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GmAOC4 modulates seed germination by regulating JA biosynthesis in soybean

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Abstract

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An allene oxide cyclase 4, GmAOC4 , was determined by GWAS and RT-PCR to be significantly associated with seed germination in soybean, and regulates seed germination by promoting more JA accumulation.

Abstract

The seed germination phase is a critical component of the plant lifecycle, and a better understanding of the mechanism behind seed germination in soybeans is needed. We used a genome-wide association study (GWAS) to detect a GWAS signal on chromosome 18. In this GWAS signal, SNP S18_56189166 was located within the 3’untranslated region of Glyma.18G280900, which encodes allene oxide cyclase 4 (named GmAOC4). Analysis of real-time PCR demonstrated that expression levels of GmAOC4 in the low-germination variety (KF, carrying SNP S18_56189166-T) were higher than in the high-germination variety (NN, carrying SNP S18_56189166-C). In these two varieties, KF showed a higher JA concentration than NN at 0 and 24 h after imbibition. Moreover, the overexpression of GmAOC4 led to an increase in the concentration of jasmonic acid (JA) in soybean hairy roots and Arabidopsis thaliana. Furthermore, it was found that GmAOC4-OE lines showed less seed germination than the wild type (WT) under normal conditions in Arabidopsis. After 7 days of ABA treatment, transgenic lines exhibited lower seed germination and higher expression levels of AtABI5 compared with WT, indicating that the overexpression of GmAOC4 resulted in hypersensitivity to ABA. Our findings demonstrate that GmAOC4, which promotes more JA accumulation, helps to regulate seed germination in soybeans.

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References

  • Al-Chaarani GR, Gentzbittel L, Wedzony M, Sarrafi A (2005) Identification of QTLs for germination and seedling development in sunflower (Helianthus annuus L.). Plant Sci 169:221–227

    Article  CAS  Google Scholar 

  • Bernard RL, Cremeens CR (1988) Registration of Williams 82 soybean. Crop Sci 28:1027–1028

    Google Scholar 

  • Börner A, Nagel M, Agacka-Mołdoch M, Gierke PU, Oberforster M, Albrecht T, Mohler V (2018) QTL analysis of falling number and seed longevity in wheat (Triticum aestivum L.). J Appl Genet 59:35–42

    Article  Google Scholar 

  • Caverzan A, Giacomin R, Müller M, Biazus C, Lângaro NC, Chavarria G (2018) How does seed vigor affect soybean yield components? Agron J 110:1318–1327

    Article  CAS  Google Scholar 

  • Claus W, Susheng S (2017) Jasmonates: biosynthesis, metabolism, and signaling by proteins activating and repressing transcription. J Exp Bot 68:1303–1321

    Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium -mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  Google Scholar 

  • Dave A, Hernández ML, He Z, Andriotis VME, Vaistij FE, Larson TR, Graham IA (2011) 12-Oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis. Plant Cell 23:583–599

    Article  CAS  Google Scholar 

  • Du M, Zhao J, Tzeng DTW, Liu Y, Deng L, Yang T, Zhai Q, Wu F, Huang Z, Zhou M, Wang Q, Chen Q, Zhong S, Li C, Li C (2017) MYC2 orchestrates a hierarchical transcriptional cascade that regulates jasmonate-mediated plant immunity in tomato. Plant Cell 29:1883–1906

    Article  CAS  Google Scholar 

  • Han Z, Ku L, Zhang Z, Zhang J, Guo S, Liu H, Zhao R, Ren Z, Zhang L, Su H, Dong L, Chen Y (2014) QTLs for seed vigor-related traits identified in maize seeds germinated under artificial aging conditions. PLoS One 9:e92535

    Article  Google Scholar 

  • Hang NT, Lin Q, Liu L, Liu X, Liu S, Wang W, Li L, He N, Liu Z, Jiang L, Wan J (2015) Mapping QTLs related to rice seed storability under natural and artificial aging storage conditions. Euphytica 203:673–681

    Article  CAS  Google Scholar 

  • Hatzig SV, Frisch M, Breuer F, Nesi N, Ducournau S, Wagner M, Leckband G, Abbadi A, Snowdon RJ (2015) Genome-wide association mapping unravels the genetic control of seed germination and vigor in Brassica napus. Front Plant Sci 6:221

    Article  Google Scholar 

  • Hazman M, Hause B, Eiche E, Nick P, Riemann M (2015) Increased tolerance to salt stress in OPDA-deficient rice ALLENE OXIDE CYCLASE mutants is linked to an increased ROS-scavenging activity. J Exp Bot 66:3339–3352

    Article  CAS  Google Scholar 

  • He Y, Zhao J, Yang B, Sun S, Peng L, Wang Z (2020) Indole-3-acetate beta-glucosyltransferase OsIAGLU regulates seed vigor through mediating crosstalk between auxin and abscisic acid in rice. Plant Biotechnol J 18:1933–1945

    Article  CAS  Google Scholar 

  • Jin D, Wu M, Li B, Bücker B, Keil P, Zhang S, Li J, Kang D, Liu J, Dong J, Deng XW, Irish V, Wei N (2018) The COP9 Signalosome regulates seed germination by facilitating protein degradation of RGL2 and ABI5. PLoS Genet 14:e1007237

    Article  Google Scholar 

  • Ju L, Jing Y, Shi P, Liu J, Chen J, Yan J, Chu J, Chen KM, Sun J (2019) JAZ proteins modulate seed germination through interaction with ABI 5 in bread wheat and Arabidopsis. New Phytol 223:246–260

    Article  CAS  Google Scholar 

  • Kereszt A, Li D, Indrasumunar A, Nguyen CD, Nontachaiyapoom S, Kinkema M, Gresshoff PM (2007) Agrobacterium rhizogenes-mediated transformation of soybean to study root biology. Nat Protoc 2:948–952

    Article  CAS  Google Scholar 

  • Lekklar C, Pongpanich M, Suriya-arunroj D, Chinpongpanich A, Tsai H, Comai L, Chadchawan S, Buaboocha T (2019) Genome-wide association study for salinity tolerance at the flowering stage in a panel of rice accessions from Thailand. BMC Genom 20:76

    Article  Google Scholar 

  • Li Y, Wang C, Liu X, Song J, Li H, Sui Z, Zhang M, Fang S, Chu J, Xin M, Xie C, Zhang Y, Sun Q, Ni Z (2016) Up-regulating the abscisic acid inactivation gene ZmABA8ox1b contributes to seed germination heterosis by promoting cell expansion. J Exp Bot 67:2889–2900

    Article  CAS  Google Scholar 

  • Lipka AE, Tian F, Wang Q, Peiffer J, Li M, Bradbury PJ, Gore MA, Buckler ES, Zhang Z (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics 28:2397–2399

    Article  CAS  Google Scholar 

  • Liu F, Jiang Y, Zhao Y, Schulthess AW, Reif JC (2020) Haplotype-based genome-wide association increases the predictability of leaf rust (Puccinia triticina) resistance in wheat. J EXP BOT 71:6958–6968

    Article  CAS  Google Scholar 

  • Mayr C (2017) Regulation by 3′-untranslated regions. Annu Rev Genet 51:171–194

    Article  CAS  Google Scholar 

  • Pan J, Hu Y, Wang H, Guo Q, Chen Y, Howe GA, Yu D (2020) Molecular Mechanism underlying the synergetic effect of jasmonate on abscisic acid signaling during seed germination in Arabidopsis. Plant Cell 32:3846–3865

    Article  CAS  Google Scholar 

  • Pang Y, Liu C, Wang D, St. Amand P, Bernardo A, Li W, He F, Li L, Wang L, Yuan X, Dong L, Su Y, Zhang H, Zhao M, Liang Y, Jia H, Shen X, Lu Y, Jiang H, Wu Y, Li A, Wang H, Kong L, Bai G, and Liu S (2020) High-resolution genome-wide association study identifies genomic regions and candidate genes for important agronomic traits in wheat. Mol Plant 13, 1311–1327.

  • Perry DA (1978) Problems of the development and application of vigour tests to vegetable seeds. Acta Hort 83:141–146

    Article  Google Scholar 

  • Qi T, Huang H, Song S, Xie D (2015) Regulation of jasmonate-mediated stamen development and seed production by a bHLH-MYB complex in Arabidopsis. Plant Cell 27:1620

    Article  CAS  Google Scholar 

  • Rajjou LC, Duval M, Gallardo K, Catusse J, Bally J, Job C, Job D (2012) Seed germination and vigor. Annu Rev Plant Biol 63:507–533

    Article  CAS  Google Scholar 

  • Shelar VR, Shaikh RS, Nikam AS (2008) Soybean seed quality during storage: a review. Agric Rev 29(2):125–131

    Google Scholar 

  • Song J, Shang L, Wang X, Xing Y, Xu W, Zhang Y, Wang T, Li H, Zhang J, Ye Z (2020) MAPK11 regulates seed germination and ABA signaling in tomato by phosphorylating SnRKs. J Exp Bot 27:1677–1690

    Google Scholar 

  • Wang Y, Hou Y, Qiu J, Wang H, Wang S, Tang L, Tong X, Zhang J (2020) Abscisic acid promotes jasmonic acid biosynthesis via a ‘SAPK10-bZIP72-AOC’ pathway to synergistically inhibit seed germination in rice (Oryza sativa). New Phytol 228:1336–1353

    Article  CAS  Google Scholar 

  • Wasternack C, Hause B (2013) jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in annals of botany. Ann Bot 111:1021–1058

    Article  CAS  Google Scholar 

  • Xie L, Tan Z, Zhou Y, Xu R, Feng L, Xing Y, Qi X (2014) Identification and fine mapping of quantitative trait loci for seed vigor in germination and seedling establishment in rice. J Integr Plant Biol 56:749–759

    Article  CAS  Google Scholar 

  • Zhang X, Hina A, Song S, Kong J, Bhat JA, Zhao T (2019a) Whole-genome mapping identified novel “QTL hotspots regions” for seed storability in soybean (Glycine max L.). BMC Genom 20:499

    Article  Google Scholar 

  • Zhang W, Liao X, Cui Y, Ma W, Zhang X, Du H, Ma Y, Ning L, Wang H, Huang F, Yang H, Kan G, Yu D (2019b) A cation diffusion facilitator, GmCDF1, negatively regulates salt tolerance in soybean. PLoS Genet 15:e1007798

    Article  Google Scholar 

  • Zhang W, Xu W, Zhang H, Liu X, Cui X, Li S, Song L, Zhu Y, Chen X, Chen H (2021) Comparative selective signature analysis and high-resolution GWAS reveal a new candidate gene controlling seed weight in soybean. Theor Appl Genet 134:1329–1341

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Key R&D project of Jiangsu Province (BE2019376), the Natural Science Foundation of Jiangsu Province (BK20210154), the National Key Research and Development Program of China (2018YFE0112200), and Jiangsu Agriculture Science and Technology Innovation Fund[CX(20)2007].

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ZW, WX, HZ, and SL were all involved in the experimental design and the collection of phenotypic data; ZW and XC conducted the phenotypic analysis; WX, LS, XL, YZ, and CX helped revise the manuscript; ZW assessed the experimental results; ZW and HT wrote the paper. The manuscript was reviewed by all authors, who each contributed suggestions.

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Correspondence to Xin Chen or Huatao Chen.

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The authors declare that they have no conflict of interest.

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Communicated by Istvan Rajcan.

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Zhang, W., Xu, W., Li, S. et al. GmAOC4 modulates seed germination by regulating JA biosynthesis in soybean. Theor Appl Genet 135, 439–447 (2022). https://doi.org/10.1007/s00122-021-03974-0

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