Plant Molecular Biology

, 77:391 | Cite as

Transcriptional dynamics during cell wall removal and regeneration reveals key genes involved in cell wall development in rice

  • Rita Sharma
  • Feng Tan
  • Ki-Hong Jung
  • Manoj K. Sharma
  • Zhaohua Peng
  • Pamela C. RonaldEmail author


Efficient and cost-effective conversion of plant biomass to usable forms of energy requires a thorough understanding of cell wall biosynthesis, modification and degradation. To elucidate these processes, we assessed the expression dynamics during enzymatic removal and regeneration of rice cell walls in suspension cells over time. In total, 928 genes exhibited significant up-regulation during cell wall removal, whereas, 79 genes were up-regulated during cell wall regeneration. Both gene sets are enriched for kinases, transcription factors and genes predicted to be involved in cell wall-related functions. Integration of the gene expression datasets with a catalog of known and/or predicted biochemical pathways from rice, revealed metabolic and hormonal pathways involved in cell wall degradation and regeneration. Rice lines carrying Tos17 mutations in genes up-regulated during cell wall removal exhibit dwarf phenotypes. Many of the genes up-regulated during cell wall development are also up-regulated in response to infection and environmental perturbations indicating a coordinated response to diverse types of stress.


Cell wall Defense response Expression Microarray Protoplast Stress 



MultiExperiment Viewer


Carbohydrate-Active enZymes


Gene expression omnibus


Ethylene response factors


Jasmonic acid




Glycoside hydrolase



This work was supported by a US Department of Energy (DEFG0207ER6445907110980) and USDA (2007355041824007110980) grant to PCR and ZP; an Office of Science, Office of Biological and Environmental Research of the US DOE contract no. DE-AC02-05CH11231 to the Joint BioEnergy Institute and a grant from the Next-Generation BioGreen 21 Program (No. SSAC2011), Rural Development Administration, Republic of Korea to KHJ. We thank Dr. Peijian Cao for helping with data normalization.

Supplementary material

11103_2011_9819_MOESM1_ESM.xls (17 kb)
Online Resource 1. List of quantitative PCR primers used for validation of microarray data. (XLS 17 kb)
11103_2011_9819_MOESM2_ESM.xls (180 kb)
Online Resource 2a. List of genes up-regulated during cell wall removal. 2b. List of genes down-regulated during cell wall removal. (XLS 180 kb)
11103_2011_9819_MOESM3_ESM.xls (52 kb)
Online Resource 3a. List of genes up-regulated during cell wall regeneration. 3b. List of genes down-regulated during cell wall regeneration. (XLS 52 kb)
11103_2011_9819_MOESM4_ESM.eps (1.8 mb)
Online Resource 4. Hierarchical cluster display showing log2 fold changes exhibited by cell wall-related genes during cell wall removal and regeneration. Green represents down-regulation and red signifies up-regulation of genes with respect to suspension cells and protoplasts during cell wall removal and regeneration, respectively. The time points analyzed are shown at the top. S: suspension cell; D1: 2 h; D2: 6 h after enzymatic treatment; P: protoplasts at 0 h on regeneration medium; R1: 4 h; R2: 12 h and R3: 48 h after incubation in regeneration medium. The dendrogram at the left represents hierarchical clustering of genes. The LOCUS IDs of genes are on the right. (EPS 1869 kb)
11103_2011_9819_MOESM5_ESM.xlsx (116 kb)
Online Resource 5. List of genes up-regulated during cell wall removal and different stress treatments. (XLSX 115 kb)
11103_2011_9819_MOESM6_ESM.xlsx (60 kb)
Online Resource 6. List of genes up-regulated during cell wall regeneration and different stress treatments. (XLSX 60 kb)


  1. Alexandrow MG, Hamlin JL (2005) Chromatin decondensation in S-phase involves recruitment of Cdk2 by Cdc45 and histone H1 phosphorylation. J Cell Biol 168:875–886PubMedCrossRefGoogle Scholar
  2. Amstel TNMv, Kengen HMP (1996) Callose deposition in the primary wall of suspension cells and regenerating protoplasts, and its relationship to patterned cellulose synthesis. Can J Bot 74:1040–1049CrossRefGoogle Scholar
  3. Arora R, Agarwal P, Ray S, Singh AK, Singh VP, Tyagi AK, Kapoor S (2007) MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8:242PubMedCrossRefGoogle Scholar
  4. Baluska F, Samaj J, Wojtaszek P, Volkmann D, Menzel D (2003) Cytoskeleton-plasma membrane-cell wall continuum in plants. Emerging links revisited. Plant Physiol 133:482–491PubMedCrossRefGoogle Scholar
  5. Bart RS, Chern M, Vega-Sanchez ME, Canlas P, Ronald PC (2010) Rice Snl6, a cinnamoyl-CoA reductase-like gene family member, is required for NH1-mediated immunity to Xanthomonas oryzae pv. oryzae. PLoS Genet 6:e1001123Google Scholar
  6. Berger JA, Hautaniemi S, Jarvinen AK, Edgren H, Mitra SK, Astola J (2004) Optimized LOWESS normalization parameter selection for DNA microarray data. BMC Bioinformatics 5:194PubMedCrossRefGoogle Scholar
  7. Bonetta DT, Facette M, Raab TK, Somerville CR (2002) Genetic dissection of plant cell-wall biosynthesis. Biochem Soc Trans 30:298–301PubMedCrossRefGoogle Scholar
  8. Bosch M, Mayer CD, Cookson A, Donnison IS (2011) Identification of genes involved in cell wall biogenesis in grasses by differential gene expression profiling of elongating and non-elongating maize internodes. J Exp Bot 62:3545–3561PubMedCrossRefGoogle Scholar
  9. Bouton S, Leboeuf E, Mouille G, Leydecker MT, Talbotec J, Granier F, Lahaye M, Hofte H, Truong HN (2002) QUASIMODO1 encodes a putative membrane-bound glycosyltransferase required for normal pectin synthesis and cell adhesion in Arabidopsis. Plant Cell 14:2577–2590PubMedCrossRefGoogle Scholar
  10. Brett C, Waldron K (1996) Physiology and biochemistry of the plant cell wall. Chapman and Hall, LondonGoogle Scholar
  11. Brummell DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 47:311–340PubMedCrossRefGoogle Scholar
  12. Burgess J (1983) Wall regeneration around isolated protoplasts. Int Rev Cytol 16:55–77Google Scholar
  13. Burgess J, Fleming EN (1974) Ultrastructural observations of cell wall regeneration around isolated tobacco protoplasts. J Cell Sci 14:439–449PubMedGoogle Scholar
  14. Burton RA, Wilson SM, Hrmova M, Harvey AJ, Shirley NJ, Medhurst A, Stone BA, Newbigin EJ, Bacic A, Fincher GB (2006) Cellulose synthase-like CslF genes mediate the synthesis of cell wall (1, 3;1, 4)-beta-D-glucans. Science 311:1940–1942PubMedCrossRefGoogle Scholar
  15. Cano-Delgado A, Penfield S, Smith C, Catley M, Bevan M (2003) Reduced cellulose synthesis invokes lignification and defense responses in Arabidopsis thaliana. Plant J 34:351–362PubMedCrossRefGoogle Scholar
  16. Cao PJ, Bartley LE, Jung KH, Ronald PC (2008) Construction of a rice glycosyltransferase phylogenomic database and identification of rice-diverged glycosyltransferases. Mol Plant 1:858–877PubMedCrossRefGoogle Scholar
  17. Carroll A, Somerville C (2009) Cellulosic biofuels. Annu Rev Plant Biol 60:165–182PubMedCrossRefGoogle Scholar
  18. Cazale AC, Rouet-Mayer MA, Barbier-Brygoo H, Mathieu Y, Lauriere C (1998) Oxidative burst and hypoosmotic stress in tobacco cell suspensions. Plant Physiol 116:659–669PubMedCrossRefGoogle Scholar
  19. Chivasa S, Ndimba BK, Simon WJ, Robertson D, Yu XL, Knox JP, Bolwell P, Slabas AR (2002) Proteomic analysis of the Arabidopsis thaliana cell wall. Electrophoresis 23:1754–1765PubMedCrossRefGoogle Scholar
  20. Cho HT, Cosgrove DJ (2000) Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:9783–9788PubMedCrossRefGoogle Scholar
  21. Chow CW, Davis RJ (2006) Proteins kinases: chromatin-associated enzymes? Cell 127:887–890PubMedCrossRefGoogle Scholar
  22. Cocuron JC, Lerouxel O, Drakakaki G, Alonso AP, Liepman AH, Keegstra K, Raikhel N, Wilkerson CG (2007) A gene from the cellulose synthase-like C family encodes a beta-1,4 glucan synthase. Proc Natl Acad Sci USA 104:8550–8555PubMedCrossRefGoogle Scholar
  23. Dardick C, Ronald P (2006) Plant and animal pathogen recognition receptors signal through non-RD kinases. PLoS Pathog 2:e2PubMedCrossRefGoogle Scholar
  24. Decreux A, Messiaen J (2005) Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol 46:268–278PubMedCrossRefGoogle Scholar
  25. Ellis C, Karafyllidis I, Turner JG (2002a) Constitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae. Mol Plant Microbe Interact 15:1025–1030PubMedCrossRefGoogle Scholar
  26. Ellis C, Karafyllidis I, Wasternack C, Turner JG (2002b) The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. Plant Cell 14:1557–1566PubMedCrossRefGoogle Scholar
  27. Fagard M, Desnos T, Desprez T, Goubet F, Refregier G, Mouille G, McCann M, Rayon C, Vernhettes S, Hofte H (2000) PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell 12:2409–2424PubMedCrossRefGoogle Scholar
  28. Farrokhi N, Burton RA, Brownfield L, Hrmova M, Wilson SM, Bacic A, Fincher GB (2006) Plant cell wall biosynthesis: genetic, biochemical and functional genomics approaches to the identification of key genes. Plant Biotechnol J 4:145–167PubMedCrossRefGoogle Scholar
  29. Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442PubMedCrossRefGoogle Scholar
  30. Fukao T, Xu K, Ronald PC, Bailey-Serres J (2006) A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18:2021–2034PubMedCrossRefGoogle Scholar
  31. Garcia R, Bermejo C, Grau C, Perez R, Rodriguez-Pena JM, Francois J, Nombela C, Arroyo J (2004) The global transcriptional response to transient cell wall damage in Saccharomyces cerevisiae and its regulation by the cell integrity signaling pathway. J Biol Chem 279:15183–15195PubMedCrossRefGoogle Scholar
  32. Guo H, Li L, Ye H, Yu X, Algreen A, Yin Y (2009a) Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc Natl Acad Sci USA 106:7648–7653PubMedCrossRefGoogle Scholar
  33. Guo S, Shen X, Yan G, Ma D, Bai X, Li S, Jiang Y (2009b) A MAP kinase dependent feedback mechanism controls Rho1 GTPase and actin distribution in yeast. PLoS One 4:e6089PubMedCrossRefGoogle Scholar
  34. Harholt J, Jensen JK, Sorensen SO, Orfila C, Pauly M, Scheller HV (2006) ARABINAN DEFICIENT 1 is a putative arabinosyltransferase involved in biosynthesis of pectic arabinan in Arabidopsis. Plant Physiol 140:49–58PubMedCrossRefGoogle Scholar
  35. Hematy K, Hofte H (2008) Novel receptor kinases involved in growth regulation. Curr Opin Plant Biol 11:321–328PubMedCrossRefGoogle Scholar
  36. Hematy K, Sado PE, Van Tuinen A, Rochange S, Desnos T, Balzergue S, Pelletier S, Renou JP, Hofte H (2007) A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr Biol 17:922–931PubMedCrossRefGoogle Scholar
  37. Hernandez-Blanco C, Feng DX, Hu J, Sanchez-Vallet A, Deslandes L, Llorente F, Berrocal-Lobo M, Keller H, Barlet X, Sanchez-Rodriguez C, Anderson LK, Somerville S, Marco Y, Molina A (2007) Impairment of cellulose synthases required for Arabidopsis secondary cell wall formation enhances disease resistance. Plant Cell 19:890–903PubMedCrossRefGoogle Scholar
  38. His I, Driouich A, Nicol F, Jauneau A, Hofte H (2001) Altered pectin composition in primary cell walls of korrigan, a dwarf mutant of Arabidopsis deficient in a membrane-bound endo-1,4-beta-glucanase. Planta 212:348–358PubMedCrossRefGoogle Scholar
  39. Hochholdinger F, Wen TJ, Zimmermann R, Chimot-Marolle P, e Silva O, Bruce W, Lamkey KR, Wienand U, Schnable PS (2008) The maize (Zea mays L.) roothairless 3 gene encodes a putative GPI-anchored, monocot-specific, COBRA-like protein that significantly affects grain yield. Plant J 54:888–898PubMedCrossRefGoogle Scholar
  40. Hoffmann L, Maury S, Martz F, Geoffroy P, Legrand M (2003) Purification, cloning, and properties of an acyltransferase controlling shikimate and quinate ester intermediates in phenylpropanoid metabolism. J Biol Chem 278:95–103PubMedCrossRefGoogle Scholar
  41. Hu X, Li W, Chen Q, Yang Y (2009) Early signal transduction linking the synthesis of jasmonic acid in plant. Plant Signal Behav 4:696–697PubMedCrossRefGoogle Scholar
  42. Humphrey TV, Bonetta DT, Goring DR (2007) Sentinels at the wall: cell wall receptors and sensors. New Phytol 176:7–21PubMedCrossRefGoogle Scholar
  43. Imoto K, Yokoyama R, Nishitani K (2005) Comprehensive approach to genes involved in cell wall modifications in Arabidopsis thaliana. Plant Mol Biol 58:177–192PubMedCrossRefGoogle Scholar
  44. Iraki NM, Bressan RA, Carpita NC (1989a) Extracellular polysaccharides and proteins of tobacco cell cultures and changes in composition associated with growth-limiting adaptation to water and saline stress. Plant Physiol 91:54–61PubMedCrossRefGoogle Scholar
  45. Iraki NM, Bressan RA, Hasegawa PM, Carpita NC (1989b) Alteration of the physical and chemical structure of the primary cell wall of growth-limited plant cells adapted to osmotic stress. Plant Physiol 91:39–47PubMedCrossRefGoogle Scholar
  46. Iraki NM, Singh N, Bressan RA, Carpita NC (1989c) Cell walls of tobacco cells and changes in composition associated with reduced growth upon adaptation to water and saline stress. Plant Physiol 91:48–53PubMedCrossRefGoogle Scholar
  47. Irshad M, Canut H, Borderies G, Pont-Lezica R, Jamet E (2008) A new picture of cell wall protein dynamics in elongating cells of Arabidopsis thaliana: confirmed actors and newcomers. BMC Plant Biol 8:94PubMedCrossRefGoogle Scholar
  48. Jaiswal P, Ni J, Yap I, Ware D, Spooner W, Youens-Clark K, Ren L, Liang C, Zhao W, Ratnapu K, Faga B, Canaran P, Fogleman M, Hebbard C, Avraham S, Schmidt S, Casstevens TM, Buckler ES, Stein L, McCouch S (2006) Gramene: a bird’s eye view of cereal genomes. Nucleic Acids Res 34:D717–D723PubMedCrossRefGoogle Scholar
  49. Jha G, Patel HK, Dasgupta M, Palaparthi M, Sonti RV (2010) Transcriptional profiling of rice leaves undergoing a hypersensitive response like reaction induced by Xanthomonas oryzae pv. Oryzae cellulase Rice 3:1–21Google Scholar
  50. Jones L, Ennos AR, Turner SR (2001) Cloning and characterization of irregular xylem4 (irx4): a severely lignin-deficient mutant of Arabidopsis. Plant J 26:205–216PubMedCrossRefGoogle Scholar
  51. Jung KH, Dardick C, Bartley LE, Cao P, Phetsom J, Canlas P, Seo YS, Shultz M, Ouyang S, Yuan Q, Frank BC, Ly E, Zheng L, Jia Y, Hsia AP, An K, Chou HH, Rocke D, Lee GC, Schnable PS, An G, Buell CR, Ronald PC (2008) Refinement of light-responsive transcript lists using rice oligonucleotide arrays: evaluation of gene-redundancy. PLoS One 3:e3337PubMedCrossRefGoogle Scholar
  52. Jung KH, Jeon JS, An G (2011) Web tools for rice transcriptome analyses. J Plant Biol 54:65–80CrossRefGoogle Scholar
  53. Kwon HK, Yokoyama R, Nishitani K (2005) A proteomic approach to apoplastic proteins involved in cell wall regeneration in protoplasts of Arabidopsis suspension-cultured cells. Plant Cell Physiol 46:843–857PubMedCrossRefGoogle Scholar
  54. Lally D, Ingmire P, Tong HY, He ZH (2001) Antisense expression of a cell wall-associated protein kinase, WAK4, inhibits cell elongation and alters morphology. Plant Cell 13:1317–1331PubMedCrossRefGoogle Scholar
  55. Lee TJ, Shultz RW, Hanley-Bowdoin L, Thompson WF (2004) Establishment of rapidly proliferating rice cell suspension culture and its characterization by fluorescence-activated cell sorting analysis. Plant mol Biol Reporter 22:259–267CrossRefGoogle Scholar
  56. Liepman AH, Wilkerson CG, Keegstra K (2005) Expression of cellulose synthase-like (Csl) genes in insect cells reveals that CslA family members encode mannan synthases. Proc Natl Acad Sci USA 102:2221–2226PubMedCrossRefGoogle Scholar
  57. Lionetti V, Francocci F, Ferrari S, Volpi C, Bellincampi D, Galletti R, D’Ovidio R, De Lorenzo G, Cervone F (2009) Engineering the cell wall by reducing de-methyl-esterified homogalacturonan improves saccharification of plant tissues for bioconversion. Proc Natl Acad Sci USA 107:616–621PubMedCrossRefGoogle Scholar
  58. Lopez-Casado G, Urbanowicz BR, Damasceno CM, Rose JK (2008) Plant glycosyl hydrolases and biofuels: a natural marriage. Curr Opin Plant Biol 11:329–337PubMedCrossRefGoogle Scholar
  59. Lu R, Lee GC, Shultz M, Dardick C, Jung K, Phetsom J, Jia Y, Rice RH, Goldberg Z, Schnable PS, Ronald P, Rocke DM (2008) Assessing probe-specific dye and slide biases in two-color microarray data. BMC Bioinformatics 9:314PubMedCrossRefGoogle Scholar
  60. Manfield IW, Orfila C, McCartney L, Harholt J, Bernal AJ, Scheller HV, Gilmartin PM, Mikkelsen JD, Paul Knox J, Willats WG (2004) Novel cell wall architecture of isoxaben-habituated Arabidopsis suspension-cultured cells: global transcript profiling and cellular analysis. Plant J 40:260–275PubMedCrossRefGoogle Scholar
  61. Marsch-Martinez N, Greco R, Becker JD, Dixit S, Bergervoet JH, Karaba A, de Folter S, Pereira A (2006) BOLITA, an Arabidopsis AP2/ERF-like transcription factor that affects cell expansion and proliferation/differentiation pathways. Plant Mol Biol 62:825–843PubMedCrossRefGoogle Scholar
  62. McQueen-Mason S, Cosgrove DJ (1994) Disruption of hydrogen bonding between plant cell wall polymers by proteins that induce wall extension. Proc Natl Acad Sci USA 91:6574–6578PubMedCrossRefGoogle Scholar
  63. Mitchell RA, Dupree P, Shewry PR (2007) A novel bioinformatics approach identifies candidate genes for the synthesis and feruloylation of arabinoxylan. Plant Physiol 144:43–53PubMedCrossRefGoogle Scholar
  64. Ouyang B, Yang T, Li H, Zhang L, Zhang Y, Zhang J, Fei Z, Ye Z (2007) Identification of early salt stress response genes in tomato root by suppression subtractive hybridization and microarray analysis. J Exp Bot 58:507–520PubMedCrossRefGoogle Scholar
  65. Penning BW, Hunter CT III, Tayengwa R, Eveland AL, Dugard CK, Olek AT, Vermerris W, Koch KE, McCarty DR, Davis MF, Thomas SR, McCann MC, Carpita NC (2009) Genetic resources for maize cell wall biology. Plant Physiol 151:1703–1728PubMedCrossRefGoogle Scholar
  66. Pilling E, Hofte H (2003) Feedback from the wall. Curr Opin Plant Biol 6:611–616PubMedCrossRefGoogle Scholar
  67. Pojnar E, Cocking EC (1967) Cell-wall regeneration by isolated tomato-fruit protoplasts. Biochem J 103:74P–75PPubMedGoogle Scholar
  68. Roudier F, Fernandez AG, Fujita M, Himmelspach R, Borner GH, Schindelman G, Song S, Baskin TI, Dupree P, Wasteneys GO, Benfey PN (2005) COBRA, an Arabidopsis extracellular glycosyl-phosphatidyl inositol-anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. Plant Cell 17:1749–1763PubMedCrossRefGoogle Scholar
  69. Seifert GJ, Blaukopf C (2010) Irritable walls: the plant extracellular matrix and signaling. Plant Physiol 153:467–478PubMedCrossRefGoogle Scholar
  70. Seifert GJ, Barber C, Wells B, Roberts K (2004) Growth regulators and the control of nucleotide sugar flux. Plant Cell 16:723–730PubMedCrossRefGoogle Scholar
  71. Shea EM, Gibeaut DM, Carpita NC (1989) Stuctural analysis of the cell walls regenerated by carrot protoplasts. Planta 179:293–308CrossRefGoogle Scholar
  72. Skopelitis DS, Paranychianakis NV, Paschalidis KA, Pliakonis ED, Delis ID, Yakoumakis DI, Kouvarakis A, Papadakis AK, Stephanou EG, Roubelakis-Angelakis KA (2006) Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine. Plant Cell 18:2767–2781PubMedCrossRefGoogle Scholar
  73. Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Persson S, Raab T, Vorwerk S, Youngs H (2004) Toward a systems approach to understanding plant cell walls. Science 306:2206–2211PubMedCrossRefGoogle Scholar
  74. Steinwand BJ, Kieber JJ (2010) The role of receptor-like kinases in regulating cell wall function. Plant Physiol 153:479–484PubMedCrossRefGoogle Scholar
  75. Sterling JD, Atmodjo MA, Inwood SE, Kumar Kolli VS, Quigley HF, Hahn MG, Mohnen D (2006) Functional identification of an Arabidopsis pectin biosynthetic homogalacturonan galacturonosyltransferase. Proc Natl Acad Sci USA 103:5236–5241PubMedCrossRefGoogle Scholar
  76. Strassera R, Bondilia JS, Vavraa U, Schoberera J, Svobodaa B, Glössla J, Léonardb R, Stadlmannb J, Altmannb F, Steinkellnera H, Macha L (2007) A unique beta1,3-galactosyltransferase is indispensable for the biosynthesis of N-glycans containing Lewis a structures in Arabidopsis thaliana. Plant Cell 19:2278–2292CrossRefGoogle Scholar
  77. Szczegielniak J, Klimecka M, Liwosz A, Ciesielski A, Kaczanowski S, Dobrowolska G, Harmon AC, Muszynska G (2005) A wound-responsive and phospholipid-regulated maize calcium-dependent protein kinase. Plant Physiol 139:1970–1983PubMedCrossRefGoogle Scholar
  78. Tan F, Li G, Chitteti BR, Peng Z (2007) Proteome and phosphoproteome analysis of chromatin associated proteins in rice (Oryza sativa). Proteomics 7:4511–4527PubMedCrossRefGoogle Scholar
  79. Tan F, Zhang K, Mujahid H, Verma DP, Peng Z (2011) Differential histone modification and protein expression associated with cell wall removal and regeneration in rice (Oryza sativa). J Proteome Res 10:551–563Google Scholar
  80. Tanurdzic M, Vaughn MW, Jiang H, Lee TJ, Slotkin RK, Sosinski B, Thompson WF, Doerge RW, Martienssen RA (2008) Epigenomic consequences of immortalized plant cell suspension culture. PLoS Biol 6:2880–2895PubMedCrossRefGoogle Scholar
  81. Turner SR, Taylor N, Jones L (2001) Mutations of the secondary cell wall. Plant Mol Biol 47:209–219PubMedCrossRefGoogle Scholar
  82. Vaughn KC, Turley RB (2001) Ultrastructural effects of cellulose biosynthesis inhibitor herbicides on developing cotton fibers. Protoplasma 216:80–93PubMedCrossRefGoogle Scholar
  83. Wang HJ, Wan AR, Hsu CM, Lee KW, Yu SM, Jauh GY (2007) Transcriptomic adaptations in rice suspension cells under sucrose starvation. Plant Mol Biol 63:441–463PubMedCrossRefGoogle Scholar
  84. Wang H, Avci U, Nakashima J, Hahn MG, Chen F, Dixon RA (2010) Mutation of WRKY transcription factors initiates pith secondary wall formation and increases stem biomass in dicotyledonous plants. Proc Natl Acad Sci USA 107:22338–22343PubMedCrossRefGoogle Scholar
  85. Wen TJ, Schnable PS (1994) Analyses of mutants of three genes that influence root hair development in Zea mays (Gramineae) suggest that root hairs are dispensable. Am J Bot 81:833–842CrossRefGoogle Scholar
  86. Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442:705–708PubMedCrossRefGoogle Scholar
  87. Xu SL, Rahman A, Baskin TI, Kieber JJ (2008) Two leucine-rich repeat receptor kinases mediate signaling, linking cell wall biosynthesis and ACC synthase in Arabidopsis. Plant Cell 20:3065–3079PubMedCrossRefGoogle Scholar
  88. Yang X, Tu L, Zhu L, Fu L, Min L, Zhang X (2008) Expression profile analysis of genes involved in cell wall regeneration during protoplast culture in cotton by suppression subtractive hybridization and macroarray. J Exp Bot 59:3661–3674PubMedCrossRefGoogle Scholar
  89. Yong W, Link B, O’Malley R, Tewari J, Hunter CT, Lu CA, Li X, Bleecker AB, Koch KE, McCann MC, McCarty DR, Patterson SE, Reiter WD, Staiger C, Thomas SR, Vermerris W, Carpita NC (2005) Genomics of plant cell wall biogenesis. Planta 221:747–751PubMedCrossRefGoogle Scholar
  90. Zhong R, Ye ZH (2007) Regulation of cell wall biosynthesis. Curr Opin Plant Biol 10:564–572PubMedCrossRefGoogle Scholar
  91. Zhong R, 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 14:165–179PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Rita Sharma
    • 1
    • 2
  • Feng Tan
    • 3
  • Ki-Hong Jung
    • 1
    • 4
  • Manoj K. Sharma
    • 1
    • 2
  • Zhaohua Peng
    • 3
  • Pamela C. Ronald
    • 1
    • 2
    • 4
    Email author
  1. 1.Department of Plant PathologyUniversity of CaliforniaDavisUSA
  2. 2.Joint Bioenergy InstituteEmeryvilleUSA
  3. 3.Department of Biochemistry and Molecular BiologyMississippi State UniversityStarkvilleUSA
  4. 4.Department of Plant Molecular Systems Biotechnology and Crop Biotech InstituteKyung Hee UniversityYonginKorea

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