Skip to main content
SpringerLink
Log in

DIMINUTO 1 affects the lignin profile and secondary cell wall formation in Arabidopsis

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Brassinosteroids (BRs) play a crucial role in plant growth and development and DIMINUTO 1 (DIM1), a protein involved in BR biosynthesis, was previously identified as a cell elongation factor in Arabidopsis thaliana. Through promoter expression analysis, we showed that DIM1 was expressed in most of the tissue types in seedlings and sectioning of the inflorescence stem revealed that DIM1 predominantly localizes to the xylem vessels and in the interfascicular cambium. To investigate the role of DIM1 in cell wall formation, we generated loss-of-function and gain-of-function mutants. Disruption of the gene function caused a dwarf phenotype with up to 38 and 23% reductions in total lignin and cellulose, respectively. Metabolite analysis revealed a significant reduction in the levels of fructose, glucose and sucrose in the loss-of-function mutant compared to the wild type control. The loss-of-function mutant also had a lower S/G lignin monomer ratio relative to wild type, but no changes were detected in the gain-of-function mutant. Phloroglucinol and toluidine blue staining showed a size reduction of the vascular apparatus with smaller and disintegrated xylem vessels in the inflorescence stem of the loss-of-function mutant. Taken together, these data indicate a role for DIM1 in secondary cell wall formation. Moreover, this study demonstrated the potential role of BR hormones in modulating cell wall structure and composition.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

BR:

Brassinosteroid

CesA:

Cellulose synthase

CWR:

Cell wall residue

DIM1:

DIMINUTO 1

GUS:

β-Glucuronidase

MS:

Murashige and Skoog

qPCR:

Quantitative real-time PCR

RNAi:

RNA interference

TGA:

Thioglycolic acid

References

  • Arioli T, Peng L, Betzner AS, Burn J, Wittke W, Herth W, Camilleri C, Höfte H, Plazinski J, Birch R, Cork A, Glover J, Redmond J, Williamson RE (1998) Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279:717–720

    Article  PubMed  CAS  Google Scholar 

  • Bessueille L, Sindt N, Guichardant M, Djerbi S, Teeri TT, Bulone V (2009) Plasma membrane microdomains from hybrid aspen cells are involved in cell wall polysaccharide biosynthesis. Biochem J 420:93–103

    Article  PubMed  CAS  Google Scholar 

  • Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546

    Article  PubMed  CAS  Google Scholar 

  • Bonawitz ND, Chapple C (2010) The genetics of lignin biosynthesis: connecting genotype to phenotype. Annu Rev Genet 44:337–363

    Article  PubMed  CAS  Google Scholar 

  • Brinkmann K, Blaschke L, Polle A (2002) Comparison of different methods for lignin determination as a basis for calibration of near-infrared reflectance spectroscopy and implications of lignoproteins. J Chem Ecol 28:2483–2501

    Article  PubMed  CAS  Google Scholar 

  • Catterou M, Dubois F, Schaller H, Aubanelle L, Vilcot B, Sangwan-Norreel BS, Sangwan RS (2001) Brassinosteroids, microtubules and cell elongation in Arabidopsis thaliana. II. Effects of brassinosteroids on microtubules and cell elongation in the bul1 mutant. Planta 212:673–683

    Article  PubMed  CAS  Google Scholar 

  • Choe S, Dilkes BP, Gregory BD, Ross AS, Yuan H, Noguchi T, Fujioka S, Takatsuto S, Tanaka A, Yoshida S, Tax FE, Feldmann KA (1999) The Arabidopsis dwarf1 mutant is defective in the conversion of 24-methylenecholesterol to campesterol in brassinosteroid biosynthesis. Plant Physiol 119:897–907

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Clouse SD (2000) Plant development: a role for sterols in embryogenesis. Curr Biol 10:R601–R604

    Article  PubMed  CAS  Google Scholar 

  • Clouse SD, Langford M, McMorris TC (1996) A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol 111:671–678

    Article  PubMed  CAS  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861

    Article  PubMed  CAS  Google Scholar 

  • Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133:462–469

    Article  PubMed  CAS  Google Scholar 

  • De Bolt S, Scheible W-R, Schrick K, Auer M, Beisson F, Bischoff V, Bouvier-Navé P, Carroll A, Hematy K, Li Y, Milne J, Nair M, Schaller H, Zemla M, Somerville C (2009) Mutations in UDP-glucose:sterol glucosyltransferase in Arabidopsis cause transparent testa phenotype and suberization defect in seeds. Plant Physiol 151:78–87

    Article  Google Scholar 

  • Dello Ioio R, Nakamura K, Moubayidin L, Perilli S, Taniguchi M, Morita MT, Aoyama T, Costantino P, Sabatini S (2008) A genetic framework for the control of cell division and differentiation in the root meristem. Science 322:1380–1384

    Article  PubMed  CAS  Google Scholar 

  • Endler A, Persson S (2011) Cellulose synthases and synthesis in Arabidopsis. Mol Plant 4:199–211

    Article  PubMed  CAS  Google Scholar 

  • Endo S, Pesquet E, Yamaguchi M, Tashiro G, Sato M, Toyooka K, Nishikubo N, Udagawa-Motose M, Kubo M, Fukuda H, Demura T (2009) Identifying new components participating in the secondary cell wall formation of vessel elements in Zinnia and Arabidopsis. Plant Cell 21:1155–1165

    Article  PubMed  CAS  Google Scholar 

  • Foster CE, Martin TM, Pauly M (2010) Comprehensive compositional analysis of plant cell walls (lignocellulosic biomass) Part I: Lignin. JoVE 37 http://www.jove.com/index/Details.stp?ID=1745. doi: 10.3791/1745

  • Fujioka S, Yokota T (2003) Biosynthesis and metabolism of brassinosteroids. Annu Rev Plant Biol 54:137–164

    Article  PubMed  CAS  Google Scholar 

  • Fujioka S, Li J, Choi YH, Seto H, Takatsuto S, Noguchi T, Watanabe T, Kuriyama H, Yokota T, Chory J, Sakurai A (1997) The Arabidopsis deetiolated2 mutant is blocked early in brassinosteroid biosynthesis. Plant Cell 9:1951–1962

    Article  PubMed  CAS  Google Scholar 

  • Genovesi V, Fornale S, Fry SC, Ruel K, Ferrer P, Encina A, Sonbol FM, Puigdomènech P, Rigau J, Caparrós-Ruiz D (2008) ZmXTH1, a new xyloglucan endotransglucosylase/hydrolase in maize, affects cell wall structure and composition in Arabidopsis thaliana. J Exp Bot 59:875–889

    Article  PubMed  CAS  Google Scholar 

  • Gray WM (2004) Hormonal regulation of plant growth and development. PLoS Biol 2:e311

    Article  PubMed  Google Scholar 

  • Gu Y, Kaplinsky N, Bringmann M, Cobb A, Carroll A, Sampathkumar A, Baskin TI, Persson S, Somerville CR (2010) Identification of a cellulose synthase-associated protein required for cellulose biosynthesis. Proc Natl Acad Sci USA 107:12866–12871

    Article  PubMed  Google Scholar 

  • Halliday KJ (2004) Plant hormones: the interplay of brassinosteroids and auxin. Curr Biol 14:R1008–R1010

    Article  PubMed  CAS  Google Scholar 

  • Hardtke CS (2007) Transcriptional auxin-brassinosteroid crosstalk: who’s talking? BioEssays 29:1115–1123

    Article  PubMed  CAS  Google Scholar 

  • Hobbie L, Estelle M (1994) Genetic approaches to auxin action. Plant Cell Environ 17:525–540

    Article  PubMed  CAS  Google Scholar 

  • Karimi M, Inzé D, Depicker A (2002) Gateway vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193–195

    Article  PubMed  CAS  Google Scholar 

  • Kauschmann A, Jessop A, Koncz C, Szekeres M, Willmitzer L, Altmann T (1996) Genetic evidence for an essential role of brassinosteroids in plant development. Plant J 9:701–713

    Article  CAS  Google Scholar 

  • Kim HB, Kwon M, Ryu H, Fujioka S, Takatsuto S, Yoshida S, An CS, Lee I, Hwang I, Choe S (2006) The regulation of DWARF4 expression is likely a critical mechanism in maintaining the homeostasis of bioactive brassinosteroids in Arabidopsis. Plant Physiol 140:548–557

    Article  PubMed  CAS  Google Scholar 

  • Klahre U, Noguchi T, Fujioka S, Takatsuto S, Yokota T, Nomura T, Yoshida S, Chua NH (1998) The Arabidopsis DIMINUTO/DWARF1 gene encodes a protein involved in steroid synthesis. Plant Cell 10:1677–1690

    Article  PubMed  CAS  Google Scholar 

  • Lapierre C, Monties B, Rolando C (1985) Thioacidolysis of lignin: comparison with acidolysis. J Wood Chem Technol 5:277–292

    Article  CAS  Google Scholar 

  • Li X, Weng J-K, Chapple C (2008) Improvement of biomass through lignin modification. Plant J 54:569–581

    Article  PubMed  CAS  Google Scholar 

  • Li X, Ximenes E, Kim Y, Slininger M, Meilan R, Ladisch M, Chapple C (2010) Lignin monomer composition affects Arabidopsis cell-wall degradability after liquid hot water pretreatment. Biotechnol Biofuels 3:27

    Article  PubMed  CAS  Google Scholar 

  • Liscum E, Reed JW (2002) Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol 49:387–400

    Article  PubMed  CAS  Google Scholar 

  • Mussig C (2005) Brassinosteroid-promoted growth. Plant Biol (Stuttg.) 7:110–117

    Article  CAS  Google Scholar 

  • Nemhauser JL, Mockler TC, Chory J (2004) Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol 2:e258

    Article  PubMed  Google Scholar 

  • Pagant S, Bichet A, Sugimoto K, Lerouxel O, Desprez T, McCann M, Lerouge P, Vernhettes S, Höfte H (2002) KOBITO1 encodes a novel plasma membrane protein necessary for normal synthesis of cellulose during cell expansion in Arabidopsis. Plant Cell 14:2001–2013

    Article  PubMed  CAS  Google Scholar 

  • Peña MJ, Zhong R, Zhou GK, Richardson EA, O’Neill MA, Darvill AG, York WS, Ye ZH (2007) Arabidopsis irregular xylem8 and irregular xylem9: implications for the complexity of glucuronoxylan biosynthesis. Plant Cell 19:549–563

    Article  PubMed  Google Scholar 

  • Peng L, Kawagoe Y, Hogan P, Delmer D (2002) Sitosterol-β-glucoside as primer for cellulose synthesis in plants. Science 295:147–150

    Article  PubMed  CAS  Google Scholar 

  • Persson S, Caffall KH, Freshour G, Hilley MT, Bauer S, Poindexter P, Hahn MG, Mohnen D, Somerville C (2007) The Arabidopsis irregular xylem8 mutant is deficient in glucuronoxylan and homogalacturonan, which are essential for secondary cell wall integrity. Plant Cell 19:237–255

    Article  PubMed  CAS  Google Scholar 

  • Raes J, Rohde A, Christensen JH, Van de Peer Y, Boerjan W (2003) Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiol 133:1051–1071

    Article  PubMed  CAS  Google Scholar 

  • Ramakers C, Ruijter JM, Deprez RH, Moorman AF (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66

    Article  PubMed  CAS  Google Scholar 

  • Salas Fernandez MG, Becraft PW, Yin Y, Lübberstedt T (2009) From dwarves to giants? Plant height manipulation for biomass yield. Trends Plant Sci 14:454–461

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Rodríguez C, Rubio-Somoza I, Sibout R, Persson S (2010) Phytohormones and the cell wall in Arabidopsis during seedling growth. Trends Plant Sci 15:291–301

    Article  PubMed  Google Scholar 

  • Sato S, Kato T, Kakegawa K, Ishii T, Liu YG, Awano T, Takabe K, Nishiyama Y, Kuga S, Sato S, Nakamura Y, Tabata S, Shibata D (2001) Role of the putative membrane-bound endo-1,4-glucanase KORRIGAN in cell elongation and cellulose synthesis in Arabidopsis thaliana. Plant Cell Physiol 42:251–263

    Article  PubMed  CAS  Google Scholar 

  • Schindelman G, Morikami A, Jung J, Baskin TI, Carpita NC, Derbyshire P, McCann MC, Benfey PN (2001) COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes Dev 15:1115–1127

    Article  PubMed  CAS  Google Scholar 

  • Schmidt MA, Barbazuk WB, Sandford M, May G, Song Z, Zhou W, Nikolau BJ, Herman EM (2011) Silencing of soybean seed storage proteins results in a rebalanced protein composition preserving seed protein content without major collateral changes in the metabolome and transcriptome. Plant Physiol 156:330–345

    Article  PubMed  CAS  Google Scholar 

  • Schrick K, Fujioka S, Takatsuto S, Stierhof Y-D, Stransky H, Yoshida S, Jürgens G (2004) A link between sterol biosynthesis, the cell wall, and cellulose in Arabidopsis. Plant J 38:227–243

    Article  PubMed  CAS  Google Scholar 

  • Somerville C (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22:53–78

    Article  PubMed  CAS  Google Scholar 

  • Sonbol FM, Fornalé S, Capellades M, Encina A, Touriño S, Torres JL, Rovira P, Ruel K, Puigdomènech P, Rigau J, Caparrós-Ruizet D (2009) The maize ZmMYB42 represses the phenylpropanoid pathway and affects the cell wall structure, composition and degradability in Arabidopsis thaliana. Plant Mol Biol 70:283–296

    Article  PubMed  CAS  Google Scholar 

  • Szekeres M, Németh K, Koncz-Kálmán Z, Mathur J, Kauschmann A, Altmann T, Rédei GP, Nagy F, Schell J, Koncz C (1996) Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85:171–182

    Article  PubMed  CAS  Google Scholar 

  • Takahashi T, Gasch A, Nishizawa N, Chua NH (1995) The DIMINUTO gene of Arabidopsis is involved in regulating cell elongation. Genes Dev 9:97–107

    Article  PubMed  CAS  Google Scholar 

  • Updegraff DM (1969) Semimicro determination of cellulose in biological materials. Anal Biochem 32:420–424

    Article  PubMed  CAS  Google Scholar 

  • Vandenbussche F, Verbelen J-P, Van Der Straeten D (2005) Of light and length: regulation of hypocotyl growth in Arabidopsis. BioEssays 27:275–284

    Article  PubMed  CAS  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.1–0034.11

    Google Scholar 

  • Vert G, Nemhauser JL, Geldner N, Hong F, Chory J (2005) Molecular mechanisms of steroid hormone signaling in plants. Annu Rev Cell Dev Biol 21:177–201

    Article  PubMed  CAS  Google Scholar 

  • Xie L, Yang C, Wang X (2011) Brassinosteroids can regulate cellulose biosynthesis by controlling the expression of CESA genes in Arabidopsis. J Expt Bot. doi:10.1093/jxb/err164

  • Xu W, Purugganan MM, Polisensky DH, Antosiewicz DM, Fry SC, Braam J (1995) Arabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycosylase. Plant Cell 7:1555–1567

    Article  PubMed  CAS  Google Scholar 

  • Zhao Q, Dixon RA (2011) Transcriptional networks for lignin biosynthesis: more complex than we thought? Trends Plant Sci 16:227–233

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by the Agricultural Bioproducts Innovation Program as part of the Cellulosic Biofuel Network, Canada. ZH and JJ were recipients of Visiting Fellowships in Canadian Government Laboratories. We thank Alex Molnar for helping with the figures.

Author information

Author notes

  1. Jinwook Jung

    Present address: Bayer CropScience Ltd, 16F, Sambu B/D, 676 Yoksam-dong, Gangnam-gu, Seoul, 135-979, Korea

Authors and Affiliations

  1. Agriculture and Agri-Food Canada, 1391 Sandford Street, London, ON, N5V 4T3, Canada

    Zakir Hossain, Brian McGarvey, Lisa Amyot, Jinwook Jung & Abdelali Hannoufa

  2. Agriculture and Agri-Food Canada, 107 Science Place, Saskatoon, SK, S7N 0X2, Canada

    Margaret Gruber

Authors
  1. Zakir Hossain
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brian McGarvey
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lisa Amyot
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Margaret Gruber
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jinwook Jung
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Abdelali Hannoufa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abdelali Hannoufa.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 86 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hossain, Z., McGarvey, B., Amyot, L. et al. DIMINUTO 1 affects the lignin profile and secondary cell wall formation in Arabidopsis. Planta 235, 485–498 (2012). https://doi.org/10.1007/s00425-011-1519-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-011-1519-4

Keywords

Search

Navigation