Empirical evidence that glucan-interacting amino acid side chains within the transmembrane channel collectively facilitate cellulose synthase function

Kwansa, Albert L.; Chaves, Arielle M.; Del Mundo, Joshua T.; Pierce, Ethan T.; Gomez, Esther W.; Gomez, Enrique D.; Haigler, Candace H.; Yingling, Yaroslava G.; Roberts, Alison W.

doi:10.1007/s11103-025-01615-4

Empirical evidence that glucan-interacting amino acid side chains within the transmembrane channel collectively facilitate cellulose synthase function

Journal Article · Wed Jul 09 00:00:00 EDT 2025 · Plant Molecular Biology

DOI:https://doi.org/10.1007/s11103-025-01615-4· OSTI ID:2997619

Kwansa, Albert L. ^[1]; Chaves, Arielle M. ^[2]; Del Mundo, Joshua T. ^[3]; Pierce, Ethan T. ^[1]; Gomez, Esther W. ^[3]; Gomez, Enrique D. ^[3]; Haigler, Candace H. ^[1]; Yingling, Yaroslava G. ^[1]; ^[2]

North Carolina State University, Raleigh, NC (United States)
University of Rhode Island, Kingston, RI (United States)
The Pennsylvania State University, University Park, PA (United States)

The fundamental mechanism of cellulose synthesis is widely conserved across Kingdoms and depends on cellulose synthases, which are processive, dual-function, family 2 glycosyltransferases (GT-2). These enzymes polymerize glucose on the cytoplasmic side of the plasma membrane and export the glucan chain to the cell surface through an integral transmembrane (TM) channel. Structural studies of active plant cellulose synthases (CESAs) have revealed interactions between the nascent glucan chain and the side chains of polar, charged, and aromatic amino acid residues that line the TM channel. However, the functional consequences of modifying these side chains have not been tested in vivo in CESAs or other processive GT-2s. To test this, we used an established in vivo assay based on genetic complementation of CESA5 in the moss, Physcomitrium patens. For accurate prediction of glucan-interacting amino acid residues, we generated a complete homotrimeric molecular model of PpCESA5 using a combination of homology and de novo modeling. All-atom molecular dynamics-based analyses of contact metrics and interaction energy identified 23 amino acid residues with high propensity to interact with the nascent glucan chain within the TM channel or on the apoplastic surface of PpCESA5. Mutating any one of 18 of these amino acid residues to alanine, thereby removing their side chains, abolished or impaired CESA function, with the strongest effects observed upon the loss of charged amino acid side chains. This provides direct evidence to support the hypothesis that multiple amino acid residues collectively maintain a smooth energy landscape within the TM channel to facilitate glucan translocation.

View Accepted Manuscript (DOE)

Research Organization:: The Pennsylvania State University, University Park, PA (United States)

Sponsoring Organization:: National Institute of General Medical Sciences of the National Institutes of Health; USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-05CH11231; SC0001090

OSTI ID:: 2997619

Journal Information:: Plant Molecular Biology, Journal Name: Plant Molecular Biology Journal Issue: 4 Vol. 115; ISSN 1573-5028; ISSN 0167-4412

Publisher:: Springer Science and Business Media LLCCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
Cellulose microfibril
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Empirical evidence that glucan-interacting amino acid side chains within the transmembrane channel collectively facilitate cellulose synthase function

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