Comparative Structural and Computational Analysis Supports Eighteen Cellulose Synthases in the Plant Cellulose Synthesis Complex

B. Tracy Nixon; Katayoun Mansouri; Abhishek Singh; Juan Du; Jonathan K. Davis; Jung Goo Lee; Erin Slabaugh; Venu Gopal Vandavasi; Hugh O'Neill; Eric M. Roberts; Alison W. Roberts; Yaroslava G. Yingling; Candace H. Haigler

doi:10.1038/srep28696

Comparative Structural and Computational Analysis Supports Eighteen Cellulose Synthases in the Plant Cellulose Synthesis Complex

B. Tracy Nixon, Katayoun Mansouri, Abhishek Singh, Juan Du, Jonathan K. Davis, Jung Goo Lee, Erin Slabaugh, Venu Gopal Vandavasi, Hugh O'Neill, Eric M. Roberts, Alison W. Roberts, Yaroslava G. Yingling, Candace H. Haigler

Biochemistry & Molecular Biology

Research output: Contribution to journal › Article › peer-review

163 Scopus citations

Abstract

A six-lobed membrane spanning cellulose synthesis complex (CSC) containing multiple cellulose synthase (CESA) glycosyltransferases mediates cellulose microfibril formation. The number of CESAs in the CSC has been debated for decades in light of changing estimates of the diameter of the smallest microfibril formed from the β-1,4 glucan chains synthesized by one CSC. We obtained more direct evidence through generating improved transmission electron microscopy (TEM) images and image averages of the rosette-type CSC, revealing the frequent triangularity and average cross-sectional area in the plasma membrane of its individual lobes. Trimeric oligomers of two alternative CESA computational models corresponded well with individual lobe geometry. A six-fold assembly of the trimeric computational oligomer had the lowest potential energy per monomer and was consistent with rosette CSC morphology. Negative stain TEM and image averaging showed the triangularity of a recombinant CESA cytosolic domain, consistent with previous modeling of its trimeric nature from small angle scattering (SAXS) data. Six trimeric SAXS models nearly filled the space below an average FF-TEM image of the rosette CSC. In summary, the multifaceted data support a rosette CSC with 18 CESAs that mediates the synthesis of a fundamental microfibril composed of 18 glucan chains.

Original language	English (US)
Article number	28696
Journal	Scientific reports
Volume	6
DOIs	https://doi.org/10.1038/srep28696
State	Published - Jun 27 2016

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Nixon, B. T., Mansouri, K., Singh, A., Du, J., Davis, J. K., Lee, J. G., Slabaugh, E., Vandavasi, V. G., O'Neill, H., Roberts, E. M., Roberts, A. W., Yingling, Y. G., & Haigler, C. H. (2016). Comparative Structural and Computational Analysis Supports Eighteen Cellulose Synthases in the Plant Cellulose Synthesis Complex. Scientific reports, 6, Article 28696. https://doi.org/10.1038/srep28696

@article{930175c5055b4419a51421c1e99c782f,

title = "Comparative Structural and Computational Analysis Supports Eighteen Cellulose Synthases in the Plant Cellulose Synthesis Complex",

abstract = "A six-lobed membrane spanning cellulose synthesis complex (CSC) containing multiple cellulose synthase (CESA) glycosyltransferases mediates cellulose microfibril formation. The number of CESAs in the CSC has been debated for decades in light of changing estimates of the diameter of the smallest microfibril formed from the β-1,4 glucan chains synthesized by one CSC. We obtained more direct evidence through generating improved transmission electron microscopy (TEM) images and image averages of the rosette-type CSC, revealing the frequent triangularity and average cross-sectional area in the plasma membrane of its individual lobes. Trimeric oligomers of two alternative CESA computational models corresponded well with individual lobe geometry. A six-fold assembly of the trimeric computational oligomer had the lowest potential energy per monomer and was consistent with rosette CSC morphology. Negative stain TEM and image averaging showed the triangularity of a recombinant CESA cytosolic domain, consistent with previous modeling of its trimeric nature from small angle scattering (SAXS) data. Six trimeric SAXS models nearly filled the space below an average FF-TEM image of the rosette CSC. In summary, the multifaceted data support a rosette CSC with 18 CESAs that mediates the synthesis of a fundamental microfibril composed of 18 glucan chains.",

author = "Nixon, {B. Tracy} and Katayoun Mansouri and Abhishek Singh and Juan Du and Davis, {Jonathan K.} and Lee, {Jung Goo} and Erin Slabaugh and Vandavasi, {Venu Gopal} and Hugh O'Neill and Roberts, {Eric M.} and Roberts, {Alison W.} and Yingling, {Yaroslava G.} and Haigler, {Candace H.}",

note = "Funding Information: This work was supported as part of The Center for LignoCellulose Structure and Formation, an Energy Frontier Research Center funded by the U.S. Department of Energy, Office of Science, Basic Energy Sciences under Award # DE-SC0001090. We thank Ethan Pierce for assistance with measurements and compiling Fig. 2 and Table 1 and Zhen Zheng for help with initial particle picking.",

year = "2016",

month = jun,

day = "27",

doi = "10.1038/srep28696",

language = "English (US)",

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journal = "Scientific reports",

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T1 - Comparative Structural and Computational Analysis Supports Eighteen Cellulose Synthases in the Plant Cellulose Synthesis Complex

AU - Nixon, B. Tracy

AU - Mansouri, Katayoun

AU - Singh, Abhishek

AU - Du, Juan

AU - Davis, Jonathan K.

AU - Lee, Jung Goo

AU - Slabaugh, Erin

AU - Vandavasi, Venu Gopal

AU - O'Neill, Hugh

AU - Roberts, Eric M.

AU - Roberts, Alison W.

AU - Yingling, Yaroslava G.

AU - Haigler, Candace H.

N1 - Funding Information: This work was supported as part of The Center for LignoCellulose Structure and Formation, an Energy Frontier Research Center funded by the U.S. Department of Energy, Office of Science, Basic Energy Sciences under Award # DE-SC0001090. We thank Ethan Pierce for assistance with measurements and compiling Fig. 2 and Table 1 and Zhen Zheng for help with initial particle picking.

PY - 2016/6/27

Y1 - 2016/6/27

N2 - A six-lobed membrane spanning cellulose synthesis complex (CSC) containing multiple cellulose synthase (CESA) glycosyltransferases mediates cellulose microfibril formation. The number of CESAs in the CSC has been debated for decades in light of changing estimates of the diameter of the smallest microfibril formed from the β-1,4 glucan chains synthesized by one CSC. We obtained more direct evidence through generating improved transmission electron microscopy (TEM) images and image averages of the rosette-type CSC, revealing the frequent triangularity and average cross-sectional area in the plasma membrane of its individual lobes. Trimeric oligomers of two alternative CESA computational models corresponded well with individual lobe geometry. A six-fold assembly of the trimeric computational oligomer had the lowest potential energy per monomer and was consistent with rosette CSC morphology. Negative stain TEM and image averaging showed the triangularity of a recombinant CESA cytosolic domain, consistent with previous modeling of its trimeric nature from small angle scattering (SAXS) data. Six trimeric SAXS models nearly filled the space below an average FF-TEM image of the rosette CSC. In summary, the multifaceted data support a rosette CSC with 18 CESAs that mediates the synthesis of a fundamental microfibril composed of 18 glucan chains.

AB - A six-lobed membrane spanning cellulose synthesis complex (CSC) containing multiple cellulose synthase (CESA) glycosyltransferases mediates cellulose microfibril formation. The number of CESAs in the CSC has been debated for decades in light of changing estimates of the diameter of the smallest microfibril formed from the β-1,4 glucan chains synthesized by one CSC. We obtained more direct evidence through generating improved transmission electron microscopy (TEM) images and image averages of the rosette-type CSC, revealing the frequent triangularity and average cross-sectional area in the plasma membrane of its individual lobes. Trimeric oligomers of two alternative CESA computational models corresponded well with individual lobe geometry. A six-fold assembly of the trimeric computational oligomer had the lowest potential energy per monomer and was consistent with rosette CSC morphology. Negative stain TEM and image averaging showed the triangularity of a recombinant CESA cytosolic domain, consistent with previous modeling of its trimeric nature from small angle scattering (SAXS) data. Six trimeric SAXS models nearly filled the space below an average FF-TEM image of the rosette CSC. In summary, the multifaceted data support a rosette CSC with 18 CESAs that mediates the synthesis of a fundamental microfibril composed of 18 glucan chains.

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Comparative Structural and Computational Analysis Supports Eighteen Cellulose Synthases in the Plant Cellulose Synthesis Complex

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