Abstract
Key message
Two major genetic loci, qTN5.1 and qAB9.1, were identified and finely mapped to the 255 Kb region with one potential candidate gene for tiller number and the 521 Kb region with eight candidate genes for axillary branch number, respectively.
Abstract
Vegetative branching including tillering and axillary branching are vital traits affecting both the plant architecture and the biomass in cereal crops. However, the mechanism underlying the formation of vegetative branching in foxtail millet is largely unknown. Here, a foxtail millet cultivar and its bushy wild relative Setaria viridis accession were used to construct segregating populations to identify candidate genes regulating tiller number and axillary branch number. Transcriptome analysis using vegetative branching bud samples of parental accessions was performed, and key differentially expressed genes and pathways regulating vegetative branching were pointed out. Bulk segregant analysis on their F2:3 segregating population was carried out, and a major QTL for tiller number (qTN5.1) and two major QTLs for axillary branch number (qAB2.1 and qAB9.1) were detected. Fine-mapping strategy was further performed on F2:4 segregate population, and Seita.5G356600 encoding β-glucosidase 11 was identified as the promising candidate gene for qTN5.1, and eight genes, especially Seita.9G125300 and Seita.9G125400 annotated as B-S glucosidase 44, were finally identified as candidate genes for regulating axillary branching. Findings in this study will help to elucidate the genetic basis of the vegetative branching formation of foxtail millet and lay a foundation for breeding foxtail millet varieties with ideal vegetative branching numbers.
Similar content being viewed by others
Data availability
The data sets supporting the results of the article are included within the article and its supplementary information files.
References
Brzobohaty B, Moore I, Kristoffersen P, Bako L, Campos N, Schell J, Palme K (1993) Release of active cytokinin by a beta-glucosidase localized to the maize root meristem. Science 262:1051–1054
Chen R, Yao Y, Fang H, Zhang E, Li P, Xu Y, Yin S, Huangfu L, Sun G, Xu C, Zhou Y, Yang Z (2019) Origin, evolution and functional characterization of the land plant glycoside hydrolase subfamily GH5_11. Mol Phylogenet Evolut 138:205–218
Choi MS, Woo MO, Koh EB, Lee J, Ham TH, Seo HS, Koh HJ (2012) Teosinte branched 1 modulates tillering in rice plants. Plant Cell Rep 31:57–65
Doebley J, Stec A, Gustus C (1995) Teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141:333–346
Doust A (2007a) Architectural evolution and its implications for domestication in grasses. Ann Bot 100:941–950
Doust A (2007b) Grass architecture: genetic and environmental control of branching. Curr Opin Plant Biol 10:21–25
Doust AN, Kellogg EA (2006) Effect of genotype and environment on branching in weedy green millet (Setaria viridis) and domesticated foxtail millet (Setaria italica) (Poaceae). Mol Ecol 15:1335–1349
Doust AN, Devos KM, Gadberry MD, Gale MD, Kellogg EA (2004) Genetic control of branching in foxtail millet. Proc Natl Acad Sci USA 101:9045–9050
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
Falk A, Rask L (1995) Expression of a zeatin-O-glucoside-degrading beta-glucosidase in Brassica napus. Plant Physiol 108:1369–1377
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 Genom 17(1):336
Gallavotti A, Zhao Q, Kyozuka J, Meeley RB, Ritter MK, Doebley JF, Pe ME, Schmidt RJ (2004) The role of barren stalk1 in the architecture of maize. Nature 432:630–635
He Q, Tang S, Zhi H, Chen J, Zhang J, Liang H, Alam O, Li H, Zhang H, Xing L, Li X, Zhang W, Wang H, Shi J, Du H, Wu H, Wang L, Yang P, Xing L, Yan H, Song Z, Liu J, Wang H, Tian X, Qiao Z, Feng G, Guo R, Zhu W, Ren Y, Hao H, Li M, Zhang A, Guo E, Yan F, Li Q, Liu Y, Tian B, Zhao X, Jia R, Feng B, Zhang J, Wei J, Lai J, Jia G, Purugganan M, Diao X (2023) A graph-based genome and pan-genome variation of the model plant Setaria. Nat Genet 55:1232–1242
Hunt HV, Przelomska NAS, Campana MG, Cockram J, Bligh HFJ, Kneale CJ, Romanova OI, Malinovskaya EV, Jones MK (2021) Population genomic structure of Eurasian and African foxtail millet landrace accessions inferred from genotyping-by-sequencing. Plant Genome 14:e20081
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
Ketudat Cairns JR, Esen A (2010) beta-Glucosidases. Cell Mol Life Sci 67:3389–3405
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 USA 100:11765–11770
Lafarge TA, Broad J, Hammer GL (2002) Tillering in grain sorghum over a wide range of population densities: identification of a common hierarchy for tiller emergence, leaf area development and fertility. Ann Bot 90:87–98
Lee KH, Piao HL, Kim HY, Choi SM, Jiang F, Hartung W, Hwang I, Kwak JM, Lee IJ, Hwang I (2006) Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126:1109–1120
Lewis JM, Mackintosh CA, Shin S, Gilding E, Kravchenko S, Baldridge G, Zeyen R, Muehlbauer GJ (2008) Overexpression of the maize Teosinte branched1 gene in wheat suppresses tiller development. Plant Cell Rep 27:1217–1225
Li X, Qian Q, Fu Z, Wang Y, Xiong G, Zeng D, Wang X, Liu X, Teng S, Hiroshi F, Yuan M, Luo D, Han B, Li J (2003) Control of tillering in rice. Nature 422:618–621
Li W, Tang S, Zhang S, Shan J, Tang C, Chen Q, Jia G, Han Y, Zhi H, Diao X (2016) Gene mapping and functional analysis of the novel leaf color gene SiYGL1 in foxtail millet [Setaria italica (L.) P. Beauv]. Physiol Plant 157:24–37
Li Z, Yun L, Ren X, Shi F, Mi F (2022) Analysis of controlling genes for tiller growth of Psathyrostachys juncea based on transcriptome sequencing technology. BMC Plant Biol 22:456
Liu T, Zhang X, Zhang H, Cheng Z, Liu J, Zhou C, Luo S, Luo W, Li S, Xing X, Chang Y, Shi C, Ren Y, Zhu S, Lei C, Guo X, Wang J, Zhao Z, Wang H, Zhai H, Lin Q, Wan J (2022a) Dwarf and High Tillering1 represses rice tillering through mediating the splicing of D14 pre-mRNA. Plant Cell 34:3301–3318
Liu T, Liu X, He J, Dong K, Pan W, Zhang L, Ren R, Zhang Z, Yang T (2022b) Identification and fine-mapping of a major QTL (PH1.1) conferring plant height in broomcorn millet (Panicum miliaceum). Front Plant Sci 13:1010057
Mae T (1997) Physiological nitrogen efficiency in rice: nitrogen utilization, photosynthesis, and yield potential. Plant Soil 196:201–210
Mauro-Herrera M, Doust AN (2016) Development and genetic control of plant architecture and biomass in the panicoid grass Setaria. PLoS ONE 11(3):e0151346
McSteen P (2009) Hormonal regulation of branching in grasses. Plant Physiol 149:46–55
Nadeem F, Ahmad Z, Ul Hassan M, Wang R, Diao X, Li X (2020) Adaptation of foxtail millet (Setaria italica L.) to abiotic stresses: a special perspective of responses to nitrogen and phosphate limitations. Front Plant Sci 11:187
Poncet V, Lamy F, Devos KM, Gale MD, Sarr A, Robert T (2000) Genetic control of domestication traits in pearl millet (Pennisetum glaucum L., Poaceae). Theor Appl Genet 100:147–159
Ramsay L, Comadran J, Druka A, Marshall DF, Thomas WT, Macaulay M, MacKenzie K, Simpson C, Fuller J, Bonar N, Hayes PM, Lundqvist U, Franckowiak JD, Close TJ, Muehlbauer GJ, Waugh R (2011) INTERMEDIUM-C, a modifier of lateral spikelet fertility in barley, is an ortholog of the maize domestication gene TEOSINTE BRANCHED 1. Nat Genet 43:169–172
Remigereau MS, Lakis G, Rekima S, Leveugle M, Fontaine MC, Langin T, Sarr A, Robert T (2011) Cereal domestication and evolution of branching: evidence for soft selection in the Tb1 orthologue of pearl millet (Pennisetum glaucum [L.] R. Br.). PLoS ONE 6:e22404
Ren RJ, Wang P, Wang LN, Su JP, Sun LJ, Sun Y, Chen DF, Chen XW (2020) Os4BGlu14, a monolignol beta-Glucosidase, negatively affects seed longevity by influencing primary metabolism in rice. Plant Mol Biol 104:513–527
Schliemann W (1984) Hydrolysis of conjugated gibberellins by beta-Glucosidases from dwarf rice (Oryza sativa L. cv. <<Tan-ginbozu>>). J Plant Physiol 116:123–132
Shang Q, Wang Y, Tang H, Sui N, Zhang X, Wang F (2021) Genetic, hormonal, and environmental control of tillering in wheat. Crop J 9:986–991
Wang Y, Wang X, Sun S, Jin C, Su J, Wei J, Luo X, Wen J, Wei T, Sahu SK, Zou H, Chen H, Mu Z, Zhang G, Liu X, Xu X, Gram L, Yang H, Wang E, Liu H (2022) GWAS, MWAS and mGWAS provide insights into precision agriculture based on genotype-dependent microbial effects in foxtail millet. Nat Commun 13(1):5913
Wang W, Wang Y (2021) Crop plant architecture and grain yields. Sci Sin Vitae 51:1366–1375
Xu C, Wang Y, Yu Y, Duan J, Liao Z, Xiong G, Meng X, Liu G, Qian Q, Li J (2012) Degradation of MONOCULM 1 by APC/C(TAD1) regulates rice tillering. Nat Commun 3:750
Zhang Z, Sun X, Ma X, Xu B, Zhao Y, Ma Z, Li G, Khan NU, Pan Y, Liang Y, Zhang H, Li J, Li Z (2021) GNP6, a novel allele of MOC1, regulates panicle and tiller development in rice. Crop J 9:57–67
Zhu M, He Q, Lyu M, Shi T, Gao Q, Zhi H, Wang H, Jia G, Tang S, Cheng X, Wang R, Xu A, Wang H, Qiao Z, Liu J, Diao X, Gao Y (2023) Integrated genomic and transcriptomic analysis reveals genes associated with plant height of foxtail millet. Crop J 11:593–604
Funding
This study was financially supported by the China Agriculture Research System (CARS-06-14.5-A8); Natural Science Foundation of China (31960419), Special Project of Agricultural Science and Technology innovation of GAAS (2021GAAS02); Top-notch talent project in Gansu Province (2022); Doctoral Fund of Gansu Academy of Agricultural Sciences(2023GAAS26).
Author information
Authors and Affiliations
Contributions
TL contributed to the conceptualization, methodology, software, validation, formal analysis, investigation, data curation, writing—original draft, visualization and funding acquisition. XL assisted in the data curation, writing—original draft and visualization. JH, LZ, YL and RY were involved in the investigation, resources and data curation. KJ contributed to the resources, investigation, data curation and funding acquisition. TY assisted in the writing—review and editing, supervision, project administration and funding acquisition. All authors have read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts 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
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Liu, T., Liu, X., He, J. et al. Comparative transcriptome analysis and genetic dissection of vegetative branching traits in foxtail millet (Setaria italica). Theor Appl Genet 137, 39 (2024). https://doi.org/10.1007/s00122-023-04524-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00122-023-04524-6