Cellulose synthesis complexes are homo-oligomeric and hetero-oligomeric in Physcomitrium patens

Li, Xingxing; Chaves, Arielle M.; Dees, Dianka C. T.; Mansoori, Nasim; Yuan, Kai; Speicher, Tori L.; Norris, Joanna H.; Wallace, Ian S.; Trindade, Luisa M.; Roberts, Alison W.

doi:10.1093/plphys/kiac003

Title: Cellulose synthesis complexes are homo-oligomeric and hetero-oligomeric in Physcomitrium patens

Journal Article · 12 January 2022 · Plant Physiology (Bethesda)

DOI: https://doi.org/10.1093/plphys/kiac003 · OSTI ID:1860449

Li, Xingxing;

;

; Mansoori, Nasim; Yuan, Kai; Speicher, Tori L.;

;

Abstract The common ancestor of seed plants and mosses contained homo-oligomeric cellulose synthesis complexes (CSCs) composed of identical subunits encoded by a single CELLULOSE SYNTHASE (CESA) gene. Seed plants use different CESA isoforms for primary and secondary cell wall deposition. Both primary and secondary CESAs form hetero-oligomeric CSCs that assemble and function in planta only when all the required isoforms are present. The moss Physcomitrium (Physcomitrella) patens has seven CESA genes that can be grouped into two functionally and phylogenetically distinct classes. Previously, we showed that PpCESA3 and/or PpCESA8 (class A) together with PpCESA6 and/or PpCESA7 (class B) form obligate hetero-oligomeric complexes required for normal secondary cell wall deposition. Here, we show that gametophore morphogenesis requires a member of class A, PpCESA5, and is sustained in the absence of other PpCESA isoforms. PpCESA5 also differs from the other class A PpCESAs as it is able to self-interact and does not co-immunoprecipitate with other PpCESA isoforms. These results are consistent with the hypothesis that homo-oligomeric CSCs containing only PpCESA5 subunits synthesize cellulose required for gametophore morphogenesis. Analysis of mutant phenotypes also revealed that, like secondary cell wall deposition, normal protonemal tip growth requires class B isoforms (PpCESA4 or PpCESA10), along with a class A partner (PpCESA3, PpCESA5, or PpCESA8). Thus, P. patens contains both homo-oligomeric and hetero-oligomeric CSCs.

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Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0001090

OSTI ID:: 1860449

Journal Information:: Plant Physiology (Bethesda), Journal Name: Plant Physiology (Bethesda) Journal Issue: 4 Vol. 188; ISSN 0032-0889

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (47)

Two-sided confidence intervals for the single proportion: comparison of seven methods Newcombe, Robert G. Statistics in Medicine, Vol. 17, Issue 8 https://doi.org/10.1002/(SICI)1097-0258(19980430)17:8<857::AID-SIM777>3.0.CO;2-E	journal	April 1998
Efficient and modular CRISPR‐Cas9 vector system for Physcomitrella patens Mallett, Darren R.; Chang, Mingqin; Cheng, Xiaohang Plant Direct, Vol. 3, Issue 9 https://doi.org/10.1002/pld3.168	journal	September 2019
Phenotypic effects of changes in the FTVTxK region of an Arabidopsis secondary wall cellulose synthase compared with results from analogous mutations in other isoforms Burris, Jason N.; Makarem, Mohamadamin; Slabaugh, Erin Plant Direct, Vol. 5, Issue 8 https://doi.org/10.1002/pld3.335	journal	August 2021
Knocking Out the Wall: Protocols for Gene Targeting in Physcomitrella patens Roberts, Alison W.; Dimos, Christos S.; Budziszek, Michael J. Methods in Molecular Biology https://doi.org/10.1007/978-1-61779-008-9_19	book	December 2010
Morphological Analysis of Cell Growth Mutants in Physcomitrella Bibeau, Jeffrey P.; Vidali, Luis Methods in Molecular Biology https://doi.org/10.1007/978-1-62703-643-6_17	book	August 2013
A CELLULOSE SYNTHASE (CESA) gene essential for gametophore morphogenesis in the moss Physcomitrella patens Goss, Chessa A.; Brockmann, Derek J.; Bushoven, John T. Planta, Vol. 235, Issue 6 https://doi.org/10.1007/s00425-011-1579-5	journal	January 2012
Structure/function relationships in the rosette cellulose synthesis complex illuminated by an evolutionary perspective Haigler, Candace H.; Roberts, Alison W. Cellulose, Vol. 26, Issue 1 https://doi.org/10.1007/s10570-018-2157-9	journal	December 2018
The cellulose synthase (CESA) gene superfamily of the moss Physcomitrella patens Roberts, Alison W.; Bushoven, John T. Plant Molecular Biology, Vol. 63, Issue 2 https://doi.org/10.1007/s11103-006-9083-1	journal	September 2006
The Mechanism Forming the Cell Surface of Tip-Growing Rooting Cells Is Conserved among Land Plants Honkanen, Suvi; Jones, Victor A. S.; Morieri, Giulia Current Biology, Vol. 26, Issue 23 https://doi.org/10.1016/j.cub.2016.09.062	journal	December 2016
Interactions between membrane-bound cellulose synthases involved in the synthesis of the secondary cell wall Timmers, Jaap; Vernhettes, Samantha; Desprez, Thierry FEBS Letters, Vol. 583, Issue 6 https://doi.org/10.1016/j.febslet.2009.02.035	journal	March 2009
Physcomitrella patens: a model for tip cell growth and differentiation Vidali, Luis; Bezanilla, Magdalena Current Opinion in Plant Biology, Vol. 15, Issue 6 https://doi.org/10.1016/j.pbi.2012.09.008	journal	December 2012
Plant cellulose synthesis: CESA proteins crossing kingdoms Kumar, Manoj; Turner, Simon Phytochemistry, Vol. 112 https://doi.org/10.1016/j.phytochem.2014.07.009	journal	April 2015
An update on the nomenclature for the cellulose synthase genes in Populus Kumar, Manoj; Thammannagowda, Shivegowda; Bulone, Vincent Trends in Plant Science, Vol. 14, Issue 5 https://doi.org/10.1016/j.tplants.2009.02.004	journal	May 2009
The origin and early evolution of plants on land Kenrick, Paul; Crane, Peter R. Nature, Vol. 389, Issue 6646 https://doi.org/10.1038/37918	journal	September 1997
Evolution of increased complexity in a molecular machine Finnigan, Gregory C.; Hanson-Smith, Victor; Stevens, Tom H. Nature, Vol. 481, Issue 7381 https://doi.org/10.1038/nature10724	journal	January 2012
A ratchet for protein complexity Doolittle, W. Ford Nature, Vol. 481, Issue 7381 https://doi.org/10.1038/nature10816	journal	January 2012
A role for CSLD3 during cell-wall synthesis in apical plasma membranes of tip-growing root-hair cells Park, Sungjin; Szumlanski, Amy L.; Gu, Fangwei Nature Cell Biology, Vol. 13, Issue 8 https://doi.org/10.1038/ncb2294	journal	July 2011
Direct observation of the effects of cellulose synthesis inhibitors using live cell imaging of Cellulose Synthase (CESA) in Physcomitrella patens Tran, Mai L.; McCarthy, Thomas W.; Sun, Hao Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-017-18994-4	journal	January 2018
Efficient gene targeting in the moss Physcomitrella patens Schaefer, Didier G.; Zryd, Jean-Pierre The Plant Journal, Vol. 11, Issue 6 https://doi.org/10.1046/j.1365-313X.1997.11061195.x	journal	June 1997
Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis Persson, S.; Paredez, A.; Carroll, A. Proceedings of the National Academy of Sciences, Vol. 104, Issue 39 https://doi.org/10.1073/pnas.0706592104	journal	September 2007
Rapid formin-mediated actin-filament elongation is essential for polarized plant cell growth Vidali, L.; van Gisbergen, P. A. C.; Guerin, C. Proceedings of the National Academy of Sciences, Vol. 106, Issue 32 https://doi.org/10.1073/pnas.0901170106	journal	July 2009
A single heterologously expressed plant cellulose synthase isoform is sufficient for cellulose microfibril formation in vitro Purushotham, Pallinti; Cho, Sung Hyun; Díaz-Moreno, Sara M. Proceedings of the National Academy of Sciences, Vol. 113, Issue 40 https://doi.org/10.1073/pnas.1606210113	journal	September 2016
Probable Inference, the Law of Succession, and Statistical Inference Wilson, Edwin B. Journal of the American Statistical Association, Vol. 22, Issue 158 https://doi.org/10.1080/01621459.1927.10502953	journal	June 1927
Both chloronemal and caulonemal cells expand by tip growth in the moss Physcomitrella patens Menand, Benoît; Calder, Grant; Dolan, Liam Journal of Experimental Botany, Vol. 58, Issue 7 https://doi.org/10.1093/jxb/erm047	journal	April 2007
Complexes with Mixed Primary and Secondary Cellulose Synthases Are Functional in Arabidopsis Plants Carroll, Andrew; Mansoori, Nasim; Li, Shundai Plant Physiology, Vol. 160, Issue 2 https://doi.org/10.1104/pp.112.199208	journal	August 2012
Pollen Tubes of Nicotiana alata Express Two Genes from Different β-Glucan Synthase Families Doblin, Monika S.; De Melis, Linda; Newbigin, Ed Plant Physiology, Vol. 125, Issue 4 https://doi.org/10.1104/pp.125.4.2040	journal	April 2001
Synthesis and Self-Assembly of Cellulose Microfibrils from Reconstituted Cellulose Synthase Cho, Sung Hyun; Purushotham, Pallinti; Fang, Chao Plant Physiology, Vol. 175, Issue 1 https://doi.org/10.1104/pp.17.00619	journal	August 2017
Functional Specialization of Cellulose Synthase Isoforms in a Moss Shows Parallels with Seed Plants Norris, Joanna H.; Li, Xingxing; Huang, Shixin Plant Physiology, Vol. 175, Issue 1 https://doi.org/10.1104/pp.17.00885	journal	August 2017
Cellulose Synthase Stoichiometry in Aspen Differs from Arabidopsis and Norway Spruce Zhang, Xueyang; Dominguez, Pia Guadalupe; Kumar, Manoj Plant Physiology, Vol. 177, Issue 3 https://doi.org/10.1104/pp.18.00394	journal	May 2018
Profilin Is Essential for Tip Growth in the Moss Physcomitrella patens Vidali, Luis; Augustine, Robert C.; Kleinman, Ken P. The Plant Cell, Vol. 19, Issue 11 https://doi.org/10.1105/tpc.107.053413	journal	November 2007
What Do We Really Know about Cellulose Biosynthesis in Higher Plants? Guerriero, Gea; Fugelstad, Johanna; Bulone, Vincent Journal of Integrative Plant Biology, Vol. 52, Issue 2 https://doi.org/10.1111/j.1744-7909.2010.00935.x	journal	February 2010
Cellulose synthase ‘class specific regions’ are intrinsically disordered and functionally undifferentiated: Intrinsic disorder in cellulose synthases Scavuzzo-Duggan, Tess R.; Chaves, Arielle M.; Singh, Abhishek Journal of Integrative Plant Biology, Vol. 60, Issue 6 https://doi.org/10.1111/jipb.12637	journal	March 2018
Phylogenomic delineation of Physcomitrium (Bryophyta: Funariaceae) based on targeted sequencing of nuclear exons and their flanking regions rejects the retention of Physcomitrella , Physcomitridium and Aphanorrhegma Medina, Rafael; Johnson, Matthew G.; Liu, Yang Journal of Systematics and Evolution, Vol. 57, Issue 4 https://doi.org/10.1111/jse.12516	journal	July 2019
NorWood: a gene expression resource for evo-devo studies of conifer wood development Jokipii-Lukkari, Soile; Sundell, David; Nilsson, Ove New Phytologist, Vol. 216, Issue 2 https://doi.org/10.1111/nph.14458	journal	February 2017
Cellulose synthase gene expression profiling of Physcomitrella patens Tran, M. L.; Roberts, A. W. Plant Biology, Vol. 18, Issue 3 https://doi.org/10.1111/plb.12416	journal	December 2015
The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution Lang, Daniel; Ullrich, Kristian K.; Murat, Florent The Plant Journal, Vol. 93, Issue 3 https://doi.org/10.1111/tpj.13801	journal	January 2018
Convergent evolution of hetero‐oligomeric cellulose synthesis complexes in mosses and seed plants Li, Xingxing; Speicher, Tori L.; Dees, Dianka C. T. The Plant Journal https://doi.org/10.1111/tpj.14366	journal	May 2019
PEATmoss ( Physcomitrella Expression Atlas Tool): a unified gene expression atlas for the model plant Physcomitrella patens Fernandez‐Pozo, Noe; Haas, Fabian B.; Meyberg, Rabea The Plant Journal, Vol. 102, Issue 1 https://doi.org/10.1111/tpj.14607	journal	January 2020
Architecture of a catalytically active homotrimeric plant cellulose synthase complex Purushotham, Pallinti; Ho, Ruoya; Zimmer, Jochen Science, Vol. 369, Issue 6507 https://doi.org/10.1126/science.abb2978	journal	July 2020
The Cell Biology of Cellulose Synthesis McFarlane, Heather E.; Döring, Anett; Persson, Staffan Annual Review of Plant Biology, Vol. 65, Issue 1 https://doi.org/10.1146/annurev-arplant-050213-040240	journal	April 2014
Growth Mechanisms in Tip-Growing Plant Cells Rounds, Caleb M.; Bezanilla, Magdalena Annual Review of Plant Biology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev-arplant-050312-120150	journal	April 2013
The cellulose synthase superfamily in fully sequenced plants and algae Yin, Yanbin; Huang, Jinling; Xu, Ying BMC Plant Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2229-9-99	journal	January 2009
Evaluation of off-target and on-target scoring algorithms and integration into the guide RNA selection tool CRISPOR Haeussler, Maximilian; Schönig, Kai; Eckert, Hélène Genome Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s13059-016-1012-2	journal	July 2016
Understanding Plant Cellulose Synthases through a Comprehensive Investigation of the Cellulose Synthase Family Sequences Carroll, Andrew; Specht, Chelsea D. Frontiers in Plant Science, Vol. 2 https://doi.org/10.3389/fpls.2011.00005	journal	January 2011
Moss cell walls: structure and biosynthesis Roberts, Alison W.; Roberts, Eric M.; Haigler, Candace H. Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00166	journal	January 2012
A Complementation Assay for in Vivo Protein Structure/Function Analysis in Physcomitrella patens (Funariaceae) Scavuzzo-Duggan, Tess R.; Chaves, Arielle M.; Roberts, Alison W. Applications in Plant Sciences, Vol. 3, Issue 7 https://doi.org/10.3732/apps.1500023	journal	July 2015
Functional analysis of complexes with mixed primary and secondary cellulose synthases Li, Shundai; Lei, Lei; Gu, Ying Plant Signaling & Behavior, Vol. 8, Issue 3 https://doi.org/10.4161/psb.23179	journal	March 2013

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