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

Journal Article · · Plant Physiology (Bethesda)

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. Further, 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.

Research Organization:
Northwestern Univ., Evanston, IL (United States); Energy Frontier Research Centers (EFRC) (United States). Center for LignoCellulose Structure and Formation
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); National Institute of General Medical Sciences (NIGMS); National Institutes of Health (NIH)
Grant/Contract Number:
SC0001090; EPS-1004057; P20GM103440; SC0021314; IOS-1257047; MCB-1750359
OSTI ID:
1860449
Alternate ID(s):
OSTI ID: 1841312; OSTI ID: 1865661; OSTI ID: 1915239
Journal Information:
Plant Physiology (Bethesda), Journal Name: Plant Physiology (Bethesda) Vol. 188 Journal Issue: 4; ISSN 0032-0889
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United States
Language:
English

References (45)

Synthesis and Self-Assembly of Cellulose Microfibrils from Reconstituted Cellulose Synthase journal August 2017
A ratchet for protein complexity journal January 2012
Moss cell walls: structure and biosynthesis journal January 2012
Phenotypic effects of changes in the FTVTxK region of an Arabidopsis secondary wall cellulose synthase compared with results from analogous mutations in other isoforms journal August 2021
The Cell Biology of Cellulose Synthesis journal April 2014
Complexes with Mixed Primary and Secondary Cellulose Synthases Are Functional in Arabidopsis Plants journal August 2012
Direct observation of the effects of cellulose synthesis inhibitors using live cell imaging of Cellulose Synthase (CESA) in Physcomitrella patens journal January 2018
Growth Mechanisms in Tip-Growing Plant Cells journal April 2013
Cellulose synthase ‘class specific regions’ are intrinsically disordered and functionally undifferentiated: Intrinsic disorder in cellulose synthases journal March 2018
Probable Inference, the Law of Succession, and Statistical Inference journal June 1927
Rapid formin-mediated actin-filament elongation is essential for polarized plant cell growth journal July 2009
Both chloronemal and caulonemal cells expand by tip growth in the moss Physcomitrella patens journal April 2007
The Mechanism Forming the Cell Surface of Tip-Growing Rooting Cells Is Conserved among Land Plants journal December 2016
Architecture of a catalytically active homotrimeric plant cellulose synthase complex journal July 2020
Cellulose synthase gene expression profiling of Physcomitrella patens journal December 2015
Cellulose Synthase Stoichiometry in Aspen Differs from Arabidopsis and Norway Spruce journal May 2018
NorWood: a gene expression resource for evo-devo studies of conifer wood development journal February 2017
Interactions between membrane-bound cellulose synthases involved in the synthesis of the secondary cell wall journal March 2009
Profilin Is Essential for Tip Growth in the Moss Physcomitrella patens journal November 2007
A Complementation Assay for in Vivo Protein Structure/Function Analysis in Physcomitrella patens (Funariaceae) journal July 2015
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 journal July 2019
Physcomitrella patens: a model for tip cell growth and differentiation journal December 2012
The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution journal January 2018
Efficient and modular CRISPR‐Cas9 vector system for Physcomitrella patens journal September 2019
The origin and early evolution of plants on land journal September 1997
Efficient gene targeting in the moss Physcomitrella patens journal June 1997
Understanding Plant Cellulose Synthases through a Comprehensive Investigation of the Cellulose Synthase Family Sequences journal January 2011
Pollen Tubes of Nicotiana alata Express Two Genes from Different β-Glucan Synthase Families journal April 2001
An update on the nomenclature for the cellulose synthase genes in Populus journal May 2009
Evolution of increased complexity in a molecular machine journal January 2012
Functional Specialization of Cellulose Synthase Isoforms in a Moss Shows Parallels with Seed Plants journal August 2017
Plant cellulose synthesis: CESA proteins crossing kingdoms journal April 2015
Two-sided confidence intervals for the single proportion: comparison of seven methods journal April 1998
The cellulose synthase (CESA) gene superfamily of the moss Physcomitrella patens journal September 2006
Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis journal September 2007
The cellulose synthase superfamily in fully sequenced plants and algae journal January 2009
Convergent evolution of hetero‐oligomeric cellulose synthesis complexes in mosses and seed plants journal May 2019
A role for CSLD3 during cell-wall synthesis in apical plasma membranes of tip-growing root-hair cells journal July 2011
Structure/function relationships in the rosette cellulose synthesis complex illuminated by an evolutionary perspective journal December 2018
PEATmoss ( Physcomitrella Expression Atlas Tool): a unified gene expression atlas for the model plant Physcomitrella patens journal January 2020
Evaluation of off-target and on-target scoring algorithms and integration into the guide RNA selection tool CRISPOR journal July 2016
Functional analysis of complexes with mixed primary and secondary cellulose synthases journal March 2013
A CELLULOSE SYNTHASE (CESA) gene essential for gametophore morphogenesis in the moss Physcomitrella patens journal January 2012
What Do We Really Know about Cellulose Biosynthesis in Higher Plants? journal February 2010
A single heterologously expressed plant cellulose synthase isoform is sufficient for cellulose microfibril formation in vitro journal September 2016