Functional analysis of complexes with mixed primary and secondary cellulose synthases

Li, Shundai; Lei, Lei; Gu, Ying

doi:10.4161/psb.23179

Cited by 27 publications

(20 citation statements)

References 20 publications

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“…The MbYTH assay detected dimerization of membrane proteins expressed in yeast (Fetchko and Stagljar, ). Results from previous MbYTH studies with AtCESAs have not been fully consistent (Timmers et al ., ; Carroll et al ., ; Li et al ., ), highlighting the importance of corroborating these findings with other methods. The BiFC assay (Hu et al ., ; Walter et al ., ) detected interactions within plant membranes and has also been used to test interactions among AtCESAs (Desprez et al ., ; Timmers et al ., ; Carroll et al ., ).…”

Section: Discussionsupporting

confidence: 55%

“…In contrast, AtCESA1 , AtCESA3 , and AtCESA6‐ like genes are implicated in primary cell wall cellulose deposition (Arioli et al ., ; Fagard et al ., ; Scheible et al ., ; Burn et al ., ; Robert et al ., ; Desprez et al ., ; Persson et al ., ). MbYTH, Co‐IP, and BiFC experiments demonstrated in vivo and in vitro interaction among proteins encoded by these genes (Desprez et al ., ; Carroll et al ., ; Li et al ., ). As for secondary cell wall AtCESAs , AtCESA1 and AtCESA3 are non‐redundant, whereas AtCESA6 is partially redundant with AtCESA2 and AtCESA5 (Desprez et al ., ; Persson et al ., ).…”

Section: Introductionmentioning

confidence: 97%

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Convergent evolution of hetero‐oligomeric cellulose synthesis complexes in mosses and seed plants

Speicher

Dees

et al. 2019

The Plant Journal

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Summary In seed plants, cellulose is synthesized by rosette‐shaped cellulose synthesis complexes (CSCs) that are obligate hetero‐oligomeric, comprising three non‐interchangeable cellulose synthase (CESA) isoforms. The moss Physcomitrella patens has rosette CSCs and seven CESAs, but its common ancestor with seed plants had rosette CSCs and a single CESA gene. Therefore, if P. patens CSCs are hetero‐oligomeric, then CSCs of this type evolved convergently in mosses and seed plants. Previous gene knockout and promoter swap experiments showed that PpCESAs from class A (PpCESA3 and PpCESA8) and class B (PpCESA6 and PpCESA7) have non‐redundant functions in secondary cell wall cellulose deposition in leaf midribs, whereas the two members of each class are redundant. Based on these observations, we proposed the hypothesis that the secondary class A and class B PpCESAs associate to form hetero‐oligomeric CSCs. Here we show that transcription of secondary class A PpCESAs is reduced when secondary class B PpCESAs are knocked out and vice versa, as expected for genes encoding isoforms that occupy distinct positions within the same CSC. The class A and class B isoforms co‐accumulate in developing gametophores and co‐immunoprecipitate, suggesting that they interact to form a complex in planta. Finally, secondary PpCESAs interact with each other, whereas three of four fail to self‐interact when expressed in two different heterologous systems. These results are consistent with the hypothesis that obligate hetero‐oligomeric CSCs evolved independently in mosses and seed plants and we propose the constructive neutral evolution hypothesis as a plausible explanation for convergent evolution of hetero‐oligomeric CSCs.

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Section: Discussionsupporting

confidence: 55%

Section: Introductionmentioning

confidence: 97%

Convergent evolution of hetero‐oligomeric cellulose synthesis complexes in mosses and seed plants

Speicher

Dees

et al. 2019

The Plant Journal

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“…Cells that undergo SCW biosynthesis have to transition from PCW biosynthesis, representing a stage where PCW CSCs could coexist with those of the SCW. This opens the possibility that CESAs from canonically different CSCs could mix, a hypothesis supported by promoter-swap studies demonstrating the ability for CESA1 to partially complement the cesa8 null allele (Carroll et al, 2012;Li et al, 2013). If significant mixing were to occur under native conditions, it would likely alter the whole-cell stoichiometry of CESA4, CESA7, and CESA8.…”

Section: Scw Cesa Stoichiometry Is Fixed Through Stem Developmentmentioning

confidence: 99%

The Arabidopsis Cellulose Synthase Complex: A Proposed Hexamer of CESA Trimers in an Equimolar Stoichiometry

2014

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Cellulose is the most abundant renewable polymer on Earth and a major component of the plant cell wall. In vascular plants, cellulose synthesis is catalyzed by a large, plasma membrane-localized cellulose synthase complex (CSC), visualized as a hexameric rosette structure. Three unique cellulose synthase (CESA) isoforms are required for CSC assembly and function. However, elucidation of either the number or stoichiometry of CESAs within the CSC has remained elusive. In this study, we show a 1:1:1 stoichiometry between the three Arabidopsis thaliana secondary cell wall isozymes: CESA4, CESA7, and CESA8. This ratio was determined utilizing a simple but elegant method of quantitative immunoblotting using isoform-specific antibodies and 35 S-labeled protein standards for each CESA. Additionally, the observed equimolar stoichiometry was found to be fixed along the axis of the stem, which represents a developmental gradient. Our results complement recent spectroscopic analyses pointing toward an 18-chain cellulose microfibril. Taken together, we propose that the CSC is composed of a hexamer of catalytically active CESA trimers, with each CESA in equimolar amounts. This finding is a crucial advance in understanding how CESAs integrate to form higher order complexes, which is a key determinate of cellulose microfibril and cell wall properties.

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“…Very recently, a split-ubiquitin membrane yeast twohybrid system demonstrated interactions between the four primary CESAs (CESA1, CESA2, CESA3, CESA6) and three secondary CESAs (CESA4, CESA7, CESA8) but also between the primary CESAs and secondary CESAs in a limited fashion. Further functional analysis of transgenic lines showed that CESA1 could partially rescue irx1 (ce-sa8) null mutants, resulting in complementation of the plant growth defect and cellulose content deficiency [87]. The interactions between these enzymes were shown to utilize both disulfide bonds and non-covalent interactions [88].…”

Section: Complexes Involved In Cell Wall Glycan and Starch Synthesismentioning

confidence: 99%

Glycosyltransferase complexes in eukaryotes: long-known, prevalent but still unrecognized

Kellokumpu

Hassinen

Glumoff

2015

Cell. Mol. Life Sci.

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Glycosylation is the most common and complex cellular modification of proteins and lipids. It is critical for multicellular life and its abrogation often leads to a devastating disease. Yet, the underlying mechanistic details of glycosylation in both health and disease remain unclear. Partly, this is due to the complexity and dynamicity of glycan modifications, and the fact that not all the players are taken into account. Since late 1960s, a vast number of studies have demonstrated that glycosyltransferases typically form homomeric and heteromeric complexes with each other in yeast, plant and animal cells. To propagate their acceptance, we will summarize here accumulated data for their prevalence and potential functional importance for glycosylation focusing mainly on their mutual interactions, the protein domains mediating these interactions, and enzymatic activity changes that occur upon complex formation. Finally, we will highlight the few existing 3D structures of these enzyme complexes to pinpoint their individual nature and to emphasize that their lack is the main obstacle for more detailed understanding of how these enzyme complexes interact and function in a eukaryotic cell.

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Functional analysis of complexes with mixed primary and secondary cellulose synthases

Cited by 27 publications

References 20 publications

Convergent evolution of hetero‐oligomeric cellulose synthesis complexes in mosses and seed plants

Convergent evolution of hetero‐oligomeric cellulose synthesis complexes in mosses and seed plants

The Arabidopsis Cellulose Synthase Complex: A Proposed Hexamer of CESA Trimers in an Equimolar Stoichiometry

Glycosyltransferase complexes in eukaryotes: long-known, prevalent but still unrecognized

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