Cellulosic fibres of flax recruit both primary and secondary cell wall cellulose synthases during deposition of thick tertiary cell walls and in the course of graviresponse
Natalia Mokshina A , Oleg Gorshkov A , Nadezda Ibragimova A , Tatyana Chernova A and Tatyana Gorshkova A B
+ Author Affiliations
- Author Affiliations
A Kazan Institute of Biochemistry and Biophysics of Kazan Scientific Centre of the Russian Academy of Sciences, Lobachevsky str., 2/31, Kazan, Russia 420111.
B Corresponding author. Email: gorshkova@kibb.knc.ru
Functional Plant Biology 44(8) 820-831 https://doi.org/10.1071/FP17105
Submitted: 1 October 2016 Accepted: 19 May 2017 Published: 4 July 2017
Abstract
Cellulose synthesising complex consists of cellulose synthase (CESA) subunits encoded by a multigene family; different sets of CESA genes are known to be expressed during primary and secondary cell wall formation. We examined the expression of LusCESAs in flax (Linum usitatissimum L.) cellulosic fibres at various stages of development and in the course of graviresponse by means of RNA-Seq and quantitative PCR. Transcripts for both primary and secondary cell wall-related CESAs were abundant in fibres depositing highly cellulosic tertiary cell walls. Gravistimulation of flax plants temporally increased the abundance of CESA transcripts, specifically in phloem fibres located at the pulling stem side. Construction of coexpression networks for LusCESAs revealed that both primary and secondary cell wall-related CESAs were involved in the joint coexpression group in fibres depositing tertiary cell walls, as distinct from other tissues, where these genes were within separate groups. The obtained data suggest that fibres depositing tertiary cell walls have a specific mechanism of cellulose biosynthesis and a specific way of its regulation.
Additional keywords: G-layer, gravitropic response, Linum usitatissimum L., plant fibres.
References
Andersson-Gunnerås 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. The Plant Journal 45, 144–165.| Biosynthesis of cellulose enriched tension wood in Populus: global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis.Crossref | GoogleScholarGoogle Scholar |
Atanassov II, Pittman JK, Turner SR (2009) Elucidating the mechanisms of assembly and subunit interaction of the cellulose synthase complex of Arabidopsis secondary cell walls. The Journal of Biological Chemistry 284, 3833–3841.
| Elucidating the mechanisms of assembly and subunit interaction of the cellulose synthase complex of Arabidopsis secondary cell walls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1Oru78%3D&md5=ffd31ca50cb88f0c5b5e622fa0554dfaCAS |
Bashline L, Lei L, Li S, Gu Y (2014) Cell wall, cytoskeleton, and cell expansion in higher plants. Molecular Plant 7, 586–600.
| Cell wall, cytoskeleton, and cell expansion in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXls1Oitbs%3D&md5=ab469eb636160720a78250f0252bdfe0CAS |
Betancur L, Singh B, Rapp RA, Wendel JF, Marks MD, Roberts AW, Haigler CH (2010) Phylogenetically distinct cellulose synthase genes support secondary wall thickening in Arabidopsis shoot trichomes and cotton fiber. Journal of Integrative Plant Biology 52, 205–220.
| Phylogenetically distinct cellulose synthase genes support secondary wall thickening in Arabidopsis shoot trichomes and cotton fiber.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXivVCntro%3D&md5=08122d16f1b775a0bc6c9079b32d0c44CAS |
Brett CT (2000) Cellulose microfibrils in plants: biosynthesis, deposition, and integration into the cell wall. International Review of Cytology 199, 161–199.
| Cellulose microfibrils in plants: biosynthesis, deposition, and integration into the cell wall.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXltFKgsb8%3D&md5=f3ab6788602175fbdd49cebc8c0634d4CAS |
Carroll A, Specht CD (2011) Understanding plant cellulose synthases through a comprehensive investigation of the cellulose synthase family sequences. Frontiers in Plant Science 2, 5
| Understanding plant cellulose synthases through a comprehensive investigation of the cellulose synthase family sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptVGjs78%3D&md5=eb813f9d118115e369305e01afad16b3CAS |
Carroll A, Mansoori N, Li SD, Lei L, Vernhettes S, Visser RGF, Somerville C, Gu Y, Trindade LM (2012) Complexes with mixed primary and secondary cellulose synthases are functional in Arabidopsis plants. Plant Physiology 160, 726–737.
| Complexes with mixed primary and secondary cellulose synthases are functional in Arabidopsis plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFaksbnO&md5=d90b4056edf72dedc5c20525a09995aeCAS |
Chantreau M, Chabbert B, Billiard S, Hawkins S, Neutelings G (2015) Functional analyses of cellulose synthase genes in flax (Linum usitatissimum) by virus-induced gene silencing. Plant Biotechnology Journal 13, 1312–1324.
| Functional analyses of cellulose synthase genes in flax (Linum usitatissimum) by virus-induced gene silencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvVCju7rM&md5=39b0bfe39bcc1738db02a03f842572b0CAS |
Chen S, Ehrhardt DW, Somerville CR (2010) Mutations of cellulose synthase (CESA1) phosphorylation sites modulate anisotropic cell expansion and bidirectional mobility of cellulose synthase. Proceedings of the National Academy of Science of the United States of America 107, 17188–17193.
| Mutations of cellulose synthase (CESA1) phosphorylation sites modulate anisotropic cell expansion and bidirectional mobility of cellulose synthase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlSjurrJ&md5=e26a443b35324752904cf535b9161bb9CAS |
Creux NM, De Castro MH, Ranik M, Maleka MF, Myburg AA (2013) Diversity and cis-element architecture of the promoter regions of cellulose synthase genes in Eucalyptus. Tree Genetics & Genomes 9, 989–1004.
| Diversity and cis-element architecture of the promoter regions of cellulose synthase genes in Eucalyptus.Crossref | GoogleScholarGoogle 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. Proceedings of the National Academy of Sciences of the United States of America 104, 15572–15577.
| Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFaju7fM&md5=11b5d8f54e0e2a60ec375956c2a6d616CAS |
Djerbi S, Lindskog M, Arvestad L, Sterky F, Teeri TT (2005) The genome sequence of black cottonwood (Populus trichocarpa) reveals 18 conserved cellulose synthase (CesA) genes. Planta 221, 739–746.
| The genome sequence of black cottonwood (Populus trichocarpa) reveals 18 conserved cellulose synthase (CesA) genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVymsbg%3D&md5=033eb5b18c69386e74ac3f6dae49c158CAS |
Doblin MS, Kureck I, Jacob-Wilk D, Delmer DP (2002) Cellulose biosynthesis in plants: from genes to rosettes. Plant & Cell Physiology 43, 1407–1420.
| Cellulose biosynthesis in plants: from genes to rosettes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtF2gsg%3D%3D&md5=574d5a3c71391c0a377c4786a5dc0e8aCAS |
Foston M, Hubbell CA, Samuel R, Jung S, Fan H, Ding S-Y, Zeng Y, Jawdy S, Davis M, Sykes R, Gjersing E, Tuskan GA, Kalluri U, Ragauskas AJ (2011) Chemical, ultrastructural and supramolecular analysis of tension wood in Populus tremula × alba as a model substrate for reduced recalcitrance. Energy & Environmental Science 4, 4962–4971.
| Chemical, ultrastructural and supramolecular analysis of tension wood in Populus tremula × alba as a model substrate for reduced recalcitrance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFKlurbO&md5=6e95dba3c0e0ec72c373ac3800209ce1CAS |
Giddings TH, Brower DL, Staehelin LA (1980) Visualization of particle complexes in the plasma membrane of Micrasterias denticulata associated with the formation of cellulose fibrils in primary and secondary cell walls. The Journal of Cell Biology 84, 327–339.
| Visualization of particle complexes in the plasma membrane of Micrasterias denticulata associated with the formation of cellulose fibrils in primary and secondary cell walls.Crossref | GoogleScholarGoogle Scholar |
Goecks J, Nekrutenko A, Taylor J, The Galaxy Team (2010) Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biology 11, R86
| Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences.Crossref | GoogleScholarGoogle Scholar |
Gorshkov O, Mokshina N, Gorshkov V, Chemikosova S, Gogolev Yu, Gorshkova T (2017a) Transcriptome portrait of cellulose-enriched flax fibers at advanced stage of specialization. Plant Molecular Biology 93, 431–449.
| Transcriptome portrait of cellulose-enriched flax fibers at advanced stage of specialization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XitFSls7%2FF&md5=d00804976d2209a3c279a287c4fb29ccCAS |
Gorshkov O, Mokshina N, Ibragimova N, Ageeva M, Gogoleva N, Gorshkova TA (2017b) Phloem fibres as motors of gravitropic behaviour of flax plants: level of transcriptome. Functional Plant Biology
| Phloem fibres as motors of gravitropic behaviour of flax plants: level of transcriptome.Crossref | GoogleScholarGoogle Scholar |
Gorshkova TA, Sal’nikov VV, Chemikosova SB, Ageeva MV, Pavlencheva NV, van Dam JEG (2003) The snap point: a transition point in Linum usitatissimum bast fiber development. Industrial Crops and Products 18, 213–221.
| The snap point: a transition point in Linum usitatissimum bast fiber development.Crossref | GoogleScholarGoogle Scholar |
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. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 57, 328–341.
| Specific type of secondary cell wall formed by plant fibers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlslCksL0%3D&md5=66ee556c1bb3f3141cdf6719ba8a1103CAS |
Gorshkova T, Brutch N, Chabbert B, Deyholos M, Hayashi T, Lev-Yadun S, Mellerowicz EJ, Morvan C, Neutelings G, Pilate G (2012) Plant fiber formation: state of the art, recent and expected progress, and open questions. Critical Reviews in Plant Sciences 31, 201–228.
| Plant fiber formation: state of the art, recent and expected progress, and open questions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtlCrurg%3D&md5=6d8cb81f52cb74fc6988e5c111950732CAS |
Hotte NSC, Deyholos MK (2008) A flax fibre proteome: identification of proteins enriched in bast fibres. BMC Plant Biology 8, 52
| A flax fibre proteome: identification of proteins enriched in bast fibres.Crossref | GoogleScholarGoogle Scholar |
Huis R, Hawkins S, Neutelings G (2010) Selection of reference genes for quantitative gene expression normalization in flax (Linum usitatissimum L.). BMC Plant Biology 10, 71
| Selection of reference genes for quantitative gene expression normalization in flax (Linum usitatissimum L.).Crossref | GoogleScholarGoogle Scholar |
Ibragimova NN, Mokshina NE, Gorshkova TA (2012) Cell wall proteins of flax phloem fibers. Russian Journal of Bioorganic Chemistry 38, 117–125.
| Cell wall proteins of flax phloem fibers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XksFWqsbY%3D&md5=3393ebe84f1e6dbaca412e7031b191b5CAS |
Ibragimova NN, Ageeva MV, Gorshkova TA (2017) Development of gravitropic response: unusual behavior of flax phloem G-fibers. Protoplasma 254, 749–762.
| Development of gravitropic response: unusual behavior of flax phloem G-fibers.Crossref | GoogleScholarGoogle Scholar |
Ioelovich M (2008) Cellulose as a nanostructured polymer: a short review. BioResources 3, 1403–1418.
Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biology 14, R36
| TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions.Crossref | GoogleScholarGoogle Scholar |
Kumar M, Turner SR (2015) Plant cellulose synthesis: CESA proteins crossing kingdoms. Phytochemistry 112, 91–99.
| Plant cellulose synthesis: CESA proteins crossing kingdoms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1ylsbrE&md5=a3734fd5217afa4d244844de62a0ac30CAS |
Kumar M, Thammannagowda S, Bulone V, Chiang V, Han KH, Joshi CP, Mansfield SD, Mellerowicz E, Sundberg B, Teeri T, Ellis BE (2009) An update on the nomenclature for the cellulose synthase genes in Populus. Trends in Plant Science 14, 248–254.
| An update on the nomenclature for the cellulose synthase genes in Populus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXls1Oqt7o%3D&md5=54201ec1bd150de63d6ad54a42656e5cCAS |
Lei L, Li S, Gu Y (2012) Cellulose synthase complexes: composition and regulation. Frontiers in Plant Science 3, 75
| Cellulose synthase complexes: composition and regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XnsV2jur0%3D&md5=7fccd1f2f8dcb4b648380cff82dfab0bCAS |
Li S, Lei L, Gu Y (2013) Functional analysis of complexes with mixed primary and secondary cellulose synthases. Plant Signaling & Behavior 8, e23179
| Functional analysis of complexes with mixed primary and secondary cellulose synthases.Crossref | GoogleScholarGoogle Scholar |
Li S, Bashline L, Lei L, Gu Y (2014) Cellulose synthesis and its regulation. The Arabidopsis Book 12, e0169
| Cellulose synthesis and its regulation.Crossref | GoogleScholarGoogle Scholar |
Li S, Bashline L, Zheng Y, Xin X, Huang S, Kong Z, Kim SH, Cosgrove DJ, Gu Y (2016) Cellulose synthase complexes act in a concerted fashion to synthesize highly aggregated cellulose in secondary cell walls of plants. Proceedings of the National Academy of Sciences of the United States of America 113, 11348–11353.
| Cellulose synthase complexes act in a concerted fashion to synthesize highly aggregated cellulose in secondary cell walls of plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsFarsLvF&md5=baca5af95db16c7397d693975c24923fCAS |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=c6e730b8bcaab07d1e52bd2affd3622dCAS |
Lu S, Li L, Yi X, Joshi CP, Chiang VL (2008) Differential expression of three eucalyptus secondary cell wall-related cellulose synthase genes in response to tension stress. Journal of Experimental Botany 59, 681–695.
| Differential expression of three eucalyptus secondary cell wall-related cellulose synthase genes in response to tension stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsValsr8%3D&md5=869701c869dea895325a3bbf07332ddcCAS |
Mellerowicz EJ, Gorshkova TA (2012) Tensional stress generation in gelatinous fibres: a review and possible mechanism based on cell-wall structure and composition. Journal of Experimental Botany 63, 551–565.
| Tensional stress generation in gelatinous fibres: a review and possible mechanism based on cell-wall structure and composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xos1Cqtw%3D%3D&md5=a0a13f132b1da7354d3526013ef6e0dcCAS |
Mendu V, Griffiths JS, Persson S, Stork J, Downie AB, Voiniciuc C, Haughn GW, DeBolt S (2011) Subfunctionalization of cellulose synthases in seed coat epidermal cells mediates secondary radial wall synthesis and mucilage attachment. Plant Physiology 157, 441–453.
| Subfunctionalization of cellulose synthases in seed coat epidermal cells mediates secondary radial wall synthesis and mucilage attachment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Sit73P&md5=6b97b8cebf1a2942f8021557b1ba0561CAS |
Mitsuda N, Ikeda M, Takada S, Takiguchi Y, Kondou Y, Yoshizumi T, Fujita M, Shinozaki K, Matsui M, Ohme-Takagi M (2010) Efficient yeast one-/two-hybrid screening using a library composed only of transcription factors in Arabidopsis thaliana. Plant & Cell Physiology 51, 2145–2151.
| Efficient yeast one-/two-hybrid screening using a library composed only of transcription factors in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFGrs7rE&md5=6ea78b6919ac6ea244161ec54b34a48eCAS |
Mokshina N, Gorshkova T, Deyholos MK (2014) Chitinase-like (CTL) and cellulose synthase (CESA) gene expression in gelatinous-type cellulosic walls of flax (Linum usitatissimum L.) bast fibers. PLoS One 9, e97949
| Chitinase-like (CTL) and cellulose synthase (CESA) gene expression in gelatinous-type cellulosic walls of flax (Linum usitatissimum L.) bast fibers.Crossref | GoogleScholarGoogle Scholar |
Mueller SC, Brown RM (1980) Evidence for an intramembranous component associated with a cellulose microfibril synthesizing complex in higher plants. The Journal of Cell Biology 84, 315–326.
| Evidence for an intramembranous component associated with a cellulose microfibril synthesizing complex in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3c3gsVCgsw%3D%3D&md5=ce8207b5f039f4e232acb305d87702d7CAS |
Mueller SC, Brown RMJR, Scott TK (1976) Cellulosic microfibrils: nascent stages of synthesis in a higher plant cell. Science 194, 949–951.
| Cellulosic microfibrils: nascent stages of synthesis in a higher plant cell.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvgtFKqtw%3D%3D&md5=961875b89678bedf461c9ec91ca675ceCAS |
Müller M, Burghammer M, Sugiyama J (2006) Direct investigation of the structural properties of tension wood cellulose microfibrils using microbeam X-ray fibre diffraction. Holzforschung 60, 474–479.
| Direct investigation of the structural properties of tension wood cellulose microfibrils using microbeam X-ray fibre diffraction.Crossref | GoogleScholarGoogle Scholar |
Nixon BT, Mansouri K, Singh A, Du J, Davis JK, Lee J-G, Slabaugh E, Vandavasi VG, O’Neill H, Roberts EM, Roberts AW, Yingling YG, Haigler CH (2016) Comparative structural and computational analysis supports eighteen cellulose synthases in the plant cellulose synthesis complex. Scientific Reports 6, 28696
| Comparative structural and computational analysis supports eighteen cellulose synthases in the plant cellulose synthesis complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtVKhsrvP&md5=dafa7a9c8c744f68ff51104a546dab74CAS |
Norberg PH, Meier H (1966) Physical and chemical properties of gelatinous layer in tension wood fibres of aspen (Populus tremula L.). Holzforschung 20, 174–178.
| Physical and chemical properties of gelatinous layer in tension wood fibres of aspen (Populus tremula L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2sXls1Oiug%3D%3D&md5=89b34458691c8df5af4d612e46ad22afCAS |
Paux E, Carocha V, Marques C, de Sousa AM, Borralho N, Sivadon P, Grima-Pettenati J (2005) Transcript profiling of Eucalyptus xylem genes during tension wood formation. New Phytologist 167, 89–100.
| Transcript profiling of Eucalyptus xylem genes during tension wood formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtl2nsbY%3D&md5=af24456aca06beb172bb441c7ec7b783CAS |
Persson S, Wei H, Milne J, Page GP, Somerville CR (2005) Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proceedings of the National Academy of Sciences of the United States of America 102, 8633–8638.
| Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsFCgt7s%3D&md5=b47770908364b7638b68a3b11a8966baCAS |
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. Proceedings of the National Academy of Sciences of the United States of America 104, 15566–15571.
| Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFaju7rF&md5=bf2449aba77a26ffcdeb99d83f563826CAS |
Ranik M, Myburg AA (2006) Six new cellulose synthase genes from Eucalyptus are associated with primary and secondary cell wall biosynthesis. Tree Physiology 26, 545–556.
| Six new cellulose synthase genes from Eucalyptus are associated with primary and secondary cell wall biosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltFWqsrg%3D&md5=5b97aaf835841882a6d62ee97e9bf8d3CAS |
Richmond TA, Somerville CR (2000) The cellulose synthase superfamily. Plant Physiology 124, 495–498.
| The cellulose synthase superfamily.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsF2rsrY%3D&md5=3f49ac0376a0cc2c1df785fa01279df0CAS |
Robinson DG, White RK, Preston RD (1972) Fine structure of swarmers of Cladophora and Chaetomorpha. III. Wall synthesis and development. Planta 107, 131–144.
| Fine structure of swarmers of Cladophora and Chaetomorpha. III. Wall synthesis and development.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cvgsVSruw%3D%3D&md5=bcfaa621613c99b477cd0677bc94b683CAS |
Ruprecht C, Mutwil M, Saxe F, Eder M, Nikoloski Z, Persson S (2011) Large-scale co-expression approach to dissect secondary cell wall formation across plant species. Frontiers in Plant Science 2, 23
| Large-scale co-expression approach to dissect secondary cell wall formation across plant species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXovVajtb4%3D&md5=e18faefc292b270270e34463f10496cbCAS |
SEQC/MAQC-III Consortium (2014) A comprehensive assessment of RNA-seq accuracy, reproducibility and information content by the Sequencing Quality Control Consortium. Nature Biotechnology 32, 903–914.
| A comprehensive assessment of RNA-seq accuracy, reproducibility and information content by the Sequencing Quality Control Consortium.Crossref | GoogleScholarGoogle Scholar |
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Research 13, 2498–2504.
| Cytoscape: a software environment for integrated models of biomolecular interaction networks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovFWrtr4%3D&md5=f1576cd411499a27bf31104615a7331aCAS |
Somerville C (2006) Cellulose synthesis in higher plants. Annual Review of Cell and Developmental Biology 22, 53–78.
| Cellulose synthesis in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1yjs7vM&md5=2c92a2cc1849fd2624f3b837a8e88186CAS |
Song D, Shen J, Li L (2010) Characterization of cellulose synthase complexes in Populus xylem differentiation. New Phytologist 187, 777–790.
| Characterization of cellulose synthase complexes in Populus xylem differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFSmu7jK&md5=c8b677502d6c2d2fb9c17900d8e861c8CAS |
Stork J, Harris D, Griffiths J, Williams B, Beisson F, Li-Beisson Y, Mendu V, Haughn G, DeBolt S (2010) CELLULOSE SYNTHASE9 serves a nonredundant role in secondary cell wall synthesis in Arabidopsis epidermal testa cells. Plant Physiology 153, 580–589.
| CELLULOSE SYNTHASE9 serves a nonredundant role in secondary cell wall synthesis in Arabidopsis epidermal testa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnvVamtr8%3D&md5=d27c4914dd6a964e4389771afb05d411CAS |
Taylor NG, Laurie S, Turner SR (2000) Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. The Plant Cell 12, 2529–2540.
| Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXns1SgtQ%3D%3D&md5=2325cf43f6dd25169fadc27bc46d8ecfCAS |
Taylor NG, Howells RM, Huttly AK, Vickers K, Turner SR (2003) Interactions among three distinct CesA proteins essential for cellulose synthesis. Proceedings of the National Academy of Sciences of the United States of America 100, 1450–1455.
| Interactions among three distinct CesA proteins essential for cellulose synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtF2nsrc%3D&md5=5de9e3602ed142e52b0584f376e31cf9CAS |
Thomas LH, Forsyth VT, Sturcová A, Kennedy CJ, May RP, Altaner CM, Apperley DC, Wess TJ, Jarvis MC (2013) Structure of cellulose microfibrils in primary cell walls from collenchyma. Plant Physiology 161, 465–476.
| Structure of cellulose microfibrils in primary cell walls from collenchyma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXntVCks7s%3D&md5=d95e056c016887b2085965cf1e9f4916CAS |
Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protocols 7, 562–578.
| Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjt1Cjsrc%3D&md5=5d25a15df58cbd66340e6d5b17980c1bCAS |
Tzfadia O, Diels T, De Meyer S, Vandepoele K, Aharoni A, Van de Peer Y (2016) CoExpNetViz: comparative co-expression networks construction and visualization tool. Frontiers in Plant Science 6, 1194
| CoExpNetViz: comparative co-expression networks construction and visualization tool.Crossref | GoogleScholarGoogle Scholar |
Vergara CE, Carpita NC (2001) β-d-glycan synthases and the CesA gene family: lessons to be learned from the mixed-linkage (1→3),(1→4)β-d-glucan synthase. Plant Molecular Biology 47, 145–160.
| β-d-glycan synthases and the CesA gene family: lessons to be learned from the mixed-linkage (1→3),(1→4)β-d-glucan synthase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmslGmsb0%3D&md5=bcd1964d293fc6247de7df4a3a0612ccCAS |
Wang ZW, Hobson N, Galindo L, Zhu S, Shi D, McDill J, Yang L, Hawkins S, Neutelings G, Datla R, Lambert G, Galbraith DW, Grassa CJ, Geraldes A, Cronk QC, Cullis C, Dash PK, Kumar PA, Cloutier S, Sharpe AG, Wong GKS, Wang J, Deyholos MK (2012) The genome of flax (Linum usitatissimum) assembled de novo from short shotgun sequence reads. The Plant Journal 72, 461–473.
| The genome of flax (Linum usitatissimum) assembled de novo from short shotgun sequence reads.Crossref | GoogleScholarGoogle Scholar |
Watanabe Y, Meents MJ, McDonnell LM, Barkwill S, Sampathkumar A, Cartwright HN, Demura T, Ehrhardt DW, Samuels AL, Mansfield SD (2015) Visualization of cellulose synthases in Arabidopsis secondary cell walls. Science 350, 198–203.
| Visualization of cellulose synthases in Arabidopsis secondary cell walls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhs1antLnP&md5=e1dbc128bfb7883984b907d17a1ce0d0CAS |
Wightman R, Turner S (2010) Trafficking of the plant cellulose synthase complex. Plant Physiology 153, 427–432.
| Trafficking of the plant cellulose synthase complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnvVamsLk%3D&md5=a13e356c6267c14961216076703d7894CAS |
Wightman R, Marshall R, Turner SR (2009) A cellulose synthase-containing compartment moves rapidly beneath sites of secondary wall synthesis. Plant & Cell Physiology 50, 584–594.
| A cellulose synthase-containing compartment moves rapidly beneath sites of secondary wall synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsFSjtLw%3D&md5=7697dc51e34a5e97beaab514e301c4cfCAS |
