Skip to main content
SpringerLink
Log in

Development of functional modules based on co-expression patterns for cell-wall biosynthesis related genes in rice

  • Original Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

An Erratum to this article was published on 05 August 2016

Abstract

The functional elucidation of plant cell wall biosynthesis (CWB) related genes is important for understanding various stress tolerance responses as well as enhancing biomass in plants. Despite their significant role in physiology and growth of the plant, the function of a limited number of CWB related genes have been identified. Major obstacles such as functional redundancy and limited functional information pose challenges in the characterization of CWB genes. Here, a genome-wide analysis of CWB genes using meta-expression data revealed their roles in stress tolerance and developmental processes. The identification of coexpressed CWB genes suggests functional modules for plant cell wall biosynthesis associated with specific tissue types, biotic stress, abiotic stress, and hormone responses. More interestingly, we identified that glycosyl hydrolases are specialized for root and pollen development, glycosyltransferases for ubiquitous function and leaf development, and carbohydrate esterases for pollen development. A T-DNA insertional mutant of OsCESA9 showing internode preferred expression revealed severe dwarfism and a co-expression network analysis of OsCESA9 in oscesa9 mutant suggest downstream pathways for secondary cell wall biosynthesis and DNA repair processes. Data from our studies will facilitate functional genomic studies of CWB genes in rice and contribute to the enhancement of biomass and yield in crop plants.

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

Similar content being viewed by others

References

  • Adie BA, Perez-Perez J, Perez-Perez MM, Godoy M, Sanchez-Serrano JJ, Schmelz EA, Solano R (2007) ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19:1665–1681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anders N, Wilkinson MD, Lovegrove A, Freeman J, Tryfona T, Pellny TK, Weimar T, Mortimer JC, Stott K, Baker JM, Defoin-Platel M, Shewry PR, Dupree P, Mitchell RA (2012) Glycosyl transferases in family 61 mediate arabinofuranosyl transfer onto xylan in grasses. Proc Natl Acad Sci USA 109:989–993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonateethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barrett T, Troup DB, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM, Muertter RN, Holko M, Ayanbule O, Yefanov A, Soboleva A (2011) NCBI GEO: archive for functional genomics data sets—10 years on. Nucleic Acids Res 39 (Database issue):D1005–1010

    Article  CAS  PubMed  Google Scholar 

  • Brown DM, Zeef LA, Ellis J, Goodacre R, Turner SR (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17:2281–2295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai B, Li CH, Huang J (2014) Systematic identification of cell-wall related genes in Populus based on analysis of functional modules in co-expression network. PLoS One 9:e95176

    Article  PubMed  PubMed Central  Google Scholar 

  • Cao P, Jung K-H, Choi D, Hwang D, Zhu J, Ronald PC (2012) The Rice Oligonucleotide Array Database: an atlas of rice gene expression. Rice 5:17

    Article  PubMed  PubMed Central  Google Scholar 

  • Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30

    Article  CAS  PubMed  Google Scholar 

  • Chandran AKN, Jung KH (2014) Resources for systems biology in rice. J Plant Biol 57:80–92

    Article  CAS  Google Scholar 

  • Cheong YH, Chang HS, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129:661–677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ching A, Dhugga KS, Appenzeller L, Meeley R, Bourett TM, Howard RJ, Rafalski A (2006) Brittle stalk 2 encodes a putative glycosylphosphatidylinositol-anchored protein that affects mechanical strength of maize tissues by altering the composition and structure of secondary cell walls. Planta 224:1174–1184

    Article  CAS  PubMed  Google Scholar 

  • Cruz RPd, Sperotto RA, Cargnelutti D, Adamski JM, de FreitasTerra T, Fett JP (2013) Avoiding damage and achieving cold tolerance in rice plants. Food and Energy Security 2:96–119

    Article  Google Scholar 

  • Dharmawardhana P, Brunner AM, Strauss SH (2010) Genome-wide transcriptome analysis of the transition from primary to secondary stem development in Populus trichocarpa. BMC genomics 11:150

    Article  PubMed  PubMed Central  Google Scholar 

  • Gautier L, Cope L, Bolstad BM, Irizarry RA (2004) affy—analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20:307–315

    Article  CAS  PubMed  Google Scholar 

  • Gille S, Hansel U, Ziemann M, Pauly M (2009) Identification of plant cell wall mutants by means of a forward chemical genetic approach using hydrolases. Proc Natl Acad Sci USA 106:14699–14704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gomez-Porras JL, Riano-Pachon DM, Dreyer I, Mayer JE, Mueller-Roeber B (2007) Genome-wide analysis of ABA-responsive elements ABRE and CE3 reveals divergent patterns in Arabidopsis and rice. BMC genomics 8:260

    Article  PubMed  PubMed Central  Google Scholar 

  • Grennan AK (2006) Genevestigator. Facilitating web-based geneexpression analysis. Plant Physiol 141:1164–1166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamada K, Hongo K, Suwabe K, Shimizu A, Nagayama T, Abe R, Kikuchi S, Yamamoto N, Fujii T, Yokoyama K, Tsuchida H, Sano K, Mochizuki T, Oki N, Horiuchi Y, Fujita M, Watanabe M, Matsuoka M, Kurata N, Yano K (2011) OryzaExpress: an integrated database of gene expression networks and omics annotations in rice. Plant Cell Physiol 52:220–229

    Article  CAS  PubMed  Google Scholar 

  • Hirano K, Aya K, Morinaka Y, Nagamatsu S, Sato Y, Antonio BA, Namiki N, Nagamura Y, Matsuoka M (2013) Survey of genes involved in rice secondary cell wall formation through a coexpression network. Plant Cell Physiol 54:1803–1821

    Article  CAS  PubMed  Google Scholar 

  • Huang FF, Chai CL, Zhang Z, Liu ZH, Dai FY, Lu C, Xiang ZH (2008) The UDP-glucosyltransferase multigene family in Bombyx mori. BMC genomics 9:563

    Article  PubMed  PubMed Central  Google Scholar 

  • Hunter CT, Kirienko DH, Sylvester AW, Peter GF, McCarty DR, Koch KE (2012) Cellulose Synthase-Like D1 is integral to normal cell division, expansion, and leaf development in maize. Plant Physiol 158:708–724

    Article  CAS  PubMed  Google Scholar 

  • Igarashi Y, Yoshiba Y, Takeshita T, Nomura S, Otomo J, Yamaguchi-Shinozaki KKS (2000) Molecular cloning and characterization of a cDNA encoding proline transporter in rice. Plant Cell Physiol 41:750–756

    Article  CAS  PubMed  Google Scholar 

  • Jacobs AK, Lipka V, Burton RA, Panstruga R, Strizhov N, Schulze-Lefert P, Fincher GB (2003) An Arabidopsis Callose Synthase, GSL5, Is Required for Wound and Papillary Callose Formation. Plant Cell 15:2503–2513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeon JS, Lee S, Jung KH, Jun SH, Jeong DH, Lee J, Kim C, Jang S, Yang K, Nam J, An K, Han MJ, Sung RJ, Choi HS, Yu JH, Choi JH, Cho SY, Cha SS, Kim SI, An G (2000) T-DNA insertional mutagenesis for functional genomics in rice. Plant J 22:561–570

    Article  CAS  PubMed  Google Scholar 

  • Jia L, Zhang B, Mao C, Li J, Wu Y, Wu P, Wu Z (2008) OsCYTINV1 for alkaline/neutral invertase is involved in root cell development and reproductivity in rice (Oryza sativa L.). Planta 228:51–59

    Article  CAS  PubMed  Google Scholar 

  • Jung KH, An G, Ronald PC (2008a) Towards a better bowl of rice: assigning function to tens of thousands of rice genes. Nature Rev Genet 9:91–101

    CAS  PubMed  Google Scholar 

  • Jung KH, Jeon JS, An G (2011) Web Tools for Rice Transcriptome Analyses. J Plant Biol 54:65–80

    Article  CAS  Google Scholar 

  • Jung KH, Lee J, Dardick C, Seo YS, Cao P, Canlas P, Phetsom J, Xu X, Ouyang S, An K, Cho YJ, Lee GC, Lee Y, An G, Ronald PC (2008b) Identification and functional analysis of light-responsive unique genes and gene family members in rice. PLoS Genet 4:e1000164

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaplan F, Guy CL (2004) beta-Amylase induction and the protective role of maltose during temperature shock. Plant physiol 135:1674–1684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim CM, Park SH, Je BI, Park SH, Park SJ, Piao HL, Eun MY, Dolan L, Han CD (2007) OsCSLD1, a cellulose synthase-like D1 gene, is required for root hair morphogenesis in rice. Plant Physiol 143:1220–1230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kotake T, Aohara T, Hirano K, Sato A, Kaneko Y, Tsumuraya Y, Takatsuji H, Kawasaki S (2011) Rice Brittle culm 6 encodes a dominant-negative form of CesA Protein that perturbs cellulose synthesis in secondary cell walls. J Exp Bot 62:2053–2062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lerouxel O, Choo TS, Seveno M, Usadel B, Faye L, Lerouge P, Pauly M (2002) Rapid structural phenotyping of plant cell wall mutants by enzymatic oligosaccharide fingerprinting. Plant Physiol 130:1754–1763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li R, Sosa J, Zavala M (2000) Accumulation of zeatin Oglycosyltransferase in Phaseolus vulgaris and Zea mays following cold stress. Plant Growth Regul 32:295–305

    Article  CAS  Google Scholar 

  • Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42 (Database issue):D490–495

    Article  CAS  PubMed  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 

  • Mutwil M, Ruprecht C, Giorgi FM, Bringmann M, Usadel B, Persson S (2009) Transcriptional wiring of cell wall-related genes in Arabidopsis. Mol Plant 2:1015–1024

    Article  CAS  PubMed  Google Scholar 

  • Nguyen MX, Moon S, Jung KH (2013) Genome-wide expression analysis of rice aquaporin genes and development of a functional gene network mediated by aquaporin expression in roots. Planta 238:669–681

    Article  CAS  PubMed  Google Scholar 

  • O'Brien JA, Benkova E (2013) Cytokinin cross-talking during biotic and abiotic stress responses. Front Plant Sci 4:451

    PubMed  PubMed Central  Google Scholar 

  • Oikawa A, Joshi HJ, Rennie EA, Ebert B, Manisseri C, Heazlewood JL, Scheller HV (2010) An integrative approach to the identification of Arabidopsis and rice genes involved in xylan and secondary wall development. PLoS One 5:e15481

    Article  PubMed  PubMed Central  Google Scholar 

  • Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell CR (2007) The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res 35 (Database issue):D883–887

    Article  CAS  PubMed  Google Scholar 

  • Pauly M, Keegstra K (2010) Plant cell wall polymers as precursors for biofuels. Curr Opin Plant Biol 13:305–312

    Article  CAS  PubMed  Google Scholar 

  • Ruprecht C, Persson S (2012) Co-expression of cell-wall related genes: new tools and insights. Front Plant Sci 3:83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santino A, Taurino M, De Domenico S, Bonsegna S, Poltronieri P, Pastor V, Flors V (2013) Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses. Plant Cell Rep 32:1085–1098

    Article  CAS  PubMed  Google Scholar 

  • Sato Y, Antonio BA, Namiki N, Takehisa H, Minami H, Kamatsuki K, Sugimoto K, Shimizu Y, Hirochika H, Nagamura Y (2011) RiceXPro: a platform for monitoring gene expression in japonica rice grown under natural field conditions. Nucleic Acids Res 39 (Database issue):D1141–1148

    Article  CAS  PubMed  Google Scholar 

  • Sato Y, Namiki N, Takehisa H, Kamatsuki K, Minami H, Ikawa H, Ohyanagi H, Sugimoto K, Itoh J, Antonio BA, Nagamura Y (2013) RiceFREND: a platform for retrieving coexpressed gene networks in rice. Nucleic Acids Res 41 (Database issue):D1214–1221

    Article  CAS  PubMed  Google Scholar 

  • Satoh H, Shibahara K, Tokunaga T, Nishi A, Tasaki M, Hwang SK, Okita TW, Kaneko N, Fujita N, Yoshida M, Hosaka Y, Sato A, Utsumi Y, Ohdan T, Nakamura Y (2008) Mutation of the plastidial alpha-glucan phosphorylase gene in rice affects the synthesis and structure of starch in the endosperm. Plant Cell 20:1833–1849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schindelman G, Morikami A, Jung J, Baskin T, Carpita N, Derbyshire P, McCann M, Benfey P (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  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi L, Kent R, Bence N AB B (1997) Developmental expression of a DNA repair gene in Arabidopsis. Mutat Res 384:145–156

    Article  CAS  PubMed  Google Scholar 

  • Shimada A, Ueguchi-Tanaka M, Sakamoto T, Fujioka S, Takatsuto S, Yoshida S, Sazuka T, Ashikari M, Matsuoka M (2006) The rice SPINDLY gene functions as a negative regulator of gibberellin signaling by controlling the suppressive function of the DELLA protein, SLR1, and modulating brassinosteroid synthesis. Plant J 48:390–402

    Article  CAS  PubMed  Google Scholar 

  • Smekalova V, Doskocilova A, Komis G, Samaj J (2014) Crosstalk between secondary messengers, hormones and MAPK modules during abiotic stress signalling in plants. Biotech Adv 32:2–11

    Article  CAS  Google Scholar 

  • Sorrells ME, La Rota M, Bermudez-Kandianis CE, Greene RA, Kantety R, Munkvold JD, Miftahudin, Mahmoud A, Ma X, Gustafson PJ, Qi LL, Echalier B, Gill BS, Matthews DE, Lazo GR, Chao S, Anderson OD, Edwards H, Linkiewicz AM, Dubcovsky J, et al. (2003) Comparative DNA sequence analysis of wheat and rice genomes. Genome Res 13:1818–1827

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian GW, Chen MH, Zaltsman A, Citovsky V (2006) Pollen specific pectin methylesterase involved in pollen tube growth. Dev Biol 294:83–91

    Article  CAS  PubMed  Google Scholar 

  • Tyler L, Bragg JN, Wu J, Yang X, Tuskan GA, Vogel JP (2010) Annotation and comparative analysis of the glycoside hydrolase genes in Brachypodium distachyon. BMC genomics 11:600

    Article  PubMed  PubMed Central  Google Scholar 

  • Umemura K, Satou J, Iwata M, Uozumi N, Koga J, Kawano T, Koshiba T, Anzai H, Mitomi M (2009) Contribution of salicylic acid glucosyltransferase, OsSGT1, to chemically induced disease resistance in rice plants. Plant J 57:463–472

    Article  CAS  PubMed  Google Scholar 

  • Vega-Sanchez ME, Verhertbruggen Y, Christensen U, Chen X, Sharma V, Varanasi P, Jobling SA, Talbot M, White RG, Joo M, Singh S, Auer M, Scheller HV, Ronald PC (2012) Loss of Cellulose synthase-like F6 function affects mixed-linkage glucan deposition, cell wall mechanical properties, and defense responses in vegetative tissues of rice. Plant Physiol 159:56–69

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • von Schweinichen C, Büttner M (2005) Expression of a plant cell wall invertase in roots of Arabidopsis leads to early flowering and an increase in whole plant biomass. Plant Biol (Stuttg) 7:469–475

    Article  Google Scholar 

  • Wang C, Li S, Ng S, Zhang B, Zhou Y, Whelan J, Wu P, Shou H (2014a) Mutation in xyloglucan 6-xylosytransferase results in abnormal root hair development in Oryza sativa. J Exp Bot 65:4149–4157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Li E, Porth I, Chen JG, Mansfield SD, Douglas CJ (2014b) Regulation of secondary cell wall biosynthesis by poplar R2R3 MYB transcription factor PtrMYB152 in Arabidopsis. Sci Rep 4:5054

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Xu Y, Li Z, Zhang S, Lim JM, Lee KO, Li C, Qian Q, Jiang de A, Qi Y (2014c) OsMOGS is required for N-glycan formation and auxin-mediated root development in rice (Oryza sativa L.). Plant J 78:632–645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu B, Zhang B, Dai Y, Zhang L, Shang-Guan K, Peng Y, Zhou Y, Zhu Z (2012) Brittle culm15 encodes a membrane-associated chitinase-like protein required for cellulose biosynthesis in rice. Plant Physiol 159:1440–1452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiang Y, Tang N, Du H, Ye H, Xiong L (2008) Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol 148:1938–1952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie B, Deng Y, Kanaoka MM, Okada K, Hong Z (2012) Expression of Arabidopsis callose synthase 5 results in callose accumulation and cell wall permeability alteration. Plant Sci 183:1–8

    Article  CAS  PubMed  Google Scholar 

  • Xin Z, Wang Q, Yu Z, Hu L, Li J, Xiang C, Wang B, Lou Y (2013) Overexpression of a Xylanase Inhibitor Gene, OsHI-XIP, Enhances Resistance in Rice to Herbivores. Plant Mol Biol Report 32:465–475

    Article  Google Scholar 

  • Yamaguchi T, Hayashi T, Nakayama K, Koike S (2006) Expression analysis of genes for callose synthases and Rho-type small GTPbinding proteins that are related to callose synthesis in rice anther. Biosci Biotechnol Biochem 70:639–645

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto E, Yonemaru JI, Yamamoto T, Yano M (2012) OGRO: The Overview of functionally characterized Genes in Rice online database. Rice 5:1–10

    Article  Google Scholar 

  • Zhang JW, Xu L, Wu YR, Chen XA, Liu Y, Zhu SH, Ding WN, Wu P, Yi KK (2012) OsGLU3, a putative membrane-bound endo-1,4-beta-glucanase, is required for root cell elongation and division in rice (Oryza sativa L.). Mol plant 5:176–186

    Article  PubMed  Google Scholar 

  • Zhong R, Lee C, Ye ZH (2010) Evolutionary conservation of the transcriptional network regulating secondary cell wall biosynthesis. Trends Plant Sci 15:625–632

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University, Yongin, 446-701, Korea

    Anil Kumar Nalini Chandran & Ki-Hong Jung

  2. Department of Plant and Environmental New Resources, Kyung Hee University, Yongin, 446-701, Korea

    Ho Young Jeong & Chanhui Lee

Authors
  1. Anil Kumar Nalini Chandran
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ho Young Jeong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ki-Hong Jung
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chanhui Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Ki-Hong Jung or Chanhui Lee.

Additional information

These authors contributed equally to this work.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chandran, A.K.N., Jeong, H.Y., Jung, KH. et al. Development of functional modules based on co-expression patterns for cell-wall biosynthesis related genes in rice. J. Plant Biol. 59, 1–15 (2016). https://doi.org/10.1007/s12374-016-0461-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-016-0461-1

Key words

Search

Navigation