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Effects of exogenous 24-epibrassinolide and brassinazole on negative gravitropism and tension wood formation in hybrid poplar (Populus deltoids × Populus nigra)

  • Junlan Gao
  • Min Yu
  • Shiliu Zhu
  • Liang Zhou
  • Shengquan LiuEmail author
Original Article
  • 57 Downloads

Abstract

Main conclusion

Exogenous 24-epibrassinolide (BL) and brassinazole (BRZ) have regulatory roles in G-fiber cell wall development and secondary xylem cell wall carbohydrate biosynthesis during tension wood formation in hybrid poplar.

Brassinosteroids (BRs) play important roles in regulating gravitropism and vasculature development. Here, we report the effect of brassinosteroids on negative gravitropism and G-fiber cell wall development of the stem in woody angiosperms. We applied exogenous 24-epibrassinolide (BL) or its biosynthesis inhibitor brassinazole (BRZ) to slanted hybrid poplar trees (Populus deltoids × Populus nigra) and measured the morphology of gravitropic stems, anatomy and chemistry of secondary cell wall. We furthermore analyzed the expression levels of auxin transport and cellulose biosynthetic genes after 24-epibrassinolide (BL) or brassinazole (BRZ) application. The BL-treated seedlings showed no negative gravitropism bending, whereas application of BRZ dramatically enhanced negative gravitropic bending. BL treatment stimulated secondary xylem fiber elongation and G-fiber formation on the upper side of stems but delayed G-fiber maturation. BRZ inhibited xylem fiber elongation but induced the production of more mature G-fibers on the upper side of stems. Wood chemistry analyses and immunolocalization demonstrated that BL and BRZ treatments increased the cellulose content and modified the deposition of cell wall carbohydrates including arabinose, galactose and rhamnose in the secondary xylem. The expression of cellulose biosynthetic genes, especially those related to cellulose microfibril deposition (PtFLA12 and PtCOBL4) was significantly upregulated in BL- and BRZ-treated TW stems compared with control stems. The significant differences of G-fibers development and negative gravitropism bending between 24-epibrassinolide (BL) and brassinazole (BRZ) application suggest that brassinosteroids are important for secondary xylem development during tension wood formation. Our findings provide potential insights into the mechanism by which BRs regulate G-fiber cell wall development to accomplish negative gravitropism in TW formation.

Keywords

Brassinosteroids Gelatinous layer Cellulose biosynthesis PtFLA12 PtCOBL4 Immunofluorescence Cell wall carbohydrates 

Notes

Acknowledgements

This work was supported by the National Key Research and Development Program of China (No. 2017YFD0600201), the China Postdoctoral Science Foundation (No. 2016M601995), and the Anhui Province Postdoctoral Science Foundation (No. 2017B165). We are very grateful to Mr K. Liu for suggestions in identification of tension wood experimental design and manuscript writing. We would also like to thank Robbie Lewis for his assistance with language editing.

Supplementary material

425_2018_3074_MOESM1_ESM.tif (4.8 mb)
Supplementary Fig. S1 Transverse stem sections stained with DAPI showing the distribution of cellulose. (a) Blue fluorescence is observed when sections are treated with the DAPI staining. (b) Scan mode shows the scanning image of the section. Bar: 500 μm (TIFF 4907 kb)
425_2018_3074_MOESM2_ESM.tif (3.2 mb)
Supplementary Fig. S2 Negative LM5 immunolabeling controls of the inclined stem cross-sections from trees subjected to 1 week BL or BRZ stimulation. No signal is present when the primary LM5 antibodies are omitted and sections are treated with the 488 and 633 Alexa secondary antibodies. Blue fluorescence is observed when sections are treated with the DAPI staining. Scan mode shows the scanning image of the section. Bar: 50 μm (TIFF 3268 kb)
425_2018_3074_MOESM3_ESM.tif (1.1 mb)
Supplementary Fig. S3 Negative LM10 immunolabeling controls of the inclined stem cross-sections from trees subjected to 1 week BL or BRZ stimulation. No signal is present when the primary LM10 antibodies are omitted and sections are treated with the 488 and 633 Alexa secondary antibodies. Blue fluorescence is observed when sections are treated with the DAPI staining. Scan mode shows the scanning image of the section. Bar: 50 μm (TIFF 1165 kb)
425_2018_3074_MOESM4_ESM.tif (1.2 mb)
Supplementary Fig. S4 Negative LM21 immunolabeling controls of the inclined stem cross-sections from trees subjected to 1 week BL or BRZ stimulation. No signal is present when the primary LM21 antibodies are omitted and sections are treated with the 488 and 633 Alexa secondary antibodies. Blue fluorescence is observed when sections are treated with the DAPI staining. Scan mode shows the scanning image of the section. Bar: 50 μm (TIFF 1201 kb)
425_2018_3074_MOESM5_ESM.tif (1.1 mb)
Supplementary Fig. S5 Negative 2F4 immunolabeling controls of the inclined stem cross-sections from trees subjected to 1 week BL or BRZ stimulation. No signal is present when the primary 2F4 antibodies are omitted and sections are treated with the 488 and 633 Alexa secondary antibodies. Blue fluorescence is observed when sections are treated with the DAPI staining. Scan mode shows the scanning image of the section. Bar: 50 μm (TIFF 1159 kb)
425_2018_3074_MOESM6_ESM.tif (37.8 mb)
Supplementary Fig. S6 Immunolocalizations with LM5, LM10, LM21 and 2F4 antibody (in red) and cellulose (DAPI in light blue) in transverse sections of BL or BRZ-treated stems after 1 week of OW. (a) BRZ-treated stems with LM5 labeling. (b) Mock control-treated stems with LM5 labeling. (c) BL-treated stem with LM5 labeling. (d) BRZ-treated stems with LM10 labeling. (e) Mock control-treated stems with LM10 labeling. (f) BL-treated stem with LM10 labeling. (g) BRZ-treated stems with LM21 labeling. (h) Mock control-treated stems with LM21 labeling. (i) BL-treated stem with LM21 labeling. (j) BRZ-treated stems with 2F4 labeling. (k) Mock control-treated stems with 2F4 labeling. (l) BL-treated stem with 2F4 labeling. Box indicates the areas shown in detail in a–l. cz, cambial zone; pf, phloem fiber; xy, xylem; v, xylem vessel; OW, opposite wood. Arrowhead indicates the LM5, LM10, LM21 and 2F4 labeling in these fibers. Bars: a-l = 100 μm; box in a-l = 20 μm (TIFF 38,738 kb)
425_2018_3074_MOESM7_ESM.docx (20 kb)
Supplementary Table S1 Oligonucleotide sequences used in the semi-quantitative RT-PCR analysis (DOCX 19 kb)
425_2018_3074_MOESM8_ESM.xlsx (23 kb)
Supplementary Table S2 The original data of xylary fibers length (XLSX 22 kb)
425_2018_3074_MOESM9_ESM.xlsx (18 kb)
Supplementary Table S3 The original data of xylary fibers width (XLSX 18 kb)

References

  1. Altaner C, Tokareva E, Jarvis M, Harris P (2010) Distribution of (1 → 4)-beta-galactans, arabinogalactan proteins, xylans and (1 → 3)-beta-glucans in tracheid cell walls of softwoods. Tree Physiol 30:782–793CrossRefGoogle Scholar
  2. Andersson-Gunneras S, Mellerowicz EJ, Love J, Segerman B, Ohmiya Y, Coutinho PM, Nilsson P, Henrissat B, Moritz T, Sundberg B (2006) Biosynthesis of cellulose-enriched tension wood in Populus: global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis. Plant J 45:144–165CrossRefGoogle Scholar
  3. Andersson-Gunnerås S, Hellgren JM, Björklund S, Regan S, Moritz T, Sundberg B (2003) Asymmetric expression of a poplar ACC oxidase controls ethylene production during gravitational induction of tension wood. Plant J 34:339–349CrossRefGoogle Scholar
  4. Arend M (2008) Immunolocalization of (1, 4)-β-galactan in tension wood fibers of poplar. Tree Physiol 28:1263–1267CrossRefGoogle Scholar
  5. Azri W, Chambon C, Herbette S, Brunel N, Coutand C, Leplé JC, Ben RI, Ammar S, Julien JL, Roeckel-Drevet P (2009) Proteome analysis of apical and basal regions of poplar stems under gravitropic stimulation. Physiol Plant 136:193–208CrossRefGoogle Scholar
  6. Azri W, Ennajah A, Nasr Z, Woo SY, Khaldi A (2014) Transcriptome profiling the basal region of poplar stems during the early gravitropic response. Biol Plant 58:55–63CrossRefGoogle Scholar
  7. Baster P, Robert S, Kleine-Vehn J, Vanneste S, Kania U, Grunewald W, Rybel BD, Beeckman T, Friml J (2014) SCFTIR1/AFB-auxin signalling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism. EMBO J 32:260–274CrossRefGoogle Scholar
  8. Bowling AJ, Vaughn KC (2008) Immunocytochemical characterization of tension wood: gelatinous fibers contain more than just cellulose. Am J Bot 95:655–663CrossRefGoogle Scholar
  9. Clair B, Alméras T, Pilate G, Jullien D, Sugiyama J, Riekel C (2011) Maturation stress generation in poplar tension wood studied by synchrotron radiation microdiffraction. Plant Physiol 155:562–570CrossRefGoogle Scholar
  10. Coleman HD, Canam T, Kang KY, Ellis DD, Mansfield SD (2007) Over-expression of UDP-glucose pyrophosphorylase in hybrid poplar affects carbon allocation. J Exp Bot 58:4257–4268CrossRefGoogle Scholar
  11. Coleman HD, Yan J, Mansfield SD (2009) Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure. Proc Natl Acad Sci USA 106:13118–13123CrossRefGoogle Scholar
  12. Cronshaw J, Morey PR (1965) Induction of tension wood by 2,3,5-tri-iodobenzoic acid. Nature 205:816–818CrossRefGoogle Scholar
  13. Cronshaw J, Morey P (1968) The effect of plant growth substances on the development of tension wood in horizontally inclined stems of Acer rubrum seedlings. Protoplasma 65:379–391CrossRefGoogle Scholar
  14. Déjardin A, Leplé JC, Lesagedescauses MC, Costa G, Pilate G (2004) Expressed sequence tags from poplar wood tissues—a comparative analysis from multiple libraries. Plant Biol 6:55–64CrossRefGoogle Scholar
  15. Du S, Yamamoto F (2003) A study on the role of calcium in xylem development and compression wood formation in Taxodium distichum seedlings. IAWA J 24:75–85CrossRefGoogle Scholar
  16. Fagerstedt KV, Mellerowicz E, Gorshkova T, Ruel K, Joseleau JP (2014) Cell wall polymers in reaction wood. Springer, BerlinCrossRefGoogle Scholar
  17. Felten J, Vahala J, Love J, Gorzsás A, Rüggeberg M, Delhomme N, Leśniewska J, Kangasjärvi J, Hvidsten TR, Mellerowicz EJ, Sundberg B (2018) Ethylene signaling induces gelatinous layers with typical features of tension wood in hybrid aspen. New Phytol 218:999–1014CrossRefGoogle Scholar
  18. Funada R, Miura T, Shimizu Y, Kinase T, Nakaba S, Kubo T, Sano Y (2008) Gibberellin-induced formation of tension wood in angiosperm trees. Planta 227:1409–1414CrossRefGoogle Scholar
  19. Gerttula S, Zinkgraf M, Muday G, Lewis D, Ibatullin FM, Brumer H, Hart F, Mansfield SD, Filkov V, Groover A (2015) Transcriptional and hormonal regulation of gravitropism of woody stems in Populus. Plant Cell 27:2800–2813Google Scholar
  20. Ghislain B, Clair B (2017) Diversity in the organisation and lignification of tension wood fibre walls—a review. IAWA J 38:245–265CrossRefGoogle Scholar
  21. Ghislain B, Nicolini EA, Romain R, Ruelle J, Yoshinaga A, Alford MH, Clair B (2016) Multilayered structure of tension wood cell walls in Salicaceae sensu lato and its taxonomic significance. Bot J Linn Soc 182:744–756CrossRefGoogle Scholar
  22. Gorshkova TA, Gurjanov OP, Mikshina PV, Ibragimova NN, Mokshina NE, Salnikov VV, Ageeva MV, Amenitskii SI, Chernova TE, Chemikosova SB (2010) Specific type of secondary cell wall formed by plant fibers. Russ J Plant Physiol 57:328–341CrossRefGoogle Scholar
  23. Gorshkova T, Mokshina N, Chernova T, Ibragimova N, Salnikov V, Mikshina P, Tryfona T, Banasiak A, Immerzeel P, Dupree P (2015) Aspen tension wood fibers contain β-(1 → 4)-galactans and acidic arabinogalactans retained by cellulose microfibrils in gelatinous walls. Plant Physiol 169:2048–2063Google Scholar
  24. Goswami L, Dunlop JW, Jungnikl K, Eder M, Gierlinger N, Coutand C, Jeronimidis G, Fratzl P, Burgert I (2008) Stress generation in the tension wood of poplar is based on the lateral swelling power of the G-layer. Plant J 56:531–538CrossRefGoogle Scholar
  25. Gritsch C, Wan Y, Mitchell RA, Shewry PR, Hanley SJ, Karp A (2015) G-fibre cell wall development in willow stems during tension wood induction. J Exp Bot 66:6447–6459CrossRefGoogle Scholar
  26. Hellgren JM, Olofsson K, Sundberg B (2004) Patterns of auxin distribution during gravitational induction of reaction wood in poplar and pine. Plant Physiol 135:212–220CrossRefGoogle Scholar
  27. Hervé C, Rogowski A, Gilbert HJ, Paul KJ (2009) Enzymatic treatments reveal differential capacities for xylan recognition and degradation in primary and secondary plant cell walls. Plant J 58:413–422CrossRefGoogle Scholar
  28. Hossain Z, Mcgarvey B, Amyot L, Gruber M, Jung J, Hannoufa A (2012) DIMINUTO 1 affects the lignin profile and secondary cell wall formation in Arabidopsis. Planta 235:485–498CrossRefGoogle Scholar
  29. Jiang S, Xu K, Wang YZ, Ren YP, Gu S (2008) Role of GA3, GA4 and uniconazole-P in controlling gravitropism and tension wood formation in Fraxinus mandshurica Rupr. var. japonica Maxim. seedlings. J Integr Plant Biol 50:19–28CrossRefGoogle Scholar
  30. Jin H, Do J, Moon D, Noh EW, Kim W, Kwon M (2011) EST analysis of functional genes associated with cell wall biosynthesis and modification in the secondary xylem of the yellow poplar (Liriodendron tulipifera) stem during early stage of tension wood formation. Planta 234:959–977CrossRefGoogle Scholar
  31. Jin H, Do J, Shin SJ, Choi JW, Choi YI, Kim W, Kwon M (2014) Exogenously applied 24-epi brassinolide reduces lignification and alters cell wall carbohydrate biosynthesis in the secondary xylem of Liriodendron tulipifera. Phytochemistry 101:40–51CrossRefGoogle Scholar
  32. Jin YL, Tang RJ, Wang HH, Jiang CM, Bao Y, Yang Y, Liang MX, Sun ZC, Kong FJ, Li B (2017) Overexpression of Populus trichocarpa CYP85A3 promotes growth and biomass production in transgenic trees. Plant Biotechnol J 15:1309–1321CrossRefGoogle Scholar
  33. Kaneda M, Rensing K, Samuels L (2010) Secondary cell wall deposition in developing secondary xylem of poplar. J Integr Plant Biol 52:234–243CrossRefGoogle Scholar
  34. Kim JS, Daniel G (2012) Distribution of glucomannans and xylans in poplar xylem and their changes under tension stress. Planta 236:35–50CrossRefGoogle Scholar
  35. Lafarguette F, Pilate G (2004) Poplar genes encoding fasciclin-like arabinogalactan proteins are highly expressed in tension wood. New Phytol 164:107–121CrossRefGoogle Scholar
  36. Liners F, Letesson JJ, Didembourg C, Cutsem PV (1989) Monoclonal antibodies against pectin recognition of a conformation induced by calcium. Plant Physiol 91:1419–1424CrossRefGoogle Scholar
  37. Liu Z, Persson S, Sánchez-Rodríguez C (2015) At the border: the plasma membrane–cell wall continuum. J Exp Bot 66:1553–1563CrossRefGoogle Scholar
  38. 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 62:689–703CrossRefGoogle Scholar
  39. Marcus SE, Blake AW, Benians TAS, Lee KJD, Poyser C, Donaldson L, Leroux O, Rogowski A, Petersen HL, Boraston A (2010) Restricted access of proteins to mannan polysaccharides in intact plant cell walls. Plant J 64:191–203CrossRefGoogle Scholar
  40. Mauriat M, Leplé JC, Claverol S, Bartholomé J, Negroni L, Richet N, Lalanne C, Bonneu M, Coutand C, Plomion C (2015) Quantitative proteomic and phosphoproteomic approaches for deciphering the signaling pathway for tension wood formation in poplar. J Proteome Res 14:3188–3203CrossRefGoogle Scholar
  41. Mccartney L, Marcus SE, Knox JP (2005) Monoclonal antibodies to plant cell wall xylans and arabinoxylans. J Histochem Cytochem 53:543–546CrossRefGoogle Scholar
  42. Mellerowicz EJ, Gorshkova TA (2012) Tensional stress generation in gelatinous fibres: a review and possible mechanism based on cell-wall structure and composition. J Exp Bot 63:551–565CrossRefGoogle Scholar
  43. Mortimer JC, Miles GP, Brown DM, Zhang Z, Segura MP, Weimar T, Yu X, Seffen KA, Stephens E, Turner SR (2010) Absence of branches from xylan in Arabidopsis gux mutants reveals potential for simplification of lignocellulosic biomass. Proc Natl Acad Sci USA 107:17409–17414CrossRefGoogle Scholar
  44. Nakamoto D, Ikeura A, Asami T, Yamamoto KT (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 141:456–464CrossRefGoogle Scholar
  45. Nawaz F, Naeem M, Zulfiqar B, Akram A, Ashraf MY, Raheel M, Shabbir RN, Hussain RA, Anwar I, Aurangzaib M (2017) Understanding brassinosteroid-regulated mechanisms to improve stress tolerance in plants: a critical review. Environ Sci Pollut R 24:15959–15975CrossRefGoogle Scholar
  46. Oh MH, Kim H, Wu X, Clouse S, Zielinski R, Huber S (2012) Calcium/calmodulin inhibition of the Arabidopsis BRASSINOSTEROID-INSENSITIVE 1 receptor kinase provides a possible link between calcium and brassinosteroid signaling. Biochem J 443:515–523CrossRefGoogle Scholar
  47. Oklestkova J, Rárová L, Kvasnica M, Strnad M (2015) Brassinosteroids: synthesis and biological activities. Phytochem Rev 14:1053–1072CrossRefGoogle Scholar
  48. Rahman A, Takahashi M, Shibasaki K, Wu S, Inaba T, Tsurumi S, Baskin TI (2010) Gravitropism of Arabidopsis thaliana roots requires the polarization of PIN2 toward the root tip in meristematic cortical cells. Plant Cell 22:1762–1776CrossRefGoogle Scholar
  49. Rakusová H, Gallegobartolomé J, Vanstraelen M, Robert HS, Alabadí D, Blázquez MA, Benková E, Friml J (2011) Polarization of PIN3-dependent auxin transport for hypocotyl gravitropic response in Arabidopsis thaliana. Plant J 67:817–826CrossRefGoogle Scholar
  50. Reis D, Vian B (2004) Helicoidal pattern in secondary cell walls and possible role of xylans in their construction. C R Biol 327:785–790CrossRefGoogle Scholar
  51. Ruelle J (2014) Morphology, anatomy and ultrastructure of reaction wood. Springer, New YorkCrossRefGoogle Scholar
  52. Schrick K, Fujioka S, Takatsuto S, Stierhof YD, Stransky H, Yoshida S, Jürgens G (2004) A link between sterol biosynthesis, the cell wall, and cellulose in Arabidopsis. Plant J 38:227–243CrossRefGoogle Scholar
  53. Tocquard T, Lopez D, Decourteix M, Thibaut B, Julien JL, Label P, Leblanc-Fournier N, Roeckel-Drevet P (2013) The molecular mechanisms of reaction wood induction. In: Gardiner B, Barnett J (eds) The biology of reaction. Springer, New York, pp 131–138Google Scholar
  54. Updegraff DM (1969) Semimicro determination of cellulose in biological materials. Anal Biochem 32:420–424CrossRefGoogle Scholar
  55. Vandenbussche F, Suslov D, Grauwe LD, Leroux O, Vissenberg K, Straeten DVD (2011) The role of brassinosteroids in shoot gravitropism. Plant Physiol 156:1331–1336CrossRefGoogle Scholar
  56. Wang C, Zhang N, Gao C, Cui Z, Sun D, Yang C, Wang Y (2014) Comprehensive transcriptome analysis of developing xylem responding to artificial bending and gravitational stimuli in Betula platyphylla. PLoS One 9:e87566CrossRefGoogle Scholar
  57. Wimmer R, Johansson M (2014) Effects of reaction wood on the performance of wood and wood-based products. Springer, BerlinCrossRefGoogle Scholar
  58. Xie L, Yang C, Wang X (2011) Brassinosteroids can regulate cellulose biosynthesis by controlling the expression of CESA genes in Arabidopsis. J Exp Bot 62:4495–4506CrossRefGoogle Scholar
  59. Yu M, Liu K, Liu S, Chen H, Zhou L, Liu Y (2017) Effect of exogenous IAA on tension wood formation by facilitating polar auxin transport and cellulose biosynthesis in hybrid poplar (Populus deltoids × Populus nigra) wood. Holzforschung 71:179–188CrossRefGoogle Scholar
  60. Zhang D, Yang X, Zhang Z, Li B (2010) Expression and nucleotide diversity of the poplar COBL gene. Tree Genet Genomes 6:331–344CrossRefGoogle Scholar
  61. Zhao Y, Qi Z, Berkowitz GA (2013) Teaching an old hormone new tricks: cytosolic Ca2+ elevation involvement in plant brassinosteroid signal transduction cascades. Plant Physiol 163:555–565CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Forestry and Landscape ArchitectureAnhui Agricultural UniversityHefeiPeople’s Republic of China

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