Abstract
Suitable flowering time can improve fiber yield and quality, which is of great significance for jute biological breeding. In this study, 242 jute accessions were planted in Fujian for 2 consecutive years, and 244,593 SNPs distributed in jute genome were used for genome-wide association analysis of flowering time. A total of 19 candidate intervals (P < 0.0001) were identified by using GLM and FaST-LMM and were significantly associated with flowering time, with phenotypic variation explained (PVE) ranging from 5.8 to 18.61%. Six stable intervals that were repeatedly detected in different environments were further identified by the linkage disequilibrium heatmap. The most likely 7 candidate genes involved to flowering time were further predicted according to the gene functional annotations. Notably, functional analysis of the candidate gene CcPRR7 of the major loci qFT-3–1, a key factor in circadian rhythm in the photoperiodic pathway, was evaluated by linkage, haplotype, and transgenic analysis. β-glucuronidase (GUS) and luciferase (LUC) activity assay of the promoters with two specific haplotypes confirmed that the flowering time can be controlled by regulating the expression of CcPRR7. The model of CcPRR7 involved in the photoperiod regulation pathway under different photoperiods was proposed. These findings provide insights into genetic loci and genes for molecular marker-assisted selection in jute and valuable information for genetically engineering PRR7 homologs in plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The genotype data of this study can be obtained from the National Genomics Data Center of China (PRJCA005722).
References
Cheng X, Wang Z (2005) Overexpression of COL9, a CONSTANS-LIKE gene, delays flowering by reducing expression of CO and FT in Arabidopsis thaliana: overexpression of COL9 delays flowering. Plant J 43:758–768. https://doi.org/10.1111/j.1365-313x.2005.02491.x
Cho LH, Yoon J, An G (2017) The control of flowering time by environmental factors. Plant J 90:708–719. https://doi.org/10.1111/tpj.13461
Choudhary SB, Saha D, Sharma HK, Chowdhury I, Kumar AA, Jambhulkar SK, Mitra J (2019) Transcriptional analysis of a delayed-flowering mutant under short-day conditions reveal genes related to photoperiodic response in tossa jute (Corchorus olitorius L.). Ind Crops Prod 132:476–486. https://doi.org/10.1016/j.indcrop.2019.03.001
Clough S, Bent A (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. https://doi.org/10.1046/j.1365-313x.1998.00343.x
Corbesier L, Vincent C, Jang S, Fornara F, Fan QZ, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033. https://doi.org/10.1126/science.1141752
Devlin PF (2002) Signs of the time: environmental input to the circadian clock. J Exp Bot 53:1535–1550. https://doi.org/10.1093/jxb/erf024
Fornara F, Panigrahi KCS, Gissot L, Sauerbrunn N, Rühl M, Jarillo JA, Coupland G (2009) Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev Cell 17:75–86. https://doi.org/10.1016/j.devcel.2009.06.015
Hans H, Silke L, Andreas K, Gerald K, Fadia E, Denise L, Bo Z, Ingo B, Jürgen O, Siegbert M, Jörg F, Matthias F (2012) Influence of over-expression of the Flowering Promoting Factor 1 gene (FPF1) from Arabidopsis on wood formation in hybrid poplar (Populus tremula L. × P. tremuloides Michx.). Planta 235:359–373. https://doi.org/10.1007/s00425-011-1507-8
Huang X, Zhao Y, Wei X, Li C, Wang A, Zhao Q, Li W, Guo Y, Deng L, Zhu C, Fan D, Lu Y, Weng Q, Liu K, Zhou T, Jing Y, Si L, Dong G, Huang T, Lu T, Feng Q, Qian Q, Li J, Han B (2011) Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet 44:32–39. https://doi.org/10.1038/ng.1018
Imaizumi T, Schultz TF, Harmon FG, Ho LA, Kay SA (2005) FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309:293–297. https://doi.org/10.1126/science.1110586
Johansen C, Waseque M, Begum S (1985) Effect and interaction of photoperiod, temperature, water stress and nitrogen on flowering and growth in jute. Field Crops Res 12:397–406. https://doi.org/10.1016/0378-4290(85)90084-X
Li M, Liu Y, Tao Y, Xu C, Li X, Zhang X, Han Y, Yang X, Sun J, Li W, Li D, Zhao X, Zhao L (2019) Identification of genetic loci and candidate genes related to soybean flowering through genome wide association study. BMC Genom 20:987–1000. https://doi.org/10.1186/s12864-019-6324-7
Lippert C, Listgarten J, Liu Y, Kadie CM, Davidson RI, Heckerman D (2011) FaST linear mixed models for genome-wide association studies. Nat Methods 8:833–838. https://doi.org/10.1038/nmeth.1681
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Mawphlang OIL, Kharshiing EV (2017) Photoreceptor mediated plant growth responses: implications for photoreceptor engineering toward improved performance in crops. Front Plant Sci 8:1181–1195. https://doi.org/10.3389/fpls.2017.01181
Nakamichi N, Kita M, Ito S, Yamashino T, Mizuno T (2005) PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana. Plant Cell Physiol 46:686–698. https://doi.org/10.1093/pcp/pci086
Nakamichi N, Kiba T, Henriques R, Mizuno T, Chua NH, Sakakibara H (2010) PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell 22:594–605. https://doi.org/10.1105/tpc.109.072892
Raman H, Raman R, Qiu Y, Yadav A, Sureshkumar S, Borg L, Rohan M, Wheeler D, Owen O, Menz I, Balasubramanian S (2019) GWAS hints at pleiotropic roles for FLOWERING LOCUS T in flowering time and yield-related traits in canola. BMC Genom 20:636. https://doi.org/10.1186/s12864-019-5964-y
Schomburg FM, Patton DA, Meinke DW, Amasino RM (2001) FPA, a gene involved in floral induction in arabidopsis, encodes a protein containing RNA-recognition motifs. Plant Cell 13:1427–1436. https://doi.org/10.1105/tpc.13.6.1427
Shi J, Wang Y, Wang C, Wang L, Zeng W, Han G, Qiu C, Wang T, Tao Z, Wang K, Huang S, Yu S, Wang W, Chen H, Chen C, He C, Wang H, Zhu P, Hu Y, Zhang X, Xie C, Lu X, Li P (2022) Linkage mapping combined with GWAS revealed the genetic structural relationship and candidate genes of maize flowering time-related traits. BMC Plant Biol 22:328. https://doi.org/10.1186/s12870-022-03711-9
Soto-Cerda BJ, Aravena G, Cloutier S (2021) Genetic dissection of flowering time in flax (Linum usitatissimum L.) through single- and multi-locus genome-wide association studies. Mol Genet Genomics 296:877–891. https://doi.org/10.1007/s00438-021-01785-y
Srikanth A, Schmid M (2011) Regulation of flowering time: all roads lead to Rome. Cell Mol Life Sci 68:2013–2037. https://doi.org/10.1007/s00018-011-0673-y
Steinbach Y (2019) The Arabidopsis thaliana CONSTANS-LIKE 4 (COL4)–a modulator of flowering time. Front Plant Sci 10:651. https://doi.org/10.3389/fpls.2019.00651
Wang Y, Tao Z, Wang W, Filiault D, Qiu C, Wang C, Wang H, Rehman S, Shi J, Zhang Y, Li P (2020a) Molecular variation in a functionally divergent homolog of FCA regulates flowering time in Arabidopsis thaliana. Nat Commun 17:5830. https://doi.org/10.1038/s41467-020-19666-0
Wang L, Sun S, Wu T, Liu L, Sun X, Cai Y, Li J, Jia H, Yuan S, Chen L, Jiang B, Wu C, Hou W, Han T (2020b) Natural variation and CRISPR/Cas9-mediated mutation in GmPRR37 affect photoperiodic flowering and contribute to regional adaptation of soybean. Plant Biotechnol J 18:1869–1881. https://doi.org/10.1111/pbi.13346
Wang H, Yang Y, Zhang Y, Zhao T, Jiang J, Li J, Xu X, Yang H (2021) Transcriptome analysis of flower development and mining of genes related to flowering time in tomato (Solanum lycopersicum). Int J Mol Sci 22:8128. https://doi.org/10.3390/ijms22158128
Yang J, Lee SH, Goddard ME, Visscher PM (2011) GCTA: a tool for genome-wide complex trait analysis. Am J Hum Genet 88:76–82. https://doi.org/10.1016/j.ajhg.2010.11.011
Yin LL, Zhang HH, Tang ZS, Xu JY, Yin D, Zhang ZW, Yuan XH, Zhu MJ, Zhao SH, Li XY, Liu XL (2021a) rMVP: a memory-efficient, visualization-enhanced, and parallel-accelerated tool for genome-wide association study. Genom Proteom Bioinf 19:619–628. https://doi.org/10.1016/j.gpb.2020.10.007
Yin M, Ma H, Wang M, Chu G, Liu Y, Xu C, Zhang X, Wang D, Chen S (2021) Transcriptome analysis of flowering regulation by sowing date in Japonica rice (Oryza sativa L.). Sci Rep 11:15026. https://doi.org/10.1038/s41598-021-94552-3
Zhang C, Dong SS, Xu JY, He WM, Yang TL (2019) PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics 35:1786–1788. https://doi.org/10.1093/bioinformatics/bty875
Zhang L, Ma X, Zhang X, Xu Y, Ibrahim AK, Yao J, Huang H, Chen S, Liao Z, Zhang Q, Niyitanga S, Yu J, Liu Y, Xu X, Wang J, Tao A, Xu J, Chen S, Yang X, He Q, Lin L, Fang P, Zhang L, Ming R, Qi J, Zhang L (2021) Reference genomes of the two cultivated jute species. Plant Biotechnol J 19:2235–2248. https://doi.org/10.1111/pbi.13652
Zhao C, Hanada A, Yamaguchi S, Kamiya Y, Beers EP (2011) The Arabidopsis Myb genes MYR1 and MYR2 are redundant negative regulators of flowering time under decreased light intensity. Plant J 66:502–515. https://doi.org/10.1111/j.1365-313X.2011.04508.x
Acknowledgements
We are grateful for the support of the platforms of the Key Laboratory of the Ministry of Agriculture and Rural Affairs for Biological Breeding of Fujian and Taiwan Crops, Fujian Public Platform for Germplasm Resources of Bast Fiber Crops, and Fujian International Science and Technology Cooperation Base for Genetic Breeding and Multiple Utilization Development of Southern Economic Crops.
Funding
This research was supported by the National Natural Science Foundation of China (31972968, 31771369) and the China Agriculture Research System of MOF and MARA (CARS-16).
Author information
Authors and Affiliations
Contributions
JY: conceptualization, data curation, formal analysis, writing—original draft. HL: data curation. SJ, ZQ, AT, PF, JX, LL, JQ: methodology, materials. LZ: supervision the work, funding acquisition, writing—review and editing.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
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
Yao, J., Jiang, S., Li, H. et al. Genome-wide association study reveals loci and candidate genes of flowering time in jute (Corchorus L.). Mol Breeding 43, 85 (2023). https://doi.org/10.1007/s11032-023-01435-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-023-01435-8