Advertisement

Molecular Biology Reports

, Volume 46, Issue 2, pp 1909–1930 | Cite as

Genome-wide identification and expression analysis of brassinosteroid action-related genes during the shoot growth of moso bamboo

  • Sining Wang
  • Huayu Sun
  • Xiurong Xu
  • Kebin Yang
  • Hansheng Zhao
  • Ying Li
  • Xueping LiEmail author
  • Zimin GaoEmail author
Original Article
  • 204 Downloads

Abstract

Brassinosteroids (BRs) are a group of plant steroid hormones that play crucial roles in a range of plant growth and development processes. BR action includes active BR formation by a complex biosynthesis process and driving BR biological function through signal transduction. Although the characterization of several BR action-related genes has been conducted in a few model plants, systematic information about these genes in bamboo is still lacking. We identified 64 genes related to BR action from the genome of moso bamboo (Phyllostachys edulis), including twenty that participated in BR biosynthesis and forty-four involved in BR signal transduction. The characteristics of all these candidate genes were identified by bioinformatics methods, including the gene structures, basic physical and chemical properties of proteins, conserved domains and evolutionary relationships. Based on the transcriptome data, the candidate genes demonstrated different expression patterns, which were further validated by qRT-PCR using templates from bamboo shoots with different heights. Thirty-four positive and three negative co-expression modules were identified by 44 candidate genes in the newly emerging bamboo shoot. The gene expression patterns and co-expression modules of BR action-related genes in bamboo shoots indicated that they might function to promote bamboo growth through BR biosynthesis and signal transduction processes. This study provides the first step towards the cloning and functional dissection of the role of BR action-related genes in moso bamboo, which also presents an excellent opportunity for genetic engineering using the candidate genes to improve bamboo quantity and quality.

Keywords

Phyllostachys edulis Plant hormone BR biosynthesis and signal transduction Gene expression pattern 

Notes

Acknowledgements

This work received financial support from the Special Fund for Forest Scientific Research in the Public Welfare from State Forestry Administration of China (No. 201504106), and the Sub-Project of National Science and Technology Support Plan of the Twelfth Five-Year in China (Nos. 2015BAD04B01 and 2015BAD04B03).

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. 1.
    Asami T, Min YK et al (2000) Characterization of brassinazole, a triazole-type brassinosteroid biosynthesis inhibitor. Plant Physiol 123(1):93–100CrossRefGoogle Scholar
  2. 2.
    Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2:28–36PubMedGoogle Scholar
  3. 3.
    Bancos S, Szatmari AM et al (2006) Diurnal regulation of the brassinosteroid-biosynthetic CPD gene in Arabidopsis. Plant Physiol 141(1):299–309.  https://doi.org/10.1104/pp.106.079145 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Bishop GJ, Koncz C (2002) Brassinosteroids and plant steroid hormone signaling. Plant Cell 14(Suppl):S97–110CrossRefGoogle Scholar
  5. 5.
    Choe S, Chung Y (2013) The regulation of brassinosteroid biosynthesis in Arabidopsis. Crit Rev Plant Sci 32(6):396–410.  https://doi.org/10.1080/07352689.2013.797856 CrossRefGoogle Scholar
  6. 6.
    Choe S, Dilkes BP et al (1998) The DWF4 gene of Arabidopsis encodes a cytochrome P450 that mediates multiple 22alpha-hydroxylation steps in brassinosteroid biosynthesis. Plant Cell 10(2):231–243PubMedPubMedCentralGoogle Scholar
  7. 7.
    Choe S, Fujioka S et al (2001) Overexpression of DWARF4 in the brassinosteroid biosynthetic pathway results in increased vegetative growth and seed yield in Arabidopsis. Plant J: Cell Mol Biol 26(6):573–582CrossRefGoogle Scholar
  8. 8.
    Choe S, Noguchi T et al (1999) The Arabidopsis dwf7/ste1 mutant is defective in the delta7 sterol C-5 desaturation step leading to brassinosteroid biosynthesis. Plant Cell 11(2):207–221PubMedPubMedCentralGoogle Scholar
  9. 9.
    Choe S, Tanaka A et al (2000) Lesions in the sterol delta reductase gene of Arabidopsis cause dwarfism due to a block in brassinosteroid biosynthesis. Plant J: Cell Mol Biol 21(5):431–443CrossRefGoogle Scholar
  10. 10.
    Clouse SD (2011) Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 23(4):1219–1230.  https://doi.org/10.1105/tpc.111.084475 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Clouse SD, Langford M et al (1996) A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol 111(3):671–678CrossRefGoogle Scholar
  12. 12.
    Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annu Rev Plant Phys 49:427–451.  https://doi.org/10.1146/annurev.arplant.49.1.427 CrossRefGoogle Scholar
  13. 13.
    Clouse SD, Zurek D (1991) Molecular analysis of brassinolide action in plant growth and development. American Chemical Society, Washington DCCrossRefGoogle Scholar
  14. 14.
    De Jong M, Wolters-Arts M et al (2011) The Solanum lycopersicum AUXIN RESPONSE FACTOR 7 (SlARF7) mediates cross-talk between auxin and gibberellin signalling during tomato fruit set and development. J Exp Bot 62(2):617–626.  https://doi.org/10.1093/jxb/erq293 CrossRefPubMedGoogle Scholar
  15. 15.
    Divi UK, Rahman T et al (2010) Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biol 10:151.  https://doi.org/10.1186/1471-2229-10-151 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Domagalska MA, Schomburg FM et al (2007) Attenuation of brassinosteroid signaling enhances FLC expression and delays flowering. Development 134(15):2841–2850.  https://doi.org/10.1242/dev.02866 CrossRefPubMedGoogle Scholar
  17. 17.
    Fan CJ, Ma JM et al (2013) Selection of reference genes for quantitative real-time PCR in bamboo (Phyllostachys edulis). PLoS ONE 8(2):e56573.  https://doi.org/10.1371/journal.pone.0056573 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Friedrichsen DM, Joazeiro CA et al (2000) Brassinosteroid-insensitive-1 is a ubiquitously expressed leucine-rich repeat receptor serine/threonine kinase. Plant Physiol 123(4):1247–1256CrossRefGoogle Scholar
  19. 19.
    Fu FQ, Mao WH et al (2008) A role of brassinosteroids in early fruit development in cucumber. J Exp Bot 59(9):2299–2308.  https://doi.org/10.1093/jxb/ern093 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Fujioka S, Li J et al (1997) The Arabidopsis deetiolated2 mutant is blocked early in brassinosteroid biosynthesis. Plant Cell 9(11):1951–1962.  https://doi.org/10.1105/tpc.9.11.1951 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Fujioka S, Yokota T (2003) Biosynthesis and metabolism of brassinosteroids. Annu Rev Plant Phys 54:137–164.  https://doi.org/10.1146/annurev.arplant.54.031902.134921 CrossRefGoogle Scholar
  22. 22.
    Gamuyao R, Nagai K et al (2017) Hormone distribution and transcriptome profiles in bamboo shoots provide insights on bamboo stem emergence and growth. Plant Cell Physiol 58(4):702–716.  https://doi.org/10.1093/pcp/pcx023 CrossRefPubMedGoogle Scholar
  23. 23.
    Geer LY, Domrachev M et al (2002) CDART: protein homology by domain architecture. Genome Res 12(10):1619–1623.  https://doi.org/10.1101/gr.278202 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Gou X, Yin H et al (2012) Genetic evidence for an indispensable role of somatic embryogenesis receptor kinases in brassinosteroid signaling. PLoS Genet 8(1):e1002452.  https://doi.org/10.1371/journal.pgen.1002452 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    He JX, Gendron JM et al (2005) BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307(5715):1634–1638.  https://doi.org/10.1126/science.1107580 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Hong Z, Ueguchi-Tanaka M et al (2003) A rice brassinosteroid-deficient mutant, ebisu dwarf (d2), is caused by a loss of function of a new member of cytochrome P450. Plant Cell 15(12):2900–2910.  https://doi.org/10.1105/tpc.014712 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Hothorn M, Belkhadir Y et al (2011) Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature 474(7352):467–471.  https://doi.org/10.1038/nature10153 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Hou X, Hu WW et al (2008) Global identification of DELLA target genes during Arabidopsis flower development. Plant Physiol 147(3):1126–1142.  https://doi.org/10.1104/pp.108.121301 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Hu B, Jin J et al (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8):1296–1297.  https://doi.org/10.1093/bioinformatics/btu817 CrossRefPubMedGoogle Scholar
  30. 30.
    Jaillais Y, Hothorn M et al (2011) Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor. Gene Dev 25(3):232–237.  https://doi.org/10.1101/gad.2001911 CrossRefPubMedGoogle Scholar
  31. 31.
    Jiang ZH (2007) Bamboo and rattan in the world. China Publishing House, BeijingGoogle Scholar
  32. 32.
    Kim HB, Kwon M et al (2006) The regulation of DWARF4 expression is likely a critical mechanism in maintaining the homeostasis of bioactive brassinosteroids in Arabidopsis. Plant Physiol 140(2):548–557.  https://doi.org/10.1104/pp.105.067918 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Klahre U, Noguchi T et al (1998) The Arabidopsis DIMINUTO/DWARF1 gene encodes a protein involved in steroid synthesis. Plant Cell 10(10):1677–1690CrossRefGoogle Scholar
  34. 34.
    Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90(5):929–938CrossRefGoogle Scholar
  35. 35.
    Li J, Nagpal P et al (1996) A role for brassinosteroids in light-dependent development of Arabidopsis. Science 272(5260):398–401CrossRefGoogle Scholar
  36. 36.
    Li J, Nam KH (2002) Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science 295(5558):1299–1301.  https://doi.org/10.1126/science.1065769 CrossRefPubMedGoogle Scholar
  37. 37.
    Li L, Cheng Z et al (2018) The association of hormone signalling genes, transcription and changes in shoot anatomy during moso bamboo growth. Plant Biotechnol J 16(1):72–85.  https://doi.org/10.1111/pbi.12750 CrossRefPubMedGoogle Scholar
  38. 38.
    Li L, Hu T et al (2016) Genome-wide analysis of shoot growth-associated alternative splicing in moso bamboo. Mol Genet Genomics: MGG 291(4):1695–1714.  https://doi.org/10.1007/s00438-016-1212-1 CrossRefPubMedGoogle Scholar
  39. 39.
    Liu T, Zhang J et al (2007) Expression and functional analysis of ZmDWF4, an ortholog of Arabidopsis DWF4 from maize (Zea mays L.). Plant Cell Rep 26(12):2091–2099.  https://doi.org/10.1007/s00299-007-0418-4 CrossRefPubMedGoogle Scholar
  40. 40.
    Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402–408.  https://doi.org/10.1006/meth.2001.1262 CrossRefGoogle Scholar
  41. 41.
    Mandava NB (1988) Plant growth-promoting brassinosteroids. Annu Rev Plant Phys 39(1):30Google Scholar
  42. 42.
    Marchler-Bauer A, Bo Y et al (2017) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45(D1):D200–D203.  https://doi.org/10.1093/nar/gkw1129 CrossRefPubMedGoogle Scholar
  43. 43.
    Moore MJ, Sharp PA (1993) Evidence for two active sites in the spliceosome provided by stereochemistry of pre-mRNA splicing. Nature 365(6444):364–368.  https://doi.org/10.1038/365364a0 CrossRefPubMedGoogle Scholar
  44. 44.
    Mora-Garcia S, Vert G et al (2004) Nuclear protein phosphatases with Kelch-repeat domains modulate the response to brassinosteroids in Arabidopsis. Gene Dev 18(4):448–460.  https://doi.org/10.1101/gad.1174204 CrossRefPubMedGoogle Scholar
  45. 45.
    Nakamoto D, Ikeura A et al (2006) Inhibition of brassinosteroid biosynthesis by either a dwarf4 mutation or a brassinosteroid biosynthesis inhibitor rescues defects in tropic responses of hypocotyls in the arabidopsis mutant nonphototropic hypocotyl 4. Plant Physiol 141(2):456–464.  https://doi.org/10.1104/pp.105.076273 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Nebert DW, Gonzalez FJ (1987) P450 genes: structure, evolution, and regulation. Annu Rev Plant Phys 56:945–993.  https://doi.org/10.1146/annurev.bi.56.070187.004501 CrossRefGoogle Scholar
  47. 47.
    Neff MM, Nguyen SM et al (1999) BAS1: A gene regulating brassinosteroid levels and light responsiveness in Arabidopsis. P Natl Acad Sci USA 96(26):15316–15323CrossRefGoogle Scholar
  48. 48.
    Noguchi T, Fujioka S et al (1999) Arabidopsis det2 is defective in the conversion of (24R)-24-methylcholest-4-En-3-one to (24R)-24-methyl-5alpha-cholestan-3-one in brassinosteroid biosynthesis. Plant Physiol 120(3):833–840CrossRefGoogle Scholar
  49. 49.
    Nomura T, Sato T et al (2001) Accumulation of 6-deoxocathasterone and 6-deoxocastasterone in Arabidopsis, pea and tomato is suggestive of common rate-limiting steps in brassinosteroid biosynthesis. Phytochemist 57(2):171–178CrossRefGoogle Scholar
  50. 50.
    Ohnishi T, Godza B et al (2012) CYP90A1/CPD, a brassinosteroid biosynthetic cytochrome P450 of Arabidopsis, catalyzes C-3 oxidation. J Biol Chem 287(37):31551–31560.  https://doi.org/10.1074/jbc.M112.392720 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Parsons HT, Christiansen K et al (2012) Isolation and proteomic characterization of the Arabidopsis Golgi defines functional and novel components involved in plant cell wall biosynthesis. Plant Physiol 159(1):12–26.  https://doi.org/10.1104/pp.111.193151 CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Peng Z, Lu Y et al (2013) The draft genome of the fast-growing non-timber forest species moso bamboo (Phyllostachys heterocycla). Nat Genet 45(4):456–461.  https://doi.org/10.1038/ng.2569461e451-452.CrossRefPubMedGoogle Scholar
  53. 53.
    Peng Z, Zhang C et al (2013) Transcriptome sequencing and analysis of the fast growing shoots of moso bamboo (Phyllostachys edulis). PLoS ONE 8(11):e78944.  https://doi.org/10.1371/journal.pone.0078944 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Sakamoto T, Morinaka Y et al (2006) Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nat Biotechnol 24(1):105–109.  https://doi.org/10.1038/nbt1173 CrossRefPubMedGoogle Scholar
  55. 55.
    Sasse JM (2003) Physiological actions of brassinosteroids: an update. J Plant Growth Regul 22(4):276–288.  https://doi.org/10.1007/s00344-003-0062-3 CrossRefPubMedGoogle Scholar
  56. 56.
    Sekimata K, Kimura T et al (2001) A specific brassinosteroid biosynthesis inhibitor, Brz2001: evaluation of its effects on Arabidopsis, cress, tobacco, and rice. Planta 213(5):716–721CrossRefGoogle Scholar
  57. 57.
    She J, Han Z et al (2011) Structural insight into brassinosteroid perception by BRI1. Nature 474(7352):472–476.  https://doi.org/10.1038/nature10178 CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Shimada Y, Fujioka S et al (2001) Brassinosteroid-6-oxidases from Arabidopsis and tomato catalyze multiple C-6 oxidations in brassinosteroid biosynthesis. Plant Physiol 126(2):770–779CrossRefGoogle Scholar
  59. 59.
    Shimada Y, Goda H et al (2003) Organ-specific expression of brassinosteroid-biosynthetic genes and distribution of endogenous brassinosteroids in Arabidopsis. Plant Physiol 131(1):287–297.  https://doi.org/10.1104/pp.013029 CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Silvestro D, Andersen TG et al (2013) Plant sterol metabolism. Delta(7)-Sterol-C5-desaturase (STE1/DWARF7), Delta(5,7)-sterol-Delta(7)-reductase (DWARF5) and Delta(24)-sterol-Delta(24)-reductase (DIMINUTO/DWARF1) show multiple subcellular localizations in Arabidopsis thaliana (Heynh) L. PLoS ONE 8(2):e56429.  https://doi.org/10.1371/journal.pone.0056429 CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Singh AP, Fridman Y et al (2018) Interdependent nutrient availability and steroid hormone signals facilitate root growth plasticity. Dev Cell 46(1):59–72 e54.  https://doi.org/10.1016/j.devcel.2018.06.002 CrossRefPubMedGoogle Scholar
  62. 62.
    Sun H, Li L, Lou Y et al (2017) The bamboo aquaporin gene PeTIP4;1–1 confers drought and salinity tolerance in transgenic Arabidopsis. Plant Cell Rep 36(4):597–609.  https://doi.org/10.1007/s00299-017-2106-3 CrossRefPubMedGoogle Scholar
  63. 63.
    Sun HY, Lou YF et al (2017) Advance in the growth and development of bamboo culm. World Forest Res 30(4):18–23.  https://doi.org/10.13348/j.cnki.sjlyyj.2017.0035.y CrossRefGoogle Scholar
  64. 64.
    Taiz L, Zeiger E (2002) Plant physiology. Sinauer Associates, SunderlandGoogle Scholar
  65. 65.
    Tamura K, Stecher G et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729.  https://doi.org/10.1093/molbev/mst197 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Tanabe S, Ashikari M et al (2005) A novel cytochrome P450 is implicated in brassinosteroid biosynthesis via the characterization of a rice dwarf mutant, dwarf11, with reduced seed length. Plant Cell 17(3):776–790.  https://doi.org/10.1105/tpc.104.024950 CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Tanaka K, Asami T et al (2005) Brassinosteroid homeostasis in Arabidopsis is ensured by feedback expressions of multiple genes involved in its metabolism. Plant Physiol 138(2):1117–1125.  https://doi.org/10.1104/pp.104.058040 CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Tang Y, Liu H et al (2018) OsmiR396d affects gibberellin and brassinosteroid signaling to regulate plant architecture in rice. Plant Physiol 176(1):946–959.  https://doi.org/10.1104/pp.17.00964 CrossRefPubMedGoogle Scholar
  69. 69.
    Tao GY, Fu Y et al (2018) Advances in studies on molecular mechanisms of rapid growth of bamboo species. J Agric Biotechnol 26(5):17.  https://doi.org/10.3969/j.issn.1674-7968.2018.05.015 CrossRefGoogle Scholar
  70. 70.
    Thompson JD, Higgins DG et al (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680CrossRefGoogle Scholar
  71. 71.
    Turk EM, Fujioka S et al (2003) CYP72B1 inactivates brassinosteroid hormones: an intersection between photomorphogenesis and plant steroid signal transduction. Plant Physiol 133(4):1643–1653.  https://doi.org/10.1104/pp.103.030882 CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Vert G, Nemhauser JL et al (2005) Molecular mechanisms of steroid hormone signaling in plants. Annu Rev Plant Phys 21:177–201.  https://doi.org/10.1146/annurev.cellbio.21.090704.151241 CrossRefGoogle Scholar
  73. 73.
    Wang HY, Cui K et al (2015) Endogenous hormonal equilibrium linked to bamboo culm development. Geneti Mol Res: GMR 14(3):11312–11323.  https://doi.org/10.4238/2015.September.22.25 CrossRefGoogle Scholar
  74. 74.
    Wang KH, Huang BH (1996) Chinese bamboo. Publishing House for Science and Technology, ZhejiangGoogle Scholar
  75. 75.
    Wang W, Gu L et al (2017) Genome-wide analysis and transcriptomic profiling of the auxin biosynthesis, transport and signaling family genes in moso bamboo (Phyllostachys heterocycla). BMC Genom 18(1):870.  https://doi.org/10.1186/s12864-017-4250-0 CrossRefGoogle Scholar
  76. 76.
    Wang X, Chory J (2006) Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 313(5790):1118–1122.  https://doi.org/10.1126/science.1127593 CrossRefPubMedGoogle Scholar
  77. 77.
    Wang X, Kota U et al (2008) Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev Cell 15(2):220–235.  https://doi.org/10.1016/j.devcel.2008.06.011 CrossRefPubMedGoogle Scholar
  78. 78.
    Wang ZY, Seto H et al (2001) BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410(6826):380–383.  https://doi.org/10.1038/35066597 CrossRefPubMedGoogle Scholar
  79. 79.
    Werck-Reichhart D, Hehn A et al (2000) Cytochromes P450 for engineering herbicide tolerance. Trends Plant Sci 5(3):116–123CrossRefGoogle Scholar
  80. 80.
    Yang M, Li C et al (2017) SINAT E3 Ligases control the light-mediated stability of the brassinosteroid-activated transcription factor BES1 in Arabidopsis. Dev Cell 41(1):47–58 e44.  https://doi.org/10.1016/j.devcel.2017.03.014 CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Ye Q, Zhu W et al (2010) Brassinosteroids control male fertility by regulating the expression of key genes involved in Arabidopsis anther and pollen development. P Natl Acad Sci USA 107(13):6100–6105.  https://doi.org/10.1073/pnas.0912333107 CrossRefGoogle Scholar
  82. 82.
    Youn JH, Kim TW et al (2018) Function and molecular regulation of DWARF1 as a C-24 reductase in brassinosteroid biosynthesis in Arabidopsis. J Exp Bot 69(8):1873–1886.  https://doi.org/10.1093/jxb/ery038 CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Zhang Z, Xu L (2018) Arabidopsis BRASSINOSTEROID INACTIVATOR2 is a typical BAHD acyltransferase involved in brassinosteroid homeostasis. J Exp Bot 69(8):1925–1941.  https://doi.org/10.1093/jxb/ery057 CrossRefPubMedGoogle Scholar
  84. 84.
    Zhao H, Peng Z et al (2014) BambooGDB: a bamboo genome database with functional annotation and an analysis platform. Database 2014:bau006.  https://doi.org/10.1093/database/bau006 CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Zheng L, Ma J et al (2017) Genome-wide identification and expression profiling analysis of brassinolide signal transduction genes regulating apple tree architecture. Acta Physiol Plant 39(8).  https://doi.org/10.1007/s11738-017-2479-5

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Sining Wang
    • 1
  • Huayu Sun
    • 1
    • 2
  • Xiurong Xu
    • 1
  • Kebin Yang
    • 1
  • Hansheng Zhao
    • 1
  • Ying Li
    • 1
  • Xueping Li
    • 1
    Email author
  • Zimin Gao
    • 1
    Email author
  1. 1.State Forestry Administration Key Open Laboratory on the Science and Technology of Bamboo and Rattan, Institute of Gene Science for Bamboo and Rattan ResourcesInternational Centre for Bamboo and RattanBeijingChina
  2. 2.Department of Plant Science and Landscape ArchitectureUniversity of ConnecticutStorrsUSA

Personalised recommendations