Key message
Multi-environment QTL mapping identified 23 stable loci and 34 co-located QTL clusters for panicle architecture and grain yield-related traits, which provide a genetic basis for foxtail millet yield improvement.
Abstract
Panicle architecture and grain weight, both of which are influenced by genetic and environmental factors, have significant effects on grain yield potential. Here, we used a recombinant inbred line (RIL) population of 333 lines of foxtail millet, which were grown in 13 trials with varying environmental conditions, to identify quantitative trait loci (QTL) controlling nine agronomic traits related to panicle architecture and grain yield. We found that panicle weight, grain weight per panicle, panicle length, panicle diameter, and panicle exsertion length varied across different geographical locations. QTL mapping revealed 159 QTL for nine traits. Of the 159 QTL, 34 were identified in 2 to 12 environments, suggesting that the genetic control of panicle architecture in foxtail millet is sensitive to photoperiod and/or other environmental factors. Eighty-eight QTL controlling different traits formed 34 co-located QTL clusters, including the triple QTL cluster qPD9.2/qPL9.5/qPEL9.3, which was detected 23 times in 13 environments. Several candidate genes, including Seita.2G388700, Seita.3G136000, Seita.4G185300, Seita.5G241500, Seita.5G243100, Seita.9G281300, and Seita.9G342700, were identified in the genomic intervals of multi-environmental QTL or co-located QTL clusters. Using available phenotypic and genotype data, we conducted haplotype analysis for Seita.2G002300 and Seita.9G064000,which showed high correlations with panicle weight and panicle exsertion length, respectively. These results not only provided a basis for further fine mapping, functional studies and marker-assisted selection of traits related to panicle architecture in foxtail millet, but also provide information for comparative genomics analyses of cereal crops.
Similar content being viewed by others
References
Abu-Zaitoon YM (2014) Phylogenetic analysis of putative genes involved in the tryptophan-dependent pathway of auxin biosynthesis in rice. Appl Biochem Biotechnol 172:2480–2495
Ashikari M, Sakakibara H, Lin S, Yamamoto T, Takashi T, Nishimura A, Angeles ER, Qian Q, Kitano H, Matsuoka M (2005) Cytokinin oxidase regulates rice grain production. Science 309:741–745
Bommert P, Lunde C, Nardmann J, Vollbrecht E, Running M, Jackson D, Hake S, Werr W (2005) Thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase. Development (cambridge, England) 132:1235–1245
Chu H, Qian Q, Liang W, Yin C, Tan H, Yao X, Yuan Z, Yang J, Huang H, Luo D, Ma H, Zhang D (2006) The Floral Organ Number4 gene encoding a putative ortholog of Arabidopsis CLAVATA3 regulates apical meristem size in rice. Plant Physiol 142:1039–1052
Danilevskaya ON, Meng X, Ananiev EV (2010) Concerted modification of flowering time and inflorescence architecture by ectopic expression of TFL1-like genes in maize. Plant Physiol 153:238–251
Diao X, Jia G (2017) Foxtail Millet Germplasm and Inheritance of Morphological Characteristics. In: Doust A, Diao X (eds) Genetics and genomics of Setaria. Springer International Publishing, Cham, pp 73–92
Diao X, Schnable J, Bennetzen JL, Jiayang L (2014) Initiation of Setaria as a model plant. Front Agric Sci Eng 1:16–20
Doust A (2007) Architectural evolution and its implications for domestication in grasses. Ann Bot 100:941–950
Doust AN, Devos KM, Gadberry MD, Gale MD, Kellogg EA (2005) The genetic basis for inflorescence variation between foxtail and green millet (poaceae). Genetics 169:1659–1672
Doust AN, Kellogg EA, Devos KM, Bennetzen JL (2009) Foxtail millet: a sequence-driven grass model system. Plant Physiol 149:137–141
Fang X, Dong K, Wang X, Liu T, He J, Ren R, Zhang L, Liu R, Liu X, Li M, Huang M, Zhang Z, Yang T (2016) A high density genetic map and QTL for agronomic and yield traits in Foxtail millet [Setaria italica (L.) P. Beauv]. BMC Genomics 17:336
Gao X, Liang W, Yin C, Ji S, Wang H, Su X, Guo C, Kong H, Xue H-W, Zhang D (2010) The SEPALLATA-like gene OsMADS34 is required for rice inflorescence and spikelet development. Plant Physiol 153:728–740
He Q, Zhi H, Tang S, Xing L, Wang S, Wang H, Zhang A, Li Y, Gao M, Zhang H, Chen G, Dai S, Li J, Yang J, Liu H, Zhang W, Jia Y, Li S, Liu J, Qiao Z, Guo E, Jia G, Liu J, Diao X (2021) QTL mapping for foxtail millet plant height in multi-environment using an ultra-high density bin map. Theor Appl Genet 134:557–572
Hu H, Mauro-Herrera M, Doust AN (2018) Domestication and improvement in the model C4 grass. Setaria Front Plant Sci 9:719
Huang X, Qian Q, Liu Z, Sun H, He S, Luo D, Xia G, Chu C, Li J, Fu X (2009a) Natural variation at the DEP1 locus enhances grain yield in rice. Nat Genet 41:494–497
Huang XY, Chao DY, Gao JP, Zhu MZ, Shi M, Lin HX (2009b) A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes Dev 23:1805–1817
Huang P, Jiang H, Zhu C, Barry K, Jenkins J, Sandor L, Schmutz J, Box MS, Kellogg EA, Brutnell TP (2017) Sparse panicle1 is required for inflorescence development in Setaria viridis and maize. Nat Plants 3:17054
Hussin SH, Wang H, Tang S, Zhi H, Tang C, Zhang W, Jia G, Diao X (2021) SiMADS34, an E-class MADS-box transcription factor, regulates inflorescence architecture and grain yield in Setaria italica. Plant Mol Biol 105:419–434
Ikeda K, Nagasawa N, Nagato Y (2005) ABERRANT PANICLE ORGANIZATION 1 temporally regulates meristem identity in rice. Dev Biol 282:349–360
Jaiswal V, Gupta S, Gahlaut V, Muthamilarasan M, Bandyopadhyay T, Ramchiary N, Prasad M (2019) Genome-wide association study of major agronomic traits in foxtail millet (Setaria italica L.) Using ddRAD Sequencing. Sci Rep 9:5020
Jia G, Huang X, Zhi H, Zhao Y, Zhao Q, Li W, Chai Y, Yang L, Liu K, Lu H, Zhu C, Lu Y, Zhou C, Fan D, Weng Q, Guo Y, Huang T, Zhang L, Lu T, Feng Q, Hao H, Liu H, Lu P, Zhang N, Li Y, Guo E, Wang S, Wang S, Liu J, Zhang W, Chen G, Zhang B, Li W, Wang Y, Li H, Zhao B, Li J, Diao X, Han B (2013) A haplotype map of genomic variations and genome-wide association studies of agronomic traits in foxtail millet (Setaria italica). Nat Genet 45:957–961
Kobayashi K, Yasuno N, Sato Y, Yoda M, Yamazaki R, Kimizu M, Yoshida H, Nagamura Y, Kyozuka J (2012) Inflorescence meristem identity in rice is specified by overlapping functions of three AP1/FUL-like MADS box genes and PAP2, a SEPALLATA MADS box gene. Plant Cell 24:1848–1859
Komatsu M, Maekawa M, Shimamoto K, Kyozuka J (2001) The LAX1 and FRIZZY PANICLE 2 genes determine the inflorescence architecture of rice by controlling rachis-branch and spikelet development. Dev Biol 231:364–373
Komatsu K, Maekawa M, Ujiie S, Satake Y, Furutani I, Okamoto H, Shimamoto K, Kyozuka J (2003) LAX and SPA: major regulators of shoot branching in rice. Proc Natl Acad Sci U S A 100:11765–11770
Kurakawa T, Ueda N, Maekawa M, Kobayashi K, Kojima M, Nagato Y, Sakakibara H, Kyozuka J (2007) Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445:652–655
Kyozuka J, Tokunaga H, Yoshida A (2014) Control of grass inflorescence form by the fine-tuning of meristem phase change. Curr Opin Plant Biol 17:110–115
Li S, Zhao B, Yuan D, Duan M, Qian Q, Tang L, Wang B, Liu X, Zhang J, Wang J, Sun J, Liu Z, Feng YQ, Yuan L, Li C (2013) Rice zinc finger protein DST enhances grain production through controlling Gn1a/OsCKX2 expression. Proc Natl Acad Sci USA 110:3167–3172
Li S, Wang J, Zhang L (2015) Inclusive composite interval mapping of QTL by environment interactions in biparental populations. PLoS ONE 10:e0132414
Liu C, Teo ZW, Bi Y, Song S, Xi W, Yang X, Yin Z, Yu H (2013) A conserved genetic pathway determines inflorescence architecture in Arabidopsis and rice. Dev Cell 24:612–622
Liu T, He J, Dong K, Wang X, Wang W, Yang P, Ren R, Zhang L, Zhang Z, Yang T (2020) QTL mapping of yield component traits on bin map generated from resequencing a RIL population of foxtail millet (Setaria italica). BMC Genomics 21:141
Long JA, Moan EI, Medford JI, Barton MK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379:66–69
Lu H, Zhang J, Liu KB, Wu N, Li Y, Zhou K, Ye M, Zhang T, Zhang H, Yang X, Shen L, Xu D, Li Q (2009) Earliest domestication of common millet (Panicum miliaceum) in East Asia extended to 10,000 years ago. Proc Natl Acad Sci U S A 106:7367–7372
Mccouch S, Cho Y, Yano M, Paul E, Blinstrub M, Morishima H, Mccouch S, Cho Y, Paul E, Morishima H (1997) Report on QTL nomenclature. Rice Genet Newsl 14:11–13
Nakagawa M, Shimamoto K, Kyozuka J (2002) Overexpression of RCN1 and RCN2, rice TERMINAL FLOWER 1/CENTRORADIALIS homologs, confers delay of phase transition and altered panicle morphology in rice. Plant J 29:743–750
Nardmann J, Werr W (2007) The shoot stem cell Niche in angiosperms: expression patterns of WUS orthologues in rice and maize imply major modifications in the course of mono- and dicot evolution. Mol Biol Evol 23:2492–2504
Phillips KA, Skirpan AL, Liu X, Christensen A, Slewinski TL, Hudson C, Barazesh S, Cohen JD, Malcomber S, McSteen P (2011) Vanishing tassel2 encodes a grass-specific tryptophan aminotransferase required for vegetative and reproductive development in maize. Plant Cell 23:550–566
Qiao Y, Piao R, Shi J, Lee SI, Jiang W, Kim BK, Lee J, Han L, Ma W, Koh HJ (2011) Fine mapping and candidate gene analysis of dense and erect panicle 3, DEP3, which confers high grain yield in rice (Oryza sativa L.). Theor Appl Genet 122:1439–1449
Sazuka T, Kamiya N, Nishimura T, Ohmae K, Sato Y, Imamura K, Nagato Y, Koshiba T, Nagamura Y, Ashikari M, Kitano H, Matsuoka M (2009) A rice tryptophan deficient dwarf mutant, tdd1, contains a reduced level of indole acetic acid and develops abnormal flowers and organless embryos. Plant J 60:227–241
Suzaki T, Sato M, Ashikari M, Miyoshi M, Nagato Y, Hirano H-Y (2004) The gene FLORAL ORGAN NUMBER1 regulates floral meristern size in rice and encodes a leucine-rich repeat receptor kinase orthologous to Arabidopsis CLAVATA1. Development (cambridge, England) 131:5649–5657
Tsuda K, Ito Y, Sato Y, Kurata N (2011) Positive autoregulation of a KNOX gene is essential for shoot apical meristem maintenance in rice. Plant Cell 23:4368–4381
Vollbrecht E, Reiser L, Hake S (2000) Shoot meristem size is dependent on inbred background and presence of the maize homeobox gene, knotted1. Development (cambridge, England) 127:3161
Wang J, Wang Z, Du X, Yang H, Han F, Han Y, Yuan F, Zhang L, Peng S, Guo E (2017) A high-density genetic map and QTL analysis of agronomic traits in foxtail millet [Setaria italica (L.) P. Beauv.] using RAD-seq. PLoS ONE 12:e0179717
Wang Z, Wang J, Peng J, Du X, Jiang M, Li Y, Han F, Du G, Yang H, Lian S, Yong J, Cai W, Cui J, Han K, Yuan F, Chang F, Yuan G, Zhang W, Zhang L, Peng S, Zou H, Guo E (2019) QTL mapping for 11 agronomic traits based on a genome-wide Bin-map in a large F2 population of foxtail millet (Setaria italica (L.) P. Beauv.). Mol Breed 39:18
Wu Y, Wang Y, Mi XF, Shan JX, Li XM, Xu JL, Lin HX (2016) The QTL GNP1 Encodes GA20ox1, Which Increases Grain Number and Yield by Increasing Cytokinin Activity in Rice Panicle Meristems. PLoS Genet 12:e1006386
Xiang J, Tang S, Zhi H, Jia G, Wang H, Diao X (2017) Loose Panicle1 encoding a novel WRKY transcription factor, regulates panicle development, stem elongation, and seed size in foxtail millet [Setaria italica (L.) P. Beauv.]. PLoS ONE 12:e0178730
Xu M, Zhu L, Shou H, Wu P (2005) A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol 46:1674–1681
Yoshida A, Ohmori Y, Kitano H, Taguchi-Shiobara F, Hirano HY (2012) Aberrant spikelet and panicle1, encoding a TOPLESS-related transcriptional co-repressor, is involved in the regulation of meristem fate in rice. Plant J 70:327–339
Yoshida A, Sasao M, Yasuno N, Takagi K, Daimon Y, Chen R, Yamazaki R, Tokunaga H, Kitaguchi Y, Sato Y, Nagamura Y, Ushijima T, Kumamaru T, Iida S, Maekawa M, Kyozuka J (2013) TAWAWA1, a regulator of rice inflorescence architecture, functions through the suppression of meristem phase transition. Proc Natl Acad Sci USA 110:767–772
Zhang D, Yuan Z (2014) Molecular control of grass inflorescence development. Annu Rev Plant Biol 65:553–578
Zhang K, Fan G, Zhang X, Zhao F, Wei W, Du G, Feng X, Wang X, Wang F, Song G, Zou H, Zhang X, Li S, Ni X, Zhang G, Zhao Z (2017) Identification of QTLs for 14 agronomically important traits in setaria italica based on SNPs generated from high-throughput sequencing. G3 (bethesda) 7:1587–1594
Zhu K, Tang D, Yan C, Chi Z, Yu H, Chen J, Liang J, Gu M, Cheng Z (2010) Erect panicle2 encodes a novel protein that regulates panicle erectness in indica rice. Genetics 184:343–350
Acknowledgements
We thank Dr. Jin Gao helped in data analysis. This work was supported by National Key R&D Program of China (grant nos. 2019YFD1000700, and 2019YFD1000701), China Agricultural Research System (CARS06-13.5), National Natural Science foundation of China (31871630), China Postdoctoral Science Foundation (2018M641553), the Agricultural Science and Technology Innovation Program of CAAS (ICS2020YJ08BX-2), and the Agricultural Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences.
Funding
This work was supported by National Key R&D Program of China (grant nos. 2019YFD1000700, and 2019YFD1000701), China Agricultural Research System (CARS06-13.5), National Natural Science foundation of China (31871630), China Postdoctoral Science Foundation (2018M641553), the Agricultural Science and Technology Innovation Program of CAAS (ICS2020YJ08BX-2), and the Agricultural Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences.
Author information
Authors and Affiliations
Contributions
HZ and QH did data analysis and drafted the manuscript. XD and HZ designed the experiment, developed the RIL population, and revised the manuscript. JL helped in the data analysis and discussion. ST, JY, WZ, HL, YJ, GJ, AZ, YL, EG, MG, SL, JL, NQ, CZ, CM, HZ, GC, WZ, HW, ZQ, SL, RC, LX, SW, and JL collected the phenotype. All authors have read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Emma Mace.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhi, H., He, Q., Tang, S. et al. Genetic control and phenotypic characterization of panicle architecture and grain yield-related traits in foxtail millet (Setaria italica). Theor Appl Genet 134, 3023–3036 (2021). https://doi.org/10.1007/s00122-021-03875-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-021-03875-2