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Physiological and transcriptomic analyses of brassinosteroid function in moso bamboo (Phyllostachys edulis) seedlings

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Abstract

Main conclusion

This study demonstrates that brassinosteroid is essential for seedling and shoot growth in moso bamboo.

Abstract

The shoot of moso bamboo is known to grow extremely fast. The roles of phytohormones in such fast growth of bamboo shoot remain unclear. Here we reported that endogenous brassinosteroid (BR) is a major factor promoting bamboo shoot internode elongation. Reducing endogenous brassinosteroid level by its biosynthesis inhibitor propiconazole stunted shoot growth in seedling stage, whereas exogenous BR application promoted scale leaf elongation and the inclination of lamina joint of leaves and scale leaves. Genome-wide transcriptome analysis identified hundreds of genes whose expression levels are altered by BR and propiconazole in shoots and roots of bamboo seedling. The data show that BR regulates cell wall-related genes, hydrogen peroxide catabolic genes, and auxin-related genes. Our study demonstrates an essential role of BR in fast growth bamboo shoots and identifies a large number of BR-responsive genes in bamboo seedlings.

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Data availability

The RNA-seq raw data were deposited in the National Center for Biotechnology Information database (GSE123529).

Abbreviations

BR:

Brassinosteroid

BL:

Brassinolide

DEG:

Differentially expressed gene

eBL:

2,4-Epicastasterone

GO:

Gene ontology

PPZ:

Propiconazole

ROS:

Reactive oxygen species

References

  • Bao F, Shen J, Brady SR, Muday GK, Asami T, Yang Z (2004) Brassinosteroids interact with auxin to promote lateral root development in Arabidopsis. Plant Physiol 134:1624–1631

    CAS  PubMed  PubMed Central  Google Scholar 

  • Borodina T, Adjaye J, Sultan M (2011) A strand-specific library preparation protocol for RNA sequencing. Methods Enzymol 500:79–98

    CAS  PubMed  Google Scholar 

  • Chaiwanon J, Wang ZY (2015) Spatiotemporal brassinosteroid signaling and antagonism with auxin pattern stem cell dynamics in Arabidopsis roots. Curr Biol 25:1031–1042

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chaiwanon J, Wang W, Zhu JY, Oh E, Wang ZY (2016) Information integration and communication in plant growth regulation. Cell 164:1257–1268

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chung Y, Maharjan PM, Lee O, Fujioka S, Jang S, Kim B, Takatsuto S, Tsujimoto M, Kim H, Cho S, Park T, Cho H, Hwang I, Choe S (2011) Auxin stimulates DWARF4 expression and brassinosteroid biosynthesis in Arabidopsis. Plant J 66:564–578

    CAS  PubMed  Google Scholar 

  • Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451

    CAS  PubMed  Google Scholar 

  • Cui K, He CY, Zhang JG, Duan AG, Zeng YF (2012) Temporal and spatial profiling of internode elongation-associated protein expression in rapidly growing culms of bamboo. J Proteome Res 11:2492–2507

    CAS  PubMed  Google Scholar 

  • Francoz E, Ranocha P, Nguyen-Kim H, Jamet E, Burlat V, Dunand C (2015) Roles of cell wall peroxidases in plant development. Phytochemistry 112:15–21

    CAS  PubMed  Google Scholar 

  • Fu JH (2001) Chinese moso bamboo: its importance. Bamboo 22:5–7

    Google Scholar 

  • Fukuda H (2004) Signals that control plant vascular cell differentiation. Nat Rev Mol Cell Biol 5:379–391

    CAS  PubMed  Google Scholar 

  • Gamuyao R, Nagai K, Ayano M, Mori Y, Minami A, Kojima M, Suzuki T, Sakakibara H, Higashiyama T, Ashikari M, Reuscher S (2017) Hormone distribution and transcriptome profiles in bamboo shoots provide insights on bamboo stem emergence and growth. Plant Cell Physiol 58:702–716

    CAS  PubMed  Google Scholar 

  • Hartwig T, Corvalan C, Best NB, Budka JS, Zhu JY, Choe S, Schulz B (2012) Propiconazole is a specific and accessible brassinosteroid (BR) biosynthesis inhibitor for Arabidopsis and maize. PLoS ONE 7:e36625

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ibanes M, Fabregas N, Chory J, Cano-Delgado AI (2009) Brassinosteroid signaling and auxin transport are required to establish the periodic pattern of Arabidopsis shoot vascular bundles. Proc Natl Acad Sci USA 106:13630–13635

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim H, Park PJ, Hwang HJ, Lee SY, Oh MH, Kim SG (2006) Brassinosteroid signals control expression of the AXR3/IAA17 gene in the cross-talk point with auxin in root development. Biosci Biotechnol Biochem 70:768–773

    CAS  PubMed  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

    PubMed  PubMed Central  Google Scholar 

  • Li J (2010) Regulation of the nuclear activities of brassinosteroid signaling. Curr Opin Plant Biol 13:540–547

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li L, Xu J, Xu ZH, Xue HW (2005) Brassinosteroids stimulate plant tropisms through modulation of polar auxin transport in Brassica and Arabidopsis. Plant Cell 17:2738–2753

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li XJ, Guo X, Zhou YH, Shi K, Zhou J, Yu JQ, Xia XJ (2016) Overexpression of a brassinosteroid biosynthetic gene Dwarf enhances photosynthetic capacity through activation of Calvin cycle enzymes in tomato. BMC Plant Biol 16:33

    PubMed  PubMed Central  Google Scholar 

  • Liu X, Yang CY, Miao R, Zhou CL, Cao PH, Lan J, Zhu XJ, Mou CL, Huang YS, Liu SJ, Tian YL, Nguyen TL, Jiang L, Wan JM (2018) DS1/OsEMF1 interacts with OsARF11 to control rice architecture by regulation of brassinosteroid signaling. Rice 11:46

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lv B, Tian H, Zhang F, Liu J, Lu S, Bai M, Li C, Ding Z (2018) Brassinosteroids regulate root growth by controlling reactive oxygen species homeostasis and dual effect on ethylene synthesis in Arabidopsis. PLoS Genet 14:e1007144

    PubMed  PubMed Central  Google Scholar 

  • Maere S, Heymans K, Kuiper M (2005) BiNGO: a cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21:3448–3449

    CAS  PubMed  Google Scholar 

  • Maharjan PM, Schulz B, Choe S (2011) BIN2/DWF12 antagonistically transduces brassinosteroid and auxin signals in the roots of Arabidopsis. J Plant Biol 54:126–134

    CAS  Google Scholar 

  • Mahonen AP, Ten Tusscher K, Siligato R, Smetana O, Diaz-Trivino S, Salojarvi J, Wachsman G, Prasad K, Heidstra R, Scheres B (2014) PLETHORA gradient formation mechanism separates auxin responses. Nature 515:125–129

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:W182–W185

    PubMed  PubMed Central  Google Scholar 

  • Mouchel CF, Osmont KS, Hardtke CS (2006) BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth. Nature 443:458–461

    CAS  PubMed  Google Scholar 

  • Nakamura A, Higuchi K, Goda H, Fujiwara MT, Sawa S, Koshiba T, Shimada Y, Yoshida S (2003) Brassinolide induces IAA5, IAA19, and DR5, a synthetic auxin response element in Arabidopsis, implying a cross talk point of brassinosteroid and auxin signaling. Plant Physiol 133:1843–1853

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura A, Goda H, Shimada Y, Yoshida S (2004) Brassinosteroid selectively regulates PIN gene expression in Arabidopsis. Biosci Biotechnol Biochem 68:952–954

    CAS  PubMed  Google Scholar 

  • Nie WF, Wang MM, Xia XJ, Zhou YH, Shi K, Chen Z, Yu JQ (2013) Silencing of tomato RBOH1 and MPK2 abolishes brassinosteroid-induced H2O2 generation and stress tolerance. Plant Cell Environ 36:789–803

    CAS  PubMed  Google Scholar 

  • Oh E, Zhu JY, Bai MY, Arenhart RA, Sun Y, Wang ZY (2014) Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. Elife 3:e03031

    PubMed Central  Google Scholar 

  • Oh K, Matsumoto T, Hoshi T, Yoshizawa Y (2016) In vitro and in vivo evidence for the inhibition of brassinosteroid synthesis by propiconazole through interference with side chain hydroxylation. Plant Signal Behav 11:e1158372

    PubMed  PubMed Central  Google Scholar 

  • Ou Y, Lu X, Zi Q, Xun Q, Zhang J, Wu Y, Shi H, Wei Z, Zhao B, Zhang X, He K, Gou X, Li C, Li J (2016) RGF1 INSENSITIVE 1 to 5, a group of LRR receptor-like kinases, are essential for the perception of root meristem growth factor 1 in Arabidopsis thaliana. Cell Res 26:686–698

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peng Z, Lu Y, Li L, Zhao Q, Feng Q, Gao Z, Lu H, Hu T, Yao N, Liu K, Li Y, Fan D, Guo Y, Li W, Lu Y, Weng Q, Zhou C, Zhang L, Huang T, Zhao Y, Zhu C, Liu X, Yang X, Wang T, Miao K, Zhuang C, Cao X, Tang W, Liu G, Liu Y, Chen J, Liu Z, Yuan L, Liu Z, Huang X, Lu T, Fei B, Ning Z, Han B, Jiang Z (2013a) The draft genome of the fast-growing non-timber forest species moso bamboo (Phyllostachys heterocycla). Nat Genet 45:456–461

    CAS  PubMed  Google Scholar 

  • Peng Z, Zhang C, Zhang Y, Hu T, Mu S, Li X, Gao J (2013b) Transcriptome sequencing and analysis of the fast growing shoots of moso bamboo (Phyllostachys edulis). PLoS ONE 8:e78944

    CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140

    CAS  PubMed  Google Scholar 

  • Sakamoto T, Morinaka Y, Inukai Y, Kitano H, Fujioka S (2013) Auxin signal transcription factor regulates expression of the brassinosteroid receptor gene in rice. Plant J 73:676–688

    CAS  PubMed  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    CAS  PubMed  PubMed Central  Google Scholar 

  • Singh AP, Fridman Y, Friedlander-Shani L, Tarkowska D, Strnad M, Savaldi-Goldstein S (2014) Activity of the brassinosteroid transcription factors BRASSINAZOLE RESISTANT1 and BRASSINOSTEROID INSENSITIVE1-ETHYL METHANESULFONATE-SUPPRESSOR1/BRASSINAZOLE RESISTANT2 blocks developmental reprogramming in response to low phosphate availability. Plant Physiol 166:678–688

    PubMed  PubMed Central  Google Scholar 

  • Song X, Peng C, Zhou G, Gu H, Li Q, Zhang C (2016) Dynamic allocation and transfer of non-structural carbohydrates, a possible mechanism for the explosive growth of moso bamboo (Phyllostachys heterocycla). Sci Rep 6:25908

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun Y, Fan XY, Cao DM, Tang W, He K, Zhu JY, He JX, Bai MY, Zhu S, Oh E, Patil S, Kim TW, Ji H, Wong WH, Rhee SY, Wang ZY (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev Cell 19:765–777

    CAS  PubMed  PubMed Central  Google Scholar 

  • Supek F, Bosnjak M, Skunca N, Smuc T (2011) REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE 6:e21800

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tian Y, Fan M, Qin Z, Lv H, Wang M, Zhang Z, Zhou W, Zhao N, Li X, Han C, Ding Z, Wang W, Wang ZY, Bai MY (2018) Hydrogen peroxide positively regulates brassinosteroid signaling through oxidation of the BRASSINAZOLE-RESISTANT1 transcription factor. Nat Commun 9:1–13

    Google Scholar 

  • Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vilarrasa-Blasi J, Gonzalez-Garcia MP, Frigola D, Fabregas N, Alexiou KG, Lopez-Bigas N, Rivas S, Jauneau A, Lohmann JU, Benfey PN, Ibanes M, Cano-Delgado AI (2014) Regulation of plant stem cell quiescence by a brassinosteroid signaling module. Dev Cell 30:36–47

    CAS  PubMed  Google Scholar 

  • Walcher CL, Nemhauser JL (2012) Bipartite promoter element required for auxin response. Plant Physiol 158:273–282

    CAS  PubMed  Google Scholar 

  • Wang ZY, Bai MY, Oh E, Zhu JY (2012) Brassinosteroid signaling network and regulation of photomorphogenesis. Annu Rev Genet 46:701–724

    CAS  PubMed  Google Scholar 

  • Wang W, Gu L, Ye S, Zhang H, Cai C, Xiang M, Gao Y, Wang Q, Lin C, Zhu Q (2017) Genome-wide analysis and transcriptomic profiling of the auxin biosynthesis, transport and signaling family genes in moso bamboo (Phyllostachys heterocycla). BMC Genom 18:870

    Google Scholar 

  • Wang S, Sun H, Xu X, Yang K, Zhao H, Li Y, Li X, Gao Z (2019a) Genome-wide identification and expression analysis of brassinosteroid action-related genes during the shoot growth of moso bamboo. Mol Biol Rep 46:1909–1930

    CAS  PubMed  Google Scholar 

  • Wang T, Li Q, Lou S, Yang Y, Peng L, Lin Z, Hu Q, Ma L (2019b) GSK3/shaggy-like kinase 1 ubiquitously regulates cell growth from Arabidopsis to moso bamboo (Phyllostachys edulis). Plant Sci 283:290–300

    CAS  PubMed  Google Scholar 

  • Xia XJ, Gao CJ, Song LX, Zhou YH, Shi K, Yu JQ (2014) Role of H2O2 dynamics in brassinosteroid-induced stomatal closure and opening in Solanum lycopersicum. Plant Cell Environ 37:2036–2050

    CAS  PubMed  Google Scholar 

  • Youn JH, Kim TW, Joo SH, Son SH, Roh J, Kim S, Kim TW, Kim SK (2018) Function and molecular regulation of DWARF1 as a C-24 reductase in brassinosteroid biosynthesis in Arabidopsis. J Exp Bot 69:1873–1886

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yu G, Wang LG, Han Y, He Q (2012) clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS 16:284–287

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang C, Bai MY, Chong K (2014) Brassinosteroid-mediated regulation of agronomic traits in rice. Plant Cell Rep 33:683–696

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Wang H, Zhu Q, Gao Y, Wang H, Zhao L, Wang Y, Xi F, Wang W, Yang Y, Lin C, Gu L (2018) Transcriptome characterization of moso bamboo (Phyllostachys edulis) seedlings in response to exogenous gibberellin applications. BMC Plant Biol 18:125

    PubMed  PubMed Central  Google Scholar 

  • Zhao H, Gao Z, Wang L, Wang J, Wang S, Fei B, Chen C, Shi C, Liu X, Zhang H, Lou Y, Chen L, Sun H, Zhou X, Wang S, Zhang C, Xu H, Li L, Yang Y, Wei Y, Yang W, Gao Q, Yang H, Zhao S, Jiang Z (2018) Chromosome-level reference genome and alternative splicing atlas of moso bamboo (Phyllostachys edulis). Gigascience 7:115

    Google Scholar 

  • Zhou J, Wang J, Li X, Xia XJ, Zhou YH, Shi K, Chen Z, Yu JQ (2014) H2O2 mediates the crosstalk of brassinosteroid and abscisic acid in tomato responses to heat and oxidative stresses. J Exp Bot 65:4371–4383

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu T, Deng X, Zhou X, Zhu L, Zou L, Li P, Zhang D, Lin H (2016) Ethylene and hydrogen peroxide are involved in brassinosteroid-induced salt tolerance in tomato. Sci Rep 6:35392

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by a grant from the National Natural Science Foundation of China Grant (No. 31700254) and FAFU-International Collaborative Program (KXb16005A) to WW, the National Natural Science Foundation of China Grant (No. 31500226) to XY, the National Natural Science Foundation of China Grant (No. 31600230) to KS, the National Natural Science Foundation of China Grant (No. 31971734) to LG, and the Program for scientific and technological innovation team in University of Fujian province (No. 118/KLA18069A) to QZ.

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Correspondence to Wenfei Wang.

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Communicated by Dorothea Bartels.

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Zhang, Z., Yang, X., Cheng, L. et al. Physiological and transcriptomic analyses of brassinosteroid function in moso bamboo (Phyllostachys edulis) seedlings. Planta 252, 27 (2020). https://doi.org/10.1007/s00425-020-03432-z

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