolor (L. Moench) based on molecular weight, solubility, and structure. J Agric Food Chem 39:83–87
Snyder BA, Nicholson RL (1990) Synthesis of phytoalexins in sorghum as a site-specific response to fungal ingress. Science 248(4963):1637–1639. https://doi.org/10.1126/science.248.4963.1637
Song R, Segal G, Messing J (2004) Expression of the sorghum 10-member kafirin gene cluster in maize endosperm. Nucleic Acids Res 32(22):e189. https://doi.org/10.1093/nar/gnh183
Streubel J, Pesce C, Hutin M, Koebnik R, Boch J, Szurek B (2013) Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv. oryzae. New Phytol 200(3):808–819
Styles ED, Ceska O (1989) Pericarp flavonoids in genetic strains of Zea mays. Maydica 34:227–237
Taylor J, Bean SR, Ioerger BP, Taylor JRN (2007) Preferential binding of sorghum tannins with γ-kafirin and the influence of tannin binding on kafirin digestibility and biodegradation. J Cereal Sci 46:22–31
Thakur RP, Reddy BVS, Indira S, Rao VP, Navi SS, Yang XB, Ramesh S (2006) Sorghum grain mold. Information bulletin no. 72. International Crops Research Institute for the semi-arid tropics, Patancheru 502324, Andhra Pradesh, India
Upadhyaya HD, Wang YH, Sharma R, Sharma S (2013) SNP markers linked to leaf rust and grain mold resistance in sorghum. Mol Breed 32(2):451–462. https://doi.org/10.1007/s11032-013-9883-3
VanRaden PM (2008) Efficient methods to compute genomic predictions. J Dairy Sci 91(11):4414–4423. https://doi.org/10.3168/jds.2007-0980
Velazco JG, Rodriguez-Alvarez MX, Boer MP, Jordan DR, Eilers PHC, Malosetti M, van Eeuwijk FA (2017) Modelling spatial trends in sorghum breeding field trials using a two-dimensional P-spline mixed model. Theor Appl Genet 130(7):1375–1392. https://doi.org/10.1007/s00122-017-2894-4
Walker AR, Davison PA, Bolognesi-Winfield AC, James CM, Srinivasan N, Blundell TL, Esch JJ, Marks MD, Gray JC (1999) The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11(7):1337–1350
Wang J, Zhang Z (2018) GAPIT version 3: an interactive analytical tool for genomic association and prediction. preprint
Winn JA, Mason RE, Robbins AL, Rooney WL, Hays DB (2009) QTL mapping of a high protein digestibility trait in sorghum bicolor. Int J Plant Genomics. https://doi.org/10.1155/2009/471853
Wu YY, Li XR, Xiang WW, Zhu CS, Lin ZW, Wu Y, Li JR, Pandravada S, Ridder DD, Bai GH, Wang ML, Trick HN, Bean SR, Tuinstra MR, Tesso TT, Yu JM (2012) Presence of tannins in sorghum grains is conditioned by different natural alleles of Tannin1. Proc Natl Acad Sci USA 109(26):10281–10286. https://doi.org/10.1073/pnas.1201700109
Wu Y, Yuan L, Guo X, Holding DR, Messing J (2013) Mutation in the seed storage protein kafirin creates a high-value food trait in sorghum. Nat Commun 4:2217. https://doi.org/10.1038/ncomms3217
Wu Y, Guo T, Mu Q et al (2019) Allelochemicals targeted to balance competing selections in African agroecosystems. Nat Plants 5(12):1229–1236. https://doi.org/10.1038/s41477-019-0563-0
Xu JH, Messing J (2009) Amplification of prolamin storage protein genes in different subfamilies of the poaceae. Theor Appl Genet 119(8):1397–1412. https://doi.org/10.1007/s00122-009-1143-x
Xu D, Duan X, Wang B, Hong B, Ho T, Wu R (1996) Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol 110(1):249–257
Xu JH, Bennetzen JL, Messing J (2012) Dynamic gene copy number variation in collinear regions of grass genomes. Mol Biol Evol 29(2):861–871. https://doi.org/10.1093/molbev/msr261
Yu JM, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38(2):203–208. https://doi.org/10.1038/ng1702
Zhang B, Schrader A (2017) Transparent Testa Glabra 1-dependent regulation of flavonoid biosynthesis. Plants. https://doi.org/10.3390/plants6040065
Zhang ZW, Ersoz E, Lai CQ, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ, Yu JM, Arnett DK, Ordovas JM, Buckler ES (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42(4):355-U118. https://doi.org/10.1038/ng.546
Acknowledgements
This study was made possible through funding by the Feed the Future Innovation Lab for Collaborative Research on Sorghum and Millet through grants from American People provided to the United States Agency for International Development (USAID) under cooperative agreement No. AID-OAA-A-13-00047. The contents are the sole responsibility of the authors and do not necessarily reflect the views of USAID or the United States Government. We are grateful for technical support by sorghum research staffs at Melkassa, Bako and Jimma Agricultural Research Centers.
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United States Agency for International Development (USAID) under cooperative agreement No. AID-OAA-A-13-00047.
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GE, TM conceived the project and supervised the research work; HN, GG, GE, TM initiated and designed field and genotyping experiments; HN, MM, AT, AS, TB, KD, CB, TS, GA, performed field experiments and prepared leaf tissue samples; HN, GG, TM analyzed data; HN conducted the experiments and wrote the manuscript; MM, AT, GG, TT, TM contributed to the project ideas and edited the manuscript; All authors have read and approved the final version of the manuscript.
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Nida, H., Girma, G., Mekonen, M. et al. Genome-wide association analysis reveals seed protein loci as determinants of variations in grain mold resistance in sorghum. Theor Appl Genet 134, 1167–1184 (2021). https://doi.org/10.1007/s00122-020-03762-2
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DOI: https://doi.org/10.1007/s00122-020-03762-2