Advances in research of cellulose synthase genes in plants

QUE Feng, ZHA Ruofei, WEI Qiang

JOURNAL OF NANJING FORESTRY UNIVERSITY ›› 2022, Vol. 46 ›› Issue (6) : 207-214.

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JOURNAL OF NANJING FORESTRY UNIVERSITY ›› 2022, Vol. 46 ›› Issue (6) : 207-214. DOI: 10.12302/j.issn.1000-2006.202105039

Advances in research of cellulose synthase genes in plants

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Abstract

Cellulose is the most abundant polysaccharide in nature, which accounts for more than 50% of the carbon content in the plant kingdom. Cellulose is the main cell wall content in plants and plays a key role in weight bearing. The synthesis of cellulose is catalyzed by cellulose synthase components (CSCs) in the plasma membrane. The research advances on the type, structure, transcriptional regulation of CESA, and the structure, assembly, and traffic of CSCs were reviewed here. The plant cell wall was classified into the primary cell wall and the secondary cell wall. The CSCs involved in cellulose synthesis in different cell wall types are different. The proportion of CESAs in the CSCs varies according to the species. CESA stoichiometry occurs in equimolar amounts in the majority of plants, while in aspen tension wood the secondary cell wall CESA stoichiometry changed to 8∶3∶1. CSCs assemble in the Golgi and are secreted to the plasma membrane through the trans-Golgi network (TGN) compartment. The abundance and distribution of CSCs in the plasma membrane largely determine the oriented deposition of cellulose. Many key genes were found interacting with special CESA to recognize and regulate CSCs traffic. Plant hormones, such as brassinosteroids, can control the cellulose synthesis by regulating the expression of CESAs. In the future, gene-editing technology can be used to further work on CESA function, CSCs structure model, CESA stoichiometry in CSCs, the relationship between assembly and transport and cellulose synthesis speed in CSCs, and the transcriptional regulation of CESA to improve the regulation mechanisms of plant cellulose synthesis.

Key words

cellulose / cellulose synthase (CESA) / cellulose synthase components / interacting genes

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QUE Feng , ZHA Ruofei , WEI Qiang. Advances in research of cellulose synthase genes in plants[J]. JOURNAL OF NANJING FORESTRY UNIVERSITY. 2022, 46(6): 207-214 https://doi.org/10.12302/j.issn.1000-2006.202105039

References

[1]
SIRÓ I, PLACKETT D. Microfibrillated cellulose and new nanocomposite materials:a review[J]. Cellulose, 2010, 17(3):459-494.DOI:10.1007/s10570-010-9405-y.
[2]
ABE K, YANO H. Comparison of the characteristics of cellulose microfibril aggregates of wood,rice straw and potato tuber[J]. Cellulose, 2009, 16(6):1017-1023.DOI:10.1007/s10570-009-9334-9.
[3]
POLKO J K, KIEBER J J. The regulation of cellulose biosynthesis in plants[J]. Plant Cell, 2019, 31(2):282-296. DOI: 10.1105/tpc.18.00760.
[4]
SAXENA I M, BROWN R M. Cellulose biosynthesis:current views and evolving concepts[J]. Ann Bot, 2005, 96(1):9-21.DOI:10.1093/aob/mci155.
[5]
赵广荣, 刘进元. 棉纤维形态建成研究的新进展[J]. 棉花学报, 2002, 14(2):121-125.
ZHAO G R, LIU J Y. Progress in studies on cotton fiber morphogenesis[J]. Cotton Sci, 2002, 14(2):121-125.DOI:10.3969/j.issn.1002-7807.2002.02.013.
[6]
SCHNEIDER R, HANAK T, PERSSON S, et al. Cellulose and callose synthesis and organization in focus,what’s new?[J]. Curr Opin Plant Biol, 2016, 34:9-16.DOI:10.1016/j.pbi.2016.07.007.
[7]
SOMERVILLE C. Cellulose synthesis in higher plants[J]. Annu Rev Cell Dev Biol, 2006, 22:53-78.DOI:10.1146/annurev.cellbio.22.022206.160206.
[8]
BROWN R M Jr. Cellulose microfibril assembly and orientation:recent developments[J]. J Cell Sci Suppl, 1985, 2:13-32.DOI:10.1242/jcs.1985.supplement_2.2.
[9]
NEWMAN R H, HILL S J, HARRIS P J. Wide-angle X-ray scattering and solid-state nuclear magnetic resonance data combined to test models for cellulose microfibrils in mung bean cell walls[J]. Plant Physiol, 2013, 163(4):1558-1567.DOI:10.1104/pp.113.228262.
[10]
NIXON B T, MANSOURI K, SINGH A, et al. Comparative structural and computational analysis supports eighteen cellulose synthases in the plant cellulose synthesis complex[J]. Sci Rep, 2016, 6:28696.DOI:10.1038/srep28696.
[11]
FERNANDES A N, THOMAS L H, ALTANER C M, et al. Nanostructure of cellulose microfibrils in spruce wood[J]. Proc Natl Acad Sci USA, 2011, 108(47):E1195-E1203.DOI:10.1073/pnas.1108942108.
[12]
RICHMOND T. Higher plant cellulose synthases[J]. Genome Biol, 2000, 1(4):review3001.DOI:10.1186/gb-2000-1-4-reviews3001.
[13]
BI Y C, HUBBARD C, PURUSHOTHAM P, et al. Insights into the structure and function of membrane-integrated processive glycosyltransferases[J]. Curr Opin Struct Biol, 2015, 34:78-86.DOI:10.1016/j.sbi.2015.07.008.
[14]
PEAR J R, KAWAGOE Y, SCHRECKENGOST W E, et al. Higher plants contain homologs of the bacterial CelA genes encoding the catalytic subunit of cellulose synthase[J]. Proc Natl Acad Sci USA, 1996, 93(22):12637-12642.DOI:10.1073/pnas.93.22.12637.
[15]
ENDLER A, PERSSON S. Cellulose synthases and synthesis in Arabidopsis[J]. Mol Plant, 2011, 4(2):199-211.DOI:10.1093/mp/ssq079.
[16]
KUMAR M, THAMMANNAGOWDA S, BULONE V, et al. An update on the nomenclature for the cellulose synthase genes in Populus[J]. Trends Plant Sci, 2009, 14(5):248-254.DOI:10.1016/j.tplants.2009.02.004.
[17]
WANG L Q, GUO K, LI Y, et al. Expression profiling and integrative analysis of the CESA/CSL superfamily in rice[J]. BMC Plant Biol, 2010, 10:282.DOI:10.1186/1471-2229-10-282.
[18]
BEECKMAN T, PRZEMECK G K H, STAMATIOU G, et al. Genetic complexity of cellulose synthase a gene function in Arabidopsis embryogenesis[J]. Plant Physiol, 2002, 130(4):1883-1893.DOI:10.1104/pp.102.010603.
[19]
TAYLOR N G, HOWELLS R M, HUTTLY A K, et al. Interactions among three distinct CesA proteins essential for cellulose synthesis[J]. Proc Natl Acad Sci USA, 2003, 100(3):1450-1455.DOI:10.1073/pnas.0337628100.
[20]
TAYLOR N G, LAURIE S, TURNER S R. Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis[J]. Plant Cell, 2000, 12(12):2529-2540.DOI:10.1105/tpc.12.12.2529.
[21]
KUMAR M, MISHRA L, CARR P, et al. Exploiting CELLULOSE SYNTHASE (CESA) class specificity to probe cellulose microfibril biosynthesis[J]. Plant Physiol, 2018, 177(1):151-167.DOI:10.1104/pp.18.00263.
[22]
ZHANG X Y, DOMINGUEZ P G, KUMAR M, et al. Cellulose synthase stoichiometry in aspen differs from Arabidopsis and Norway spruce[J]. Plant Physiol, 2018, 177(3):1096-1107.DOI:10.1104/pp.18.00394.
[23]
PURUSHOTHAM P, HO R, ZIMMER J. Architecture of a catalytically active homotrimeric plant cellulose synthase complex[J]. Science, 2020, 369(6507):1089-1094.DOI:10.1126/science.abb2978.
[24]
SAURIN A J, BORDEN K L B, BODDY M N, et al. Does this have a familiar RING?[J]. Trends Biochem Sci, 1996, 21(6):208-214.DOI:10.1016/S0968-0004(96)80017-X.
[25]
PARK S, DING S Y. The N-terminal zinc finger of CELLULOSE SYNTHASE6 is critical in defining its functional properties by determining the level of homodimerization in Arabidopsis[J]. Plant J, 2020, 103(5):1826-1838.DOI:10.1111/tpj.14870.
[26]
RAMÍREZ-RODRÍGUEZ E A, MCFARLANE H E. Insights from the structure of a plant cellulose synthase trimer[J]. Trends Plant Sci, 2021, 26(1):4-7.DOI:10.1016/j.tplants.2020.09.010.
[27]
TIMMERS J, VERNHETTES S, DESPREZ T, et al. Interactions between membrane-bound cellulose synthases involved in the synthesis of the secondary cell wall[J]. FEBS Lett, 2009, 583(6):978-982.DOI:10.1016/j.febslet.2009.02.035.
[28]
GUTIERREZ R, LINDEBOOM J J, PAREDEZ A R, et al. Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments[J]. Nat Cell Biol, 2009, 11(7):797-806.DOI:10.1038/ncb1886.
[29]
HERTH W. Arrays of plasma-membrane “rosettes” involved in cellulose microfibril formation of Spirogyra[J]. Planta, 1983, 159(4):347-356.DOI:10.1007/BF00393174.
[30]
HILL J L, HAMMUDI M B, MING T E. The Arabidopsis cellulose synthase complex:a proposed hexamer of CESA trimers in an equimolar stoichiometry[J]. Plant Cell, 2014, 26(12):4834-4842.DOI:10.1105/tpc.114.131193.
[31]
KUBICKI J D, YANG H, SAWADA D, et al. The shape of native plant cellulose microfibrils[J]. Sci Rep, 2018, 8(1):13983.DOI:10.1038/s41598-018-32211-w.
[32]
THOMAS L H, FORSYTH V T, STURCOVÁ A, et al. Structure of cellulose microfibrils in primary cell walls from collenchyma[J]. Plant Physiol, 2013, 161(1):465-476.DOI:10.1104/pp.112.206359.
[33]
DOBLIN M S, KUREK I, JACOB-WILK D, et al. Cellulose biosynthesis in plants:from genes to rosettes[J]. Plant Cell Physiol, 2002, 43(12):1407-1420.DOI:10.1093/pcp/pcf164.
[34]
DING S Y, HIMMEL M E. The maize primary cell wall microfibril: a new model derived from direct visualization[J]. J Agric Food Chem, 2006, 54(3):597-606.DOI:10.1021/jf051851z.
[35]
MÜSSIG C. Brassinosteroid-promoted growth[J]. Plant Biol (Stuttg),2005, 7(2):110-117.DOI:10.1055/s-2005-837493.
[36]
OH E, ZHU J Y, BAI M Y, et al. Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl[J]. eLife, 2014, 3:e03031.DOI:10.7554/eLife.03031.
[37]
XIE L Q, YANG C J, WANG X L. Brassinosteroids can regulate cellulose biosynthesis by controlling the expression of CESA genes in Arabidopsis[J]. J Exp Bot, 2011, 62(13):4495-4506.DOI:10.1093/jxb/err164.
[38]
SÁNCHEZ-RODRÍGUEZ C, KETELAAR K, SCHNEIDER R, et al. BRASSINOSTEROID INSENSITIVE2 negatively regulates cellulose synthesis in Arabidopsis by phosphorylating cellulose synthase 1[J]. Proc Natl Acad Sci USA, 2017, 114(13):3533-3538.DOI:10.1073/pnas.1615005114.
[39]
QUE F, KHADR A, WANG G L, et al. Exogenous brassinosteroids altered cell length,gibberellin content,and cellulose deposition in promoting carrot petiole elongation[J]. Plant Sci, 2018, 277:110-120.DOI:10.1016/j.plantsci.2018.10.010.
[40]
GEHRING W J, AFFOLTER M, BÜRGLIN T. Homeodomain proteins[J]. Annu Rev Biochem, 1994, 63:487-526.DOI:10.1146/annurev.bi.63.070194.002415.
[41]
KONG Y Z, PEI S Q, WANG Y P, et al. HOMEODOMAIN GLABROUS2 regulates cellulose biosynthesis in seed coat mucilage by activating CELLULOSE SYNTHASE5[J]. Plant Physiol, 2021, 185(1):77-93.DOI:10.1093/plphys/kiaa007.
[42]
GU Y, KAPLINSKY N, BRINGMANN M, et al. Identification of a cellulose synthase-associated protein required for cellulose biosynthesis[J]. Proc Natl Acad Sci USA, 2010, 107(29):12866-12871.DOI:10.1073/pnas.1007092107.
[43]
YANG Q H, WAN X S, WANG J Y, et al. The loss of function of HEL,which encodes a cellulose synthase interactive protein,causes helical and vine-like growth of tomato[J]. Hortic Res, 2020, 7(1):180.DOI:10.1038/s41438-020-00402-0.
[44]
BASHLINE L, LI S D, ANDERSON C T, et al. The endocytosis of cellulose synthase in Arabidopsis is dependent on μ2,a clathrin-mediated endocytosis adaptin[J]. Plant Physiol, 2013, 163(1):150-160.DOI:10.1104/pp.113.221234.
[45]
GADEYNE A, SÁNCHEZ-RODRÍGUEZ C, VANNESTE S, et al. The TPLATE adaptor complex drives clathrin-mediated endocytosis in plants[J]. Cell, 2014, 156(4):691-704.DOI:10.1016/j.cell.2014.01.039.
[46]
SÁNCHEZ-RODRÍGUEZ C, SHI Y Y, KESTEN C, et al. The cellulose synthases are cargo of the TPLATE adaptor complex[J]. Mol Plant, 2018, 11(2):346-349.DOI:10.1016/j.molp.2017.11.012.
[47]
POLKO J K, BARNES W J, VOINICIUC C, et al. SHOU4 proteins regulate trafficking of cellulose synthase complexes to the plasma membrane[J]. Curr Biol, 2018, 28(19):3174-3182.e6.DOI:10.1016/j.cub.2018.07.076.
[48]
ZUO J, NIU Q W, NISHIZAWA N, et al. KORRIGAN,an Arabidopsis endo-1,4-beta-glucanase,localizes to the cell plate by polarized targeting and is essential for cytokinesis[J]. Plant Cell, 2000, 12(7):1137-1152.DOI:10.1105/tpc.12.7.1137.
[49]
MANSOORI N, TIMMERS J, DESPREZ T, et al. KORRIGAN1 interacts specifically with integral components of the cellulose synthase machinery[J]. PLoS One, 2014, 9(11):e112387.DOI:10.1371/journal.pone.0112387.
[50]
ENDLER A, KESTEN C, SCHNEIDER R, et al. A mechanism for sustained cellulose synthesis during salt stress[J]. Cell, 2015, 162(6):1353-1364.DOI:10.1016/j.cell.2015.08.028.
[51]
HAIGLER C H, BROWN R M. Transport of rosettes from the Golgi apparatus to the plasma membrane in isolated mesophyll cells of Zinnia elegans during differentiation to tracheary elements in suspension culture[J]. Protoplasma, 1986, 134(2/3):111-120.DOI:10.1007/BF01275709.
[52]
PAREDEZ A R, SOMERVILLE C R, EHRHARDT D W. Visualization of cellulose synthase demonstrates functional association with microtubules[J]. Science, 2006, 312(5779):1491-1495.DOI:10.1126/science.1126551.
[53]
KUREK I, KAWAGOE Y, JACOB-WILK D, et al. Dimerization of cotton fiber cellulose synthase catalytic subunits occurs via oxidation of the zinc-binding domains[J]. Proc Natl Acad Sci USA, 2002, 99(17):11109-11114.DOI:10.1073/pnas.162077099.
[54]
ZHANG X N, XUE Y, GUAN Z Y, et al. Structural insights into homotrimeric assembly of cellulose synthase CesA7 from Gossypium hirsutum[J]. Plant Biotechnol J, 2021, 19(8):1579-1587.DOI:10.1111/pbi.13571.
[55]
QIAO Z, LAMPUGNANI E R, YAN X F, et al. Structure of Arabidopsis CESA3 catalytic domain with its substrate UDP-glucose provides insight into the mechanism of cellulose synthesis[J]. Proc Natl Acad Sci USA, 2021, 118(11):e2024015118.DOI:10.1073/pnas.2024015118.
[56]
VELLOSILLO T, DINNENY J R, SOMERVILLE C R, et al. TRANVIA (TVA) facilitates cellulose synthase trafficking and delivery to the plasma membrane[J]. Proc Natl Acad Sci USA, 2021, 118(30):e2021790118.DOI:10.1073/pnas.2021790118.
[57]
MCFARLANE H E, MUTWIL-ANDERWALD D, VERBANCIC J, et al. A G protein-coupled receptor-like module regulates cellulose synthase secretion from the endomembrane system in Arabidopsis[J]. Dev Cell, 2021, 56(10):1484-1497.e7.DOI:10.1016/j.devcel.2021.03.031.
[58]
CROWELL E F, BISCHOFF V, DESPREZ T, et al. Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis[J]. Plant Cell, 2009, 21(4):1141-1154.DOI:10.1105/tpc.108.065334.
[59]
LEI L, SINGH A, BASHLINE L, et al. CELLULOSE SYNTHASE INTERACTIVE1 is required for fast recycling of cellulose synthase complexes to the plasma membrane in Arabidopsis[J]. Plant Cell, 2015, 27(10):2926-2940.DOI:10.1105/tpc.15.00442.
[60]
CHAN J, COEN E. Interaction between autonomous and microtubule guidance systems controls cellulose synthase trajectories[J]. Curr Biol, 2020, 30(5):941-947.e2.DOI:10.1016/j.cub.2019.12.066.
[61]
MCFARLANE H E, DÖRING A, PERSSON S. The cell biology of cellulose synthesis[J]. Annu Rev Plant Biol, 2014, 65:69-94.DOI:10.1146/annurev-arplant-050213-040240.
[62]
BECK M, ZHOU J, FAULKNER C, et al. Spatio-temporal cellular dynamics of the Arabidopsis flagellin receptor reveal activation status-dependent endosomal sorting[J]. Plant Cell, 2012, 24(10):4205-4219.DOI:10.1105/tpc.112.100263.
[63]
WANG C, YAN X, CHEN Q, et al. Clathrin light chains regulate clathrin-mediated trafficking,auxin signaling,and development in Arabidopsis[J]. Plant Cell, 2013, 25(2):499-516.DOI:10.1105/tpc.112.108373.
[64]
MCMAHON H T, BOUCROT E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis[J]. Nat Rev Mol Cell Biol, 2011, 12(8):517-533.DOI:10.1038/nrm3151.
[65]
COCUCCI E, AGUET F, BOULANT S, et al. The first five seconds in the life of a clathrin-coated pit[J]. Cell, 2012, 150(3):495-507.DOI:10.1016/j.cell.2012.05.047.
[66]
BASHLINE L, LI S D, ZHU X Y, et al. The TWD40-2 protein and the AP2 complex cooperate in the clathrin-mediated endocytosis of cellulose synthase to regulate cellulose biosynthesis[J]. Proc Natl Acad Sci USA, 2015, 112(41):12870-12875.DOI:10.1073/pnas.1509292112.
[67]
FUJIMOTO M, SUDA Y, VERNHETTES S, et al. Phosphatidylinositol 3-kinase and 4-kinase have distinct roles in intracellular trafficking of cellulose synthase complexes in Arabidopsis thaliana[J]. Plant Cell Physiol, 2015, 56(2):287-298.DOI:10.1093/pcp/pcu195.
[68]
LUO Y, SCHOLL S, DOERING A, et al. V-ATPase activity in the TGN/EE is required for exocytosis and recycling in Arabidopsis[J]. Nat Plants, 2015, 1:15094.DOI:10.1038/nplants.2015.94.
[69]
JOHANSEN J N, CHOW C M, MOORE I, et al. AtRAB-H1b and AtRAB-H1c GTPases,homologues of the yeast Ypt6,target reporter proteins to the Golgi when expressed in Nicotiana tabacum and Arabidopsis thaliana[J]. J Exp Bot, 2009, 60(11):3179-3193.DOI:10.1093/jxb/erp153.
[70]
HE M, LAN M, ZHANG B C, et al. Rab-H1b is essential for trafficking of cellulose synthase and for hypocotyl growth in Arabidopsis thaliana[J]. J Integr Plant Biol, 2018, 60(11):1051-1069.DOI:10.1111/jipb.12694.
[71]
XU W J, CHENG H, ZHU S R, et al. Functional understanding of secondary cell wall cellulose synthases in Populus trichocarpa via the Cas9/gRNA-induced gene knockouts[J]. New Phytol, 2021, 231(4):1478-1495.DOI:10.1111/nph.17338.
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