Skip to main content
SpringerLink
Log in

Genome-wide transcriptome profiling reveals the mechanism of the effects of uniconazole on root development in Glycine Max

  • Original Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Uniconazole, a plant growth retardant, possesses the ability to improve quality and increase tolerance of plant. However, it is known little about the effects of uniconazole on root. In this study, uniconazole treatments that were applied through seed soaking, promoted soybean root development, and the microstructure of root showed increase of cortical thickness and cortex cell width. Meanwhile, the endogenous hormone content also altered in root after uniconazole treatments. To obtain the molecular mechanism underlying the effects of uniconazole on root, we performed an RNAseq of roots harvested 3 days after uniconazole treatment. Through analyses of phytohormone-associated genes for endogenous hormones changes, we found that not only GA biosynthesis pathway but also the regulation genes of the pathway were affected. Above all, the dominant pathway plant hormone signal transduction may be the main factor of the cambium proliferation, in especial ethylene/ERF signaling pathway. Moreover, the transcriptome demonstrated differentially expressed genes that determined cell division and cell wall modification may be regulators of root growth. CLE signaling and receptor-like kinases may play a crucial role in the root elongation. Besides, 177 transcription factors (TFs) were involved in response to uniconazole. Taken together, all these findings provide insights into the complex molecular mechanisms associated with root development after uniconazole treatment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P (2008) The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20:2117–2129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bahieldin A, Atef A, Edris S, Gadalla NO, Ali HM, Hassan SM, Al-Kordy MA, Ramadan AM, Makki RM, Al-Hajar AS, El-Domyati FM (2016) Ethylene responsive transcription factor ERF109 retards PCD and improves salt tolerance in plant. BMC Plant Biol 16:216

    Article  PubMed  PubMed Central  Google Scholar 

  • Bassa C, Etemadi M, Combier JP, Bouzayen M, Audran-Delalande C (2013) Sl-IAA27 gene expression is induced during arbuscular mycorrhizal symbiosis in tomato and in Medicago truncatula. Plant Signal Behav 8:e25637–1-3

  • Bassa C, Mila I, Bouzayen M, Audran-Delalande C (2012) Phenotypes associated with down-regulation of Sl-IAA27 support functional diversity among Aux/IAA family members in tomato. Plant Cell Physiol 53:1583–1595

    Article  CAS  PubMed  Google Scholar 

  • Cai XT, Xu P, Zhao PX, Liu R, Yu LH, Xiang CB (2014) Arabidopsis ERF109 mediates cross-talk between jasmonic acid and auxin biosynthesis during lateral root formation. Nat Commun 5:5833.

    Article  CAS  PubMed  Google Scholar 

  • Chandler JW (2016) Auxin response factors. Plant Cell Environ 39:1014–1028

    Article  CAS  PubMed  Google Scholar 

  • Cheng C, Jiao C, Singer SD, Gao M, Xu X, Zhou Y, Li Z, Fei Z, Wang Y, Wang X (2015) Gibberellin-induced changes in the transcriptome of grapevine (Vitislabrusca × V. vinifera) cv. Kyoho flowers. BMC Genomics 16:128

    Article  PubMed  PubMed Central  Google Scholar 

  • Chung HS, Howe GA (2009) A critical role for the TIFY motif in repression of jasmonate signaling by a stabilized splice variant of the JASMONATE ZIM-domain protein JAZ10 in Arabidopsis. Plant Cell 21:131–145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Etchells JP, Provost CM, Turner SR (2012) Plant vascular cell division is maintained by an interaction between PXY and ethylene signalling. PLoS Genet 8:e1002997

    Article  PubMed  PubMed Central  Google Scholar 

  • Fabian T, Lorbiecke R, Umeda M, Sauter M (2000) The cell cycle genes cycA1;1 and cdc2Os-3 are coordinately regulated by gibberellin in planta. Planta 211:376–383

    Article  CAS  PubMed  Google Scholar 

  • Fletcher R, Arnold V (1986) Stimulation of cytokinins and chlorophyll synthesis in cucumber cotyledons by triadimefon. Physiol Plant 66:197–201

    Article  CAS  Google Scholar 

  • Fletcher R, Hofstra G (1990) Improvement of uniconazole-induced protection in wheat seedlings. J Plant Growth Regul 9:207–212

    Article  CAS  Google Scholar 

  • Florea L, Song L, Salzberg SL (2013) Thousands of exon skipping events differentiate among splicing patterns in sixteen human tissues. F1000 Research 2:188

    PubMed  PubMed Central  Google Scholar 

  • Ge Y, Li Y, Zhu Y M, Bai X, Lv D K, Guo D, Ji W, Cai H (2010) Global transcriptome profiling of wild soybean (Glycine soja) roots under NaHCO3 treatment. BMC Plant Biol 10:153

    Article  PubMed  PubMed Central  Google Scholar 

  • 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(Database issue):D1178–1186

    Article  CAS  PubMed  Google Scholar 

  • Goossens J, Mertens J, Goossens A (2016) Role and functioning of bHLH transcription factors in jasmonate signalling. J Exp Bot erw440

    Google Scholar 

  • Gou J, Strauss SH, Tsai CJ, Fang K, Chen Y, Jiang X, Busov VB (2010) Gibberellins regulate lateral root formation in Populus through interactions with auxin and other hormones. Plant Cell 22:623–639

    Article  CAS  PubMed  Google Scholar 

  • Ha CV, Watanabe Y, Tran UT, Le DT, Tanaka M, Nguyen KH, Seki M, Nguyen DV, Tran LS (2015) Comparative analysis of root transcriptomes from two contrasting drought-responsive Williams 82 and DT2008 soybean cultivars under normal and dehydration conditions. Front Plant Sci 6:551

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang M, Fang Y, Liu Y, Jin Y, Sun J, Tao X, Ma X, He K, Zhao H (2015) Using proteomic analysis to investigate uniconazoleinduced phytohormone variation and starch accumulation in duckweed (Landoltia punctata). BMC Biotechnol 15:81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inada S, Shimmen T (2001) Involvement of cortical microtubules in plastic extension regulated by gibberellin in Lemna minor root. Plant Cell Physiol 42:395–403

    Article  CAS  PubMed  Google Scholar 

  • Izumi K, Kamiya Y, Sakurai A, Oshio H, and Takahashi N (1985) Studies of sites of action of a new plant growth retardant (E)-1-(4-chlorophenyl)-4, 4-dimethyl-2-(1, 2, 4-trizol-1-yl)-penten-3- ol (S-3307) and comparative effects of its stereisomers in a cell free system of Cucurbits maxima. Plant Cell Physiol 29:821–827

    Google Scholar 

  • Izumi K, Nakagawa S, Kobayashi M, Oshio H, Sakurai A, Takahashi N (1988) Levels of IAA, cytokinins, ABA and ethylene in rice plants as affected by a gibberellins biosynthesis inhibitor Uniconazole P. Plant Cell Physiol 29:97–104

    CAS  Google Scholar 

  • Ji J, Strable J, Shimizu R, Koenig D, Sinha N, Scanlon MJ (2010) WOX4 promotes procambial development. Plant Physiol 152(3):1346–1356

    Article  CAS  PubMed  Google Scholar 

  • Jin J, He K, Tang X, Li Z, Lv L, Zhao Y, Luo J, Gao G (2015) An Arabidopsis transcriptional regulatory map reveals distinct functional and evolutionary features of novel transcription factors. Mol Biol Evol 32:1767–1773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin P, Zhang H, Kong L, Gao G, Luo JC (2014) Plant TFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res 42:D1182–D1187

    Article  CAS  PubMed  Google Scholar 

  • Jung JKH, McCouch S (2013) Getting to the roots of it: Genetic and hormonal control of root architecture. Front Plant Sci 4:186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khandelwal A, Elvitigala T, Ghosh B, Quatrano RS (2008) Arabidopsis transcriptome reveals control circuits regulating redox homeostasis and the role of an AP2 transcription factor. Plant Physiol 148:2050–2058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36

    Article  PubMed  PubMed Central  Google Scholar 

  • Koizumi K, Gallagher KL (2013) Identification of SHRUBBY, a SHORT-ROOT and SCARECROW interacting protein that controls root growth and radial patterning. Development 140:1292–300

    Article  CAS  PubMed  Google Scholar 

  • Kutschera U (1990) Cell-wall synthesis and elongation growth in hypocotyls of Helianthus annuus L. Planta 181:316–323

    Article  CAS  PubMed  Google Scholar 

  • Lee Y, Choi D, Kende H (2001) Expansins: ever-expanding numbers and functions. Curr Opin Plant Biol 4:527–532

    Article  CAS  PubMed  Google Scholar 

  • Leul M, Zhou W (1998) Alleviation of waterlogging damage in winter rape by application of uniconazole: Effects on morphological characteristics, hormones and photosynthesis. Field Crops Res 59:121–127

    Article  Google Scholar 

  • Leul M, Zhou WJ (1999) Alleviation of waterlogging damage in winter rape by uniconazole application: Effects on enzyme activity, lipid peroxidation, and membrane integrity. J Plant Growth Regul 18:9–14

    Article  CAS  PubMed  Google Scholar 

  • Li H P. Botanical microtechnique. Science press, Beijing, 2009, 49

    Google Scholar 

  • Liu Y, Fang Y, Huang M, Jin Y, Sun J, Tao X, Zhang G, He K, Zhao Y, Zhao H (2015a) Uniconazole-induced starch accumulation in the bioenergy crop duckweed (Landoltia punctata) I: Transcriptome analysis of the effects of uniconazole on chlorophyll and endogenous hormone biosynthesis. Biotechnol Biofuels 8:57

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Fang Y, Huang M, Jin Y, Sun J, Tao X, Zhang G, He K, Zhao Y, Zhao H (2015b) Uniconazole-induced starch accumulation in the bioenergy crop duckweed (Landoltiapunctata) II: Transcriptome alterations of pathways involved in carbohydrate metabolism and endogenous hormone crosstalk. Biotechnol Biofuels 8:1–12

    Article  Google Scholar 

  • Lorenzo O, Piqueras R, Sánchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15:165–178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacMillan CP, Mansfield SD, Stachurski ZH, Evans R, Southerton SG (2010) Fasciclin-like arabinogalactan proteins: specialization for stem biomechanics and cell wall architecture in Arabidopsis and Eucalyptus. Plant J 62:689–703

    Article  CAS  PubMed  Google Scholar 

  • Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K (2008) The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivating gene, GA2ox7, under high-salinity stress in Arabidopsis. Plant J 56:613–626

    Article  CAS  PubMed  Google Scholar 

  • Mehterov N, Balazadeh S, Hille J, Toneva V, Mueller-Roeber B, Gechev T (2012) Oxidative stress provokes distinct transcriptional responses in the stress-tolerant atr7 and stress-sensitive loh2 Arabidopsis thaliana mutants as revealed by multi-parallel quantitative realtime PCR analysis of ROS marker and antioxidant genes. Plant Physiol Biochem 59:20–29

    Article  CAS  PubMed  Google Scholar 

  • Meng L, Feldman LJ (2010) CLE14/CLE20 peptides may interact with CLAVATA2/CORYNE receptor-like kinases to irreversibly inhibit cell division in the root meristem of Arabidopsis. Planta 232:1061–1074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Merchante C, Alonso JM, Stepanova AN (2013) Ethylene signaling: Simple ligand, complex regulation. Curr Opin Plant Biol 16:554–560

    Article  CAS  PubMed  Google Scholar 

  • Mesejo C, Yuste R, Reig C, Martínez-Fuentes A, Iglesias DJ, Muñoz-Fambuena N, Bermejo A, Germanà MA, Primo-Millo E, Agustí M (2016) Gibberellin reactivates and maintains ovary-wall cell division causing fruit set in parthenocarpic Citrus species. Plant Sci 247:13–24

    Article  CAS  PubMed  Google Scholar 

  • Min XJ, Bartholomew DP (1996) Effect of plant growth regulators on ethylene production, 1-aminocyclopropane-1-carboxylic acid oxidase activity, and initiation of inflorescence development of pineapple. J Plant Growth Regul 15:121–128

    Article  CAS  Google Scholar 

  • Nieminen K, Blomster T, Helariutta Y, Mähönen AP (2015) Vascular cambium development. Arabidopsis Book 13:e0177

    Article  PubMed  PubMed Central  Google Scholar 

  • Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osnato M, Castillejo C, Matías-Hernández L, Pelaz S (2012) TEMPRANILLO genes link photoperiod and gibberellin pathways to control flowering in Arabidopsis. Nat Commun 3:808

    Article  PubMed  Google Scholar 

  • Pauwels L, Goossens A (2011) The JAZ proteins: A crucial interface in the jasmonate signaling cascade. Plant Cell 23:3089–3100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Persson H (1980) Spatial distribution of fine-root growth, mortality and decomposition in a young Scots pine stand in Central Sweden. Oikos 77–87

    Google Scholar 

  • Phillips A (1998) Gibberellins in Arabidopsis. Plant Physiol Biochem 36:115–124

    Article  CAS  Google Scholar 

  • Pierret A, Doussan C, Garrigues E, Kirby JM (2003) Observing plant roots in their environment: Current imaging options and specific contribution of two-dimensional approaches. Agronomie 23:471–479

    Article  Google Scholar 

  • Pilling J, Willmitzer L, Fisahn J (2000) Expression of a Petunia inflata pectin methyl esterase in Solanum tuberosum L. enhances stem elongation and modifies cation distribution. Planta 210:391–399

    Article  CAS  PubMed  Google Scholar 

  • Racolta A, Bryan AC, Tax FE (2014) The receptor-like kinases GSO1 and GSO2 together regulate root growth in Arabidopsis through control of cell division and cell fate specification. Dev Dyn 243:257–278

    Article  CAS  PubMed  Google Scholar 

  • Radwan O, Liu Y, Clough SJ (2011) Transcriptional analysis of soybean root response to Fusarium virguliforme, the causal agent of sudden death syndrome. MPMI 24:958–972

    Article  CAS  PubMed  Google Scholar 

  • Rhee SY, Mutwil M (2014) Towards revealing the functions of all genes in plants. Trends Plant Sci 19:212–221

    Article  CAS  PubMed  Google Scholar 

  • Rose JK, Braam J, Fry SC, Nishitani K (2002) The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: Current perspectives and a new unifying nomenclature. Plant Cell Physiol 43:1421–435

    Article  CAS  PubMed  Google Scholar 

  • Saito S, Okamoto M, Shinoda S, Kushiro T, Koshiba T, Kamiya Y, Hirai N, Todoroki Y, Sakata K, Nambara E, Mizutani M (2006) Plant growth retardant, uniconazole, is a potent inhibitor of ABA catabolism in Arabidopsis. Biosci Biotech Biochem 70:1731–1739

    Article  CAS  Google Scholar 

  • Sakamoto T, Kamiya N, Ueguchi-Tanaka M, Iwahori S, Matsuoka M (2001) KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev 15:581–590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasaki E, Ogura T, Takei K, Kojima M, Kitahata N, Sakakibara H, Asami T, Shimada Y (2013) Uniconazole, a cytochrome P450 inhibitor, inhibits trans-zeatin biosynthesis in Arabidopsis. Phytochemistry 87:30–38

    Article  CAS  PubMed  Google Scholar 

  • Sehr EM, Agusti J, Lehner R, Farmer EE, Schwarz M, Greb T (2010) Analysis of secondary growth in the Arabidopsis shoot reveals a positive role of jasmonate signalling in cambium formation. The Plant Journal 63:811–822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen C, Li D, He R. Fang Z, Xia Y, Gao J, Shen H, Cao M (2014) Comparative transcriptome analysis of RNA-seq data for coldtolerant and cold-sensitive rice genotypes under cold stress. J Plant Biol 57:337

    Article  CAS  Google Scholar 

  • Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T (2011) Cytoscape 2.8: New features for data integration and network visualization. Bioinformatics 27:431–432

    Article  CAS  PubMed  Google Scholar 

  • Song L, Prince S, Valliyodan B, Joshi T, Maldonado dos Santos JV, Wang J, Lin L, Wan J, Wang Y, Xu D, Nguyen HT (2016) Genomewide transcriptome analysis of soybean primary root under varying water-deficit conditions. BMC Genomics 17:57

    Article  PubMed  PubMed Central  Google Scholar 

  • Sorrells TR, Johnson AD (2015) Making sense of transcription networks. Cell 161:714–723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun Z, Wang Y, Mou F, Tian Y, Chen L, Zhang S, Jiang Q, Li X (2016) Genome-wide small RNA analysis of soybean reveals auxin-responsive microRNAs that are differentially expressed in response to salt stress in root apex. Front Plant Sci 6:1273

    Article  PubMed  PubMed Central  Google Scholar 

  • Takase T, Nakazawa M, Ishikawa A, Kawashima M, Ichikawa T, Takahashi N, Shimada H, Manabe K, Matsui M (2004) ydk1-D, an auxin-responsive GH3 mutant that is involved in hypocotyl and root elongation. Plant J 37:471–483

    Article  CAS  PubMed  Google Scholar 

  • Tong Z, Hong B, Yang Y, Li Q, Ma N, Ma C, Gao J (2009) Overexpression of two chrysanthemum DgDREB1 group genes causing delayed flowering or dwarfism in Arabidopsis. Plant Mol Biol 71:115–129

    Article  CAS  PubMed  Google Scholar 

  • Tsuchisaka A, Theologis A (2004) Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiol 136:2982–3000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Upadhyaya A, Davis TD, Walser RH, Galbraith AB, Sankhla N (1989) Uniconazole-induced alleviation of low-temperature damage in relation to antioxidant activity. Biotechnol Tech 3:199–204

    Article  Google Scholar 

  • Wang X, Oh M, Sakata K, Komatsu S (2016) Gel-free/label-free proteomic analysis of root tip of soybean over time under flooding and drought stresses. J Proteomics 130:42–55

    Article  CAS  PubMed  Google Scholar 

  • Yin X, Hiraga S, Hajika M, Nishimura M, Komatsu S (2017) Transcriptomic analysis reveals the flooding tolerant mechanism in flooding tolerant line and abscisic acid treated soybean. Plant Mol Biol 93:479–496

    Article  CAS  PubMed  Google Scholar 

  • Zhang M, Duan L, Tian X, He Z, Li J, Wang B, Li Z (2007) Uniconazoleinduced tolerance of soybean to water deficit stress in relation to changes in photosynthesis, hormones and antioxidant system. J Plant Physiol 164:709–717

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Li J, Ren G, Qin B, Ma H (2016) Synthesis, crystal structure and antifungal activity of a divalent cobalt(II) complex with uniconazole. Acta Crystallogr C Struct Chem 72:485–490

    Article  CAS  PubMed  Google Scholar 

  • Zhou W, Ye Q (1996) Physiological and yield effects of uniconazole on winter rape (Brassica napus L.). J Plant Growth Regul 15:69–73

    Article  CAS  Google Scholar 

  • Zhou WJ, Leul M (1998) Uniconazole-induced alleviation of freezing injury in relation to changes in hormonal balance, enzyme activities and lipid peroxidation in winter rape. Plant Growth Regul 26:41–47

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. State Key Laboratory of Forest Genetics and Tree Breeding, Northeast Forestry University, Harbin, 150040, China

    Yiqiang Han & Guifeng Liu

  2. College of Life Science and Technology, Heilongjiang Bayi Agricultural University, Daqing, 163319, China

    Yiqiang Han & Yamei Gao

  3. College of Agronomy, Heilongjiang Bayi Agricultural University, Daqing, 163319, China

    Ying Shi, Jidao Du & Dianfeng Zheng

Authors
  1. Yiqiang Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yamei Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ying Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jidao Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dianfeng Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Guifeng Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Dianfeng Zheng or Guifeng Liu.

Electronic supplementary material

12374_2017_28_MOESM1_ESM.xls

Genome-wide Transcriptome Profiling Reveals the Mechanism of the Effects of Uniconazole on Root Development in Glycine Max

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Han, Y., Gao, Y., Shi, Y. et al. Genome-wide transcriptome profiling reveals the mechanism of the effects of uniconazole on root development in Glycine Max . J. Plant Biol. 60, 387–403 (2017). https://doi.org/10.1007/s12374-017-0028-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-017-0028-9

Keywords

Search

Navigation