[go: up one dir, main page]
Skip to main content
SpringerLink
Log in

Transcriptome analysis of secondary-wall-enriched seed coat tissues of canola (Brassica napus L.)

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

The seed coat of Brassica napus (canola, oilseed rape) is derived from ovule integuments and contains a layer of palisade cells, which have thick secondary walls. Because cellulosic walls and other indigestible components of the seed coat contribute negatively to the value of oilseeds, efforts are underway to alter seed development. To facilitate these efforts, and to better understand the biology of seed coats, we used a 90,000 element microarray to identify genes whose transcripts were expressed in developing seed coats of B. napus. After dissecting seed coats into three layers, and comparing transcript expression in the middle fraction (which contained the palisade-enriched tissue and bulk of inner integument) to transcript expression in developing hypocotyls, we identified 674 genes whose transcripts were more abundant in the middle fraction of the seed coat. Among these were well-characterized markers of seed coat identity and many genes associated with metabolism of cell wall polysaccharides, flavonoids and various cell wall proteins and transcription factors. Conversely, we identified 1,203 genes whose transcripts were more abundant in the hypocotyl tissue as compared to seed coat, including xylem-specific markers, such as XCP1 and XCP2. We validated 21 of the differentially expressed transcripts using quantitative RT-PCR. The results define a set of transcripts that are highly enriched in the developing seed coat of B. napus.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Similar content being viewed by others

Abbreviations

AGI:

Arabidopsis genome initiative

DAF:

Days after flowering

DPS:

Days post-stratification

GT:

Glycosyltransferase

GH:

Glycosylhydrolase

References

  • Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78

    Article  CAS  PubMed  Google Scholar 

  • Abrahams S, Tanner GJ, Larkin PJ, Ashton AR (2002) Identification and biochemical characterization of mutants in the proanthocyanidin pathway in Arabidopsis. Plant Physiol 130:561–576

    Article  CAS  PubMed  Google Scholar 

  • Arsovski AA, Popma TM, Haughn GW, Carpita NC, McCann MC, Western TL (2009) AtBXL1 encodes a bifunctional beta-d-xylosidase/alpha-l-arabinofuranosidase required for pectic arabinan modification in arabidopsis mucilage secretory cells. Plant Physiol 150:1219–1234

    Article  CAS  PubMed  Google Scholar 

  • Auger B, Baron C, Lucas MO, Vautrin S, Berges H, Chalhoub B, Fautrel A, Renard M, Nesi N (2009) Brassica orthologs from BANYULS belong to a small multigene family, which is involved in procyanidin accumulation in the seed. Planta 230:1167–1183

    Article  CAS  PubMed  Google Scholar 

  • Avci U, Petzold HE, Ismail IO, Beers EP, Haigler CH (2008) Cysteine proteases XCP1 and XCP2 aid micro-autolysis within the intact central vacuole during xylogenesis in Arabidopsis roots. Plant J 56:303–315

    Article  CAS  PubMed  Google Scholar 

  • Baudry A, Heim MA, Dubreucq B, Caboche M, Weisshaar B, Lepiniec L (2004) TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana. Plant J 39:366–380

    Article  CAS  PubMed  Google Scholar 

  • Beeckman T, De Rycke R, Viane R, Inze D (2000) Histological study of seed coat development in Arabidopsis thaliana. J Plant Res 113:139–148

    Article  Google Scholar 

  • Bender J, Fink GR (1998) A Myb homologue, ATR1, activates tryptophan gene expression in Arabidopsis. Proc Natl Acad Sci USA 95:5655–5660

    Article  CAS  PubMed  Google Scholar 

  • Bouman F (1975) Integument initiation and testa development in some Cruciferae. Bot J Linnean Soc 70:213–229

    Google Scholar 

  • Brambilla V, Battaglia R, Colombo M, Masiero S, Bencivenga S, Kater MM, Colombo L (2007) Genetic and molecular interactions between BELL1 and MADS box factors support ovule development in Arabidopsis. Plant Cell 19:2544–2556

    Article  CAS  PubMed  Google Scholar 

  • Cernac A, Andre C, Hoffmann-Benning S, Benning C (2006) WRI1 is required for seed germination and seedling establishment. Plant Physiol 141:745–757

    Article  CAS  PubMed  Google Scholar 

  • Coutinho PM, Starn M, Blanc E, Henrissat B (2003) Why are there so many carbohydrate-active enzyme-related genes in plants? Trends Plant Sci 8:563–565

    Article  CAS  PubMed  Google Scholar 

  • Dean GH, Zheng HQ, Tewari J, Huang J, Young DS, Hwang YT, Western TL, Carpita NC, McCann MC, Mansfield SD, Haughn G (2007) The Arabidopsis MUM2 gene encodes a beta-galactosidase required for the production of seed coat mucilage with correct hydration properties. Plant Cell 19:4007–4021

    Article  CAS  PubMed  Google Scholar 

  • Debeaujon I, Lepiniec L, Pourcel L, Routaboul JM (2007) Seed coat development and dormancy. In: Bradford KJ, Nonogaki H (eds) Seed development, dormancy and germination. Blackwell, Oxford, pp 25–49

    Chapter  Google Scholar 

  • Desprez T, Juraniec M, Crowell EF, Jouy H, Pochylova Z, Parcy F, Hofte H, Gonneau M, Vernhettes S (2007) Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 104:15572–15577

    Article  CAS  PubMed  Google Scholar 

  • Dixon RA, Xie DY, Sharma SB (2005) Proanthocyanidins—a final frontier in flavonoid research? New Phytol 165:9–28

    Article  CAS  PubMed  Google Scholar 

  • Doblin M, Vergara C, Read SEN, Bacic A (2003) Plant cell wall biosynthesis: making the bricks. Blackwell Publishing, Oxford

  • Esau K (1977) Anatomy of seed plants. In: Anatomy of seed plants. Wiley, New York, pp xvi + 550

  • Friedrichsen DM, Nemhauser J, Muramitsu T, Maloof JN, Alonso J, Ecker JR, Furuya M, Chory J (2002) Three redundant brassinosteroid early response genes encode putative bHLH transcription factors required for normal growth. Genetics 162:1445–1456

    CAS  PubMed  Google Scholar 

  • Gonzalez A, Mendenhall J, Huo Y, Lloyd A (2009) TTG1 complex MYBs, MYB5 and TT2, control outer seed coat differentiation. Dev Biol 325:412–421

    Article  CAS  PubMed  Google Scholar 

  • Goujon T, Minic Z, El Amrani A, Lerouxel O, Aletti E, Lapierre C, Joseleau JP, Jouanin L (2003) AtBXL1, a novel higher plant (Arabidopsis thaliana) putative beta-xylosidase gene, is involved in secondary cell wall metabolism and plant development. Plant J 33:677–690

    Article  CAS  PubMed  Google Scholar 

  • Guo AY, He K, Liu D, Bai SN, Gu XC, Wei LP, Luo JC (2005) DATF: a database of Arabidopsis transcription factors. Bioinformatics 21:2568–2569

    Article  CAS  PubMed  Google Scholar 

  • Haughn G, Chaudhury A (2005) Genetic analysis of seed coat development in Arabidopsis. Trends Plant Sci 10:472–477

    Article  CAS  PubMed  Google Scholar 

  • Henrissat B, Coutinho PM, Davies GJ (2001) A census of carbohydrate-active enzymes in the genome of Arabidopsis thaliana. Plant Mol Biol 47:55–72

    Article  CAS  PubMed  Google Scholar 

  • Hobson N, Roach MJ, Deyholos MK (2010) Gene expression in tension wood and bast fibres. Russian J Plant Physiol 57, (in press)

  • Huang Y, Chen L, Wang LP, Vijayan K, Phan S, Liu ZY, Wan LL, Ross A, Xiang DQ, Datla R, Pan YL, Zou JT (2009) Probing the endosperm gene expression landscape in Brassica napus. BMC Genomics 10:256

    Google Scholar 

  • Jiang YQ, Deyholos MK (2009) Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol 69:91–105

    Article  CAS  PubMed  Google Scholar 

  • Kunieda T, Mitsuda N, Ohme-Takagi M, Takeda S, Aida M, Tasaka M, Kondo M, Nishimura M, Hara-Nishimura I (2008) NAC family proteins NARS1/NAC2 and NARS2/NAM in the outer integument regulate embryogenesis in Arabidopsis. Plant Cell 20:2631–2642

    Article  CAS  PubMed  Google Scholar 

  • Le J, Vandenbussche F, De Cnodder T, Van Der Straeten D, Verbelen JP (2005) Cell elongation and microtubule behavior in the Arabidopsis hypocotyl: responses to ethylene and auxin. J Plant Growth Regul 24:166–178

    Article  CAS  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 

  • Lepiniec L, Debeaujon I, Routaboul JM, Baudry A, Pourcel L, Nesi N, Caboche M (2006) Genetics and biochemistry of seed flavonoids. Ann Rev Plant Biol 57:405–430

    Article  CAS  Google Scholar 

  • Li SF, Milliken ON, Pham H, Seyit R, Napoli R, Preston J, Koltunow AM, Parisha RW (2009) The Arabidopsis MYB5 transcription factor regulates mucilage synthesis, seed coat development, and trichome morphogenesis. Plant Cell 21:72–89

    Article  CAS  PubMed  Google Scholar 

  • Lorenzo O, Chico JM, Sanchez-Serrano JJ, Solano R (2004) Jasmonate-insensitive 1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16:1938–1950

    Article  CAS  PubMed  Google Scholar 

  • Luo M, Bilodeau P, Dennis ES, Peacock WJ, Chaudhury A (2000) Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proc Natl Acad Sci USA 97:10637–10642

    Google Scholar 

  • Macquet A, Ralet MC, Loudet O, Kronenberger J, Mouille G, Marion-Poll A, North HM (2007) A naturally occurring mutation in an Arabidopsis accession affects a beta-d-galactosidase that increases the hydrophilic potential of rhamnogalacturonan I in seed mucilage. Plant Cell 19:3990–4006

    Article  CAS  PubMed  Google Scholar 

  • Matsui K, Hiratsu K, Koyama T, Tanaka H, Ohme-Takagi M (2005) A chimeric AtMYB23 repressor induces hairy roots, elongation of leaves and stems, and inhibition of the deposition of mucilage on seed coats in Arabidopsis. Plant Cell Physiol 46:147–155

    Article  CAS  PubMed  Google Scholar 

  • Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Ann Rev Plant Biol 59:595–624

    Article  CAS  Google Scholar 

  • Mikshina PV, Chemikosova SB, Mokshina NE, Ibragimova NN, Gorshkova TA (2009) Free galactose and galactosidase activity in the course of flax fiber development. Russian J Plant Physiol 56:58–67

    Article  CAS  Google Scholar 

  • Minic Z, Jouanin L (2006) Plant glycoside hydrolases involved in cell wall polysaccharide degradation. Plant Physiol Biochem 44:435–449

    Article  CAS  PubMed  Google Scholar 

  • Moise JA, Han S, Gudynaite-Savitch L, Johnson DA, Miki BLA (2005) Seed coats: structure, development, composition, and biotechnology. In Vitro Cell Dev Biol Plant 41:620–644

    Article  Google Scholar 

  • Nakaune S, Yamada K, Kondo M, Kato T, Tabata S, Nishimura M, Hara-Nishimura I (2005) A vacuolar processing enzyme, delta VPE, is involved in seed coat formation at the early stage of seed development. Plant Cell 17:876–887

    Article  CAS  PubMed  Google Scholar 

  • Ng M, Yanofsky MF (2001) Function and evolution of the plant MADS-box gene family. Nat Rev Genet 2:186–195

    Article  CAS  PubMed  Google Scholar 

  • Obermeier C, Hosseini B, Friedt W, Snowdon R (2009) Gene expression profiling via LongSAGE in a non-model plant species: a case study in seeds of Brassica napus. BMC Genomics 10:295

    Google Scholar 

  • Penfield S, Meissner RC, Shoue DA, Carpita NC, Bevan MW (2001) MYB61 is required for mucilage deposition and extrusion in the Arabidopsis seed coat. Plant Cell 13:2777–2791

    Article  CAS  PubMed  Google Scholar 

  • Persson S, Paredez A, Carroll A, Palsdottir H, Doblin M, Poindexter P, Khitrov N, Auer M, Somerville CR (2007) Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc Natl Acad Sci USA 104:15566–15571

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002–2007

    Google Scholar 

  • Richmond TA, Somerville CR (2001) Integrative approaches to determining Csl function. Plant Mol Biol 47:131–143

    Article  CAS  PubMed  Google Scholar 

  • Ringli C, Keller B, Ryser U (2001) Glycine-rich proteins as structural components of plant cell walls. Cell Mol Life Sci 58:1430–1441

    Article  CAS  PubMed  Google Scholar 

  • Roach MJ, Deyholos MK (2008) Microarray analysis of developing flax hypocotyls identifies novel transcripts correlated with specific stages of phloem fibre differentiation. Ann Bot 102:317–330

    Article  CAS  PubMed  Google Scholar 

  • Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carre IA, Coupland G (1998) The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93:1219–1229

    Article  CAS  PubMed  Google Scholar 

  • Seifert GJ, Roberts K (2007) The biology of arabinogalactan proteins. Ann Rev Plant Biol 58:137–161

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4:447–456

    Article  CAS  PubMed  Google Scholar 

  • Swarbreck D, Wilks C, Lamesch P, Berardini TZ, Garcia-Hernandez M, Foerster H, Li D, Meyer T, Muller R, Ploetz L, Radenbaugh A, Singh S, Swing V, Tissier C, Zhang P, Huala E (2008) The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic Acids Res 36:D1009–D1014

    Article  CAS  PubMed  Google Scholar 

  • Szyjanowicz PMJ, McKinnon I, Taylor NG, Gardiner J, Jarvis MC, Turner SR (2004) The irregular xylem 2 mutant is an allele of korrigan that affects the secondary cell wall of Arabidopsis thaliana. Plant J 37:730–740

    Article  CAS  PubMed  Google Scholar 

  • Tanska M, Konopka M, Rotkiewicz D (2008) Relationships of rapeseed strength properties to seed size, colour and coat fibre composition. J Sci Food Agric 88:2186–2193

    Article  CAS  Google Scholar 

  • Toledo-Ortiz G, Huq E, Quail PH (2003) The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15:1749–1770

    Article  CAS  PubMed  Google Scholar 

  • Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116–5121

    Article  CAS  PubMed  Google Scholar 

  • Vancaeseele L, Mills JT, Sumner M, Gillespie R (1982) Cytological study of palisade development in the seed coat of candle canola. Can J Bot Rev Can Bot 60:2469–2475

    Google Scholar 

  • Vaughan JG, Whitehou JM (1971) Seed structure and taxonomy of Cruciferae. Bot J Linnean Soc 64:383–409

    Article  Google Scholar 

  • Wan LL, Xia Q, Qiu X, Selvaraj G (2002) Early stages of seed development in Brassica napus: a seed coat-specific cysteine proteinase associated with programmed cell death of the inner integument. Plant J 30:1–10

    Article  CAS  PubMed  Google Scholar 

  • Western TL, Burn J, Tan WL, Skinner DJ, Martin-McCaffrey L, Moffatt BA, Haughn GW (2001) Isolation and characterization of mutants defective in seed coat mucilage secretory cell development in arabidopsis. Plant Physiol 127:998–1011

    Article  CAS  PubMed  Google Scholar 

  • Wong ML, Medrano JF (2005) Real-time PCR for mRNA quantitation. Biotechniques 39:75–85

    Article  CAS  PubMed  Google Scholar 

  • Xiang D, Cao Y, Schwab D, Sharma N, Nowak J, Links M, Sharpe A, Parkin I, Cutler A, Selvaraj G, Fobert P, Keller W, Bekkaoui F, Datla R (2008) High density Combimatrix Brassica oligo microarray. In: Plant and animal genomes XVI conference, San Diego, CA

  • Xie DY, Sharma SB, Paiva NL, Ferreira D, Dixon RA (2003) Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis. Science 299:396–399

    Article  CAS  PubMed  Google Scholar 

  • Yamashino T, Matsushika A, Fujimori T, Sato S, Kato T, Tabata S, Mizuno T (2003) A link between circadian-controlled bHLH factors and the APRR1/TOC1 quintet in Arabidopsis thaliana. Plant Cell Physiol 44:619–629

    Article  CAS  PubMed  Google Scholar 

  • Ye J, Fang L, Zheng HK, Zhang Y, Chen J, Zhang ZJ, Wang J, Li ST, Li RQ, Bolund L (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:W293–W297

    Article  CAS  PubMed  Google Scholar 

  • Zhao CS, Johnson BJ, Kositsup B, Beers EP (2000) Exploiting secondary growth in Arabidopsis. Construction of xylem and bark cDNA libraries and cloning of three xylem endopeptidases. Plant Physiol 123:1185–1196

    Article  CAS  PubMed  Google Scholar 

  • Zhao CS, Craig JC, Petzold HE, Dickerman AW, Beers EP (2005) The xylem and phloem transcriptomes from secondary tissues of the Arabidopsis root-hypocotyl. Plant Physiol 138:803–818

    Article  CAS  PubMed  Google Scholar 

  • Zhong RQ, Ye ZH (2007) Regulation of cell wall biosynthesis. Curr Opin Plant Biol 10:564–572

    Article  CAS  PubMed  Google Scholar 

  • Zhong RQ, Kays SJ, Schroeder BP, Ye ZH (2002) Mutation of a chitinase-like gene causes ectopic deposition of lignin, aberrant cell shapes, and overproduction of ethylene. Plant Cell 14:165–179

    Article  CAS  PubMed  Google Scholar 

  • Zhong RQ, Lee CH, Zhou JL, McCarthy RL, Ye ZH (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20:2763–2782

    Article  CAS  PubMed  Google Scholar 

  • Zhou J, Lee C, Zhong R, Ye Z-H (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21:248–266. doi:10.1105/tpc.1108.063321

    Google Scholar 

Download references

Acknowledgments

We thank Dr. Mingfeng Yang for technical assistance and Dr. Fred Peng for bioinformatics help, and Plant Biotechnology Institute (Drs. Raju Datla, Faouzi Bekkaoui) for providing the microarrays. The work is funded by Genome Canada and Genome Alberta (M.K.D.).

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Alberta, Edmonton, T6G 2E9, Canada

    Yuanqing Jiang & Michael K. Deyholos

Authors
  1. Yuanqing Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael K. Deyholos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael K. Deyholos.

Additional information

Communicated by M. Jordan.

Microarray data has been deposited in ArrayExpress accession E-MEXP-2103.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jiang, Y., Deyholos, M.K. Transcriptome analysis of secondary-wall-enriched seed coat tissues of canola (Brassica napus L.). Plant Cell Rep 29, 327–342 (2010). https://doi.org/10.1007/s00299-010-0824-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-010-0824-x

Keywords

Search

Navigation