Hetero-trans-β-Glucanase Produces Cellulose–Xyloglucan Covalent Bonds in the Cell Walls of Structural Plant Tissues and Is Stimulated by Expansin

Herburger, Klaus; Franková, Lenka; Pičmanová, Martina; Loh, Jia Wooi; Valenzuela-Ortega, Marcos; Meulewaeter, Frank; Hudson, Andrew; French, Christopher E.; Fry, Stephen C.

doi:10.1016/j.molp.2020.04.011

Cited by 34 publications

(37 citation statements)

References 71 publications

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“…The Plant Journal, (2021), 105, 1549-1565 strongest on cellulose I and at low pH agrees with recent results showing that bacterial expansin strongly augments cellulose hetero-transglucosylation (Herburger et al, 2020a).…”

Section: Plant Extracts Contain Cxe Activity Enhancerssupporting

confidence: 90%

“…alkali-untreated filter paper). As expected (Simmons et al, 2015;Herburger et al, 2020a), the measured CXE activity on pure cellulose I was only approximately 9% of that on pure cellulose II (Figure 2c), confirming that alkali-pre-treatment increases the accessibility of cellulose to EfHTG. Infiltrating hemicelluloses into cellulose I (followed by washing away the loosely bound hemicelluloses) had little if any effect on measured CXE activity.…”

Section: Efhtg Can Simultaneously Act On Cellulose and Tightly Bound supporting

confidence: 76%

“…Since 10 m m cellobiose specifically inhibits hetero‐transglucanase (MXE and CXE) activity and action in vitro and in situ , while having little effect on XET activity or action (Figures 6 and 7d), we wanted to explore its effect on whole Equisetum plants, which exhibit extractable Ef HTG activities and actions throughout its stems (Herburger et al ., 2020a). We hydroponically cultured rapidly elongating Equisetum stems, still connected to rhizome segments, in pond water (Figure 7c).…”

Section: Resultsmentioning

confidence: 99%

“…XXXGol) follows Fry et al, (1993)). Radiolabelled XyG ([ 3 H]XyG) was prepared according to Herburger et al (2020a). Other chemicals were purchased mainly from Sigma-Aldrich (Poole, UK).…”

Section: Inhibiting Cellulose Hetero-transglucosylationmentioning

confidence: 99%

“…Testing in-situ transglucanase actions in presence of cellobiose An assay for quantifying XET, MXE and CXE action in native plant cell walls was described in detail previously (Herburger et al, 2020a). Briefly, mature Equisetum stems (approximately 250 mg) were sectioned with a razor blade and incubated with 50 kBq [ 3 H] XXXGol (in 750 µl 25 mM succinate (Na + ) + 0.1% (w/v) chlorobutanol with or without 10 mM cellobiose) for 24 h, and after the reaction had been stopped with 0.5% formic acid in 96% ethanol, specimens were washed thoroughly with ethanol (90-30%).…”

Section: Assaying Radioactivitymentioning

confidence: 99%

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Defining natural factors that stimulate and inhibit cellulose:xyloglucan hetero‐transglucosylation

et al. 2021

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Certain transglucanases can covalently graft cellulose and mixed-linkage b-glucan (MLG) as donor substrates onto xyloglucan as acceptor substrate and thus exhibit cellulose:xyloglucan endotransglucosylase (CXE) and MLG:xyloglucan endotransglucosylase (MXE) activities in vivo and in vitro. However, missing information on factors that stimulate or inhibit these hetero-transglucosylation reactions limits our insight into their biological functions. To explore factors that influence hetero-transglucosylation, we studied Equisetum fluviatile hetero-trans-b-glucanase (EfHTG), which exhibits both CXE and MXE activity, exceeding its xyloglucan:xyloglucan homo-transglucosylation (XET) activity. Enzyme assays employed radiolabelled and fluorescently labelled oligomeric acceptor substrates, and were conducted in vitro and in cell walls (in situ). With whole denatured Equisetum cell walls as donor substrate, exogenous EfHTG (extracted from Equisetum or produced in Pichia) exhibited all three activities (CXE, MXE, XET) in competition with each other. Acting on pure cellulose as donor substrate, the CXE action of Pichia-produced EfHTG was up to approximately 300% increased by addition of methanol-boiled Equisetum extracts; there was no similar effect when the same enzyme acted on soluble donors (MLG or xyloglucan). The methanol-stable factor is proposed to be expansin-like, a suggestion supported by observations of pH dependence. Screening numerous low-molecular-weight compounds for hetero-transglucanase inhibition showed that cellobiose was highly effective, inhibiting the abundant endogenous CXE and MXE (but not XET) action in Equisetum internodes. Furthermore, cellobiose retarded Equisetum stem elongation, potentially owing to its effect on hetero-transglucosylation reactions. This work provides insight and tools to further study the role of cellulose hetero-transglucosylation in planta by identifying factors that govern this reaction.

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Section: Plant Extracts Contain Cxe Activity Enhancerssupporting

confidence: 90%

Section: Efhtg Can Simultaneously Act On Cellulose and Tightly Bound supporting

confidence: 76%

Section: Resultsmentioning

confidence: 99%

“…XXXGol) follows Fry et al, (1993)). Radiolabelled XyG ([ 3 H]XyG) was prepared according to Herburger et al (2020a). Other chemicals were purchased mainly from Sigma-Aldrich (Poole, UK).…”

Section: Inhibiting Cellulose Hetero-transglucosylationmentioning

confidence: 99%

Section: Assaying Radioactivitymentioning

confidence: 99%

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Defining natural factors that stimulate and inhibit cellulose:xyloglucan hetero‐transglucosylation

et al. 2021

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Plant Cell Growth and Cell Wall Enlargement

Cosgrove¹

2022

Encyclopedia of Life Sciences

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Irreversible cell enlargement begins with cell wall loosening which induces wall stress relaxation, leading to cell water uptake and cell enlargement. Growing cell walls consist of a cohesive network of cellulose microfibrils embedded in hydrophilic pectins and cellulose‐binding hemicelluloses. Models of the growing cell wall are provisional hypotheses about how these wall polymers interact to make a strong yet extensible wall. Recent results clarify how wall strength, plasticity and elasticity depend mostly on the stretching, straightening and sliding of cellulose microfibril networks in the wall. Passive sliding of cellulose microfibrils is facilitated by nonenzymic proteins named expansins while various enzymes modify pectins and hemicelluloses, altering their interactions with each other and with cellulose. Growth cessation is correlated with reduced expression of genes that promote wall loosening as well as changes in the direction of cellulose deposition and the structure of matrix polysaccharides, leading to a less extensible cell wall. Key Concepts Irreversible cell enlargement is an essential aspect of plant growth and morphogenesis. Surface enlargement of the cell wall may be highly localised, as in tip‐growing cells, or more evenly distributed over the cell wall surface, a ‘diffuse growth’ pattern common to most cells in the plant body. Cells typically enlarge substantially after they leave the meristem and before they differentiate into mature cells. Cell growth entails simultaneous uptake of water into the cell and irreversible expansion of the cell wall. In physical terms, growth begins with molecular loosening of the cell wall which leads to wall stress relaxation ; this creates the water potential difference needed for water uptake by the cell, resulting in physical enlargement of the cell. The growing cell wall is composed of a strong noncovalent network of cellulose microfibrils embedded in highly hydrated pectins and hemicelluloses that comprise the soft wall matrix. The tensile (in‐plane) mechanics of growing walls is largely determined by the behaviour of the cellulose microfibril network while pectins influence the indentation (out‐of‐plane) mechanics. Growing plant cell walls typically enlarge more rapidly at low pH (called ‘acid growth’), a process that is mediated by nonenzymatic proteins named α‐expansins; α‐expansins facilitate the passive sliding of a network of cellulose microfibrils in response to tensile wall stresses originating from cell turgor pressure. Deposition of new polymers to the wall is usually coordinated with surface expansion, but these are separable processes. Several classes of enzymes modify the structure of pectins and hemicelluloses in the cell wall, potentially affecting cell wall structure and mechanics. Cell wall mechanical properties are complex, encompassing a number of different physical behaviours that often are not well correlated with each other or with cell wall growth. Cessation of cell enlargement likely involves multiple processes, including changes in the direction of cellulose deposition, stiffening of cellulose and matrix networks, and reduced expression of wall loosening proteins.

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Combinatorial treatment with β-glucanase enzyme and chlorhexidine induces cysticidal effects in Acanthamoeba cyst

et al. 2022

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Hetero-trans-β-Glucanase Produces Cellulose–Xyloglucan Covalent Bonds in the Cell Walls of Structural Plant Tissues and Is Stimulated by Expansin

Cited by 34 publications

References 71 publications

Defining natural factors that stimulate and inhibit cellulose:xyloglucan hetero‐transglucosylation

Defining natural factors that stimulate and inhibit cellulose:xyloglucan hetero‐transglucosylation

Plant Cell Growth and Cell Wall Enlargement

Combinatorial treatment with β-glucanase enzyme and chlorhexidine induces cysticidal effects in Acanthamoeba cyst

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