Structural Organization and a Standardized Nomenclature for Plant Endo-1,4-<i>β</i>-Glucanases (Cellulases) of Glycosyl Hydrolase Family 9

Urbanowicz, Breeanna R.; Bennett, A. B.; Campillo, Elena del; Catalá, Carmen; Hayashi, Takahisa; Henrissat, Bernard; Höfte, Monica; McQueen‐Mason, Simon J.; Patterson, Sara E.; Shoseyov, Oded; Teeri, Tuula T.; Rose, Jocelyn K. C.

doi:10.1104/pp.107.102574

Cited by 97 publications

(86 citation statements)

References 20 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…These observations have potentially important implications for present models of primary plant cell wall biosynthesis and maturation, in which transglycosylation has been considered to be the preeminent xyloglucan-remodeling activity (Rose et al, 2002;Eklöf and Brumer, 2010). Although general endoglucanase (cellulase) activity has long been postulated to have a role in wall loosening (Fry, 1989;Rose and Bennett, 1999;Urbanowicz et al, 2007;Vicente et al, 2007), our results directly implicate the action of endogenous xyloglucan-specific hydrolases from glycoside hydrolase family 16 in the apoplastic arena. However, these results do not support XEHs as major actors in controlling cell wall extension.…”

Section: Resultsmentioning

confidence: 55%

Group III-AXTHGenes of Arabidopsis Encode Predominant Xyloglucan Endohydrolases That Are Dispensable for Normal Growth

et al. 2012

View full text Add to dashboard Cite

The molecular basis of primary wall extension endures as one of the central enigmas in plant cell morphogenesis. Classical cell wall models suggest that xyloglucan endo-transglycosylase activity is the primary catalyst (together with expansins) of controlled cell wall loosening through the transient cleavage and religation of xyloglucan-cellulose cross links. The genome of Arabidopsis (Arabidopsis thaliana) contains 33 phylogenetically diverse XYLOGLUCAN ENDO-TRANSGLYCOSYLASE/ HYDROLASE (XTH) gene products, two of which were predicted to be predominant xyloglucan endohydrolases due to clustering into group III-A. Enzyme kinetic analysis of recombinant AtXTH31 confirmed this prediction and indicated that this enzyme had similar catalytic properties to the nasturtium (Tropaeolum majus) xyloglucanase1 responsible for storage xyloglucan hydrolysis during germination. Global analysis of Genevestigator data indicated that AtXTH31 and the paralogous AtXTH32 were abundantly expressed in expanding tissues. Microscopy analysis, utilizing the resorufin b-glycoside of the xyloglucan oligosaccharide XXXG as an in situ probe, indicated significant xyloglucan endohydrolase activity in specific regions of both roots and hypocotyls, in good correlation with transcriptomic data. Moreover, this hydrolytic activity was essentially completely eliminated in AtXTH31/AtXTH32 double knockout lines. However, single and double knockout lines, as well as individual overexpressing lines, of AtXTH31 and AtXTH32 did not demonstrate significant growth or developmental phenotypes. These results suggest that although xyloglucan polysaccharide hydrolysis occurs in parallel with primary wall expansion, morphological effects are subtle or may be compensated by other mechanisms. We hypothesize that there is likely to be an interplay between these xyloglucan endohydrolases and recently discovered apoplastic exo-glycosidases in the hydrolytic modification of matrix xyloglucans.

show abstract

Section: Resultsmentioning

confidence: 55%

Group III-AXTHGenes of Arabidopsis Encode Predominant Xyloglucan Endohydrolases That Are Dispensable for Normal Growth

et al. 2012

View full text Add to dashboard Cite

show abstract

“…Discounting predicted starch-and chitin-cleaving enzymes, four known retaining GH families contain demonstrated endo-polysaccharidases: GH5 (mannanases, glucanases, galactanases), GH10 (xylanases), GH16 (xyloglucanases), and GH17 (b-1,3 glucanases). In contrast, for example, the 25 GH9 members (predicted endo-glucanases; Urbanowicz et al, 2007) and 67 GH28 members (pre-dicted galacturonidases) from Arabidopsis utilize the inverting glycosidase mechanism, which only allows polysaccharide hydrolysis (Sinnott, 1990). It will be interesting to see if future functional studies uncover new CAZy families in plants with polysaccharide rearrangement activities.…”

Section: Other Transglycosylases In Plantsmentioning

confidence: 99%

The XTH Gene Family: An Update on Enzyme Structure, Function, and Phylogeny in Xyloglucan Remodeling

2010

View full text Add to dashboard Cite

“…Arabidopsis thaliana encodes at least 25 EGases, comprising members that are membrane anchored (class A), secreted to the cell wall (class B), or secreted and have a CBM49 carbohydrate binding module (class C) (Urbanowicz et al, 2007). While certain microbial EGases degrade crystalline cellulose, plant EGases are unable to hydrolyze crystalline cellulose.…”

Section: Introductionmentioning

confidence: 99%

“…While certain microbial EGases degrade crystalline cellulose, plant EGases are unable to hydrolyze crystalline cellulose. However, endoglucanase activity for class C EGases has been observed with various substrates, including xyloglucan, xylan, glucomannans, mixed-linkage glucans, and soluble cellulose derivatives such as carboxymethyl cellulose (CMC) and noncrystalline phosphoric acid-swollen cellulose (Master et al, 2004;Yoshida et al, 2006;Urbanowicz et al, 2007). Arabidopsis GH9A1/KORRIGAN1 (KOR1) belongs to class A type II integral membrane EGases, consisting of a cytoplasmic domain, a single transmembrane domain, and an extracellular catalytic domain.…”

Section: Introductionmentioning

confidence: 99%

Thejiaoyao1Mutant Is an Allele ofkorrigan1That Abolishes Endoglucanase Activity and Affects the Organization of Both Cellulose Microfibrils and Microtubules inArabidopsis

et al. 2014

View full text Add to dashboard Cite

In higher plants, cellulose is synthesized by plasma membrane-localized cellulose synthase complexes (CSCs). Arabidopsis thaliana GH9A1/KORRIGAN1 is a membrane-bound, family 9 glycosyl hydrolase that is important for cellulose synthesis in both primary and secondary cell walls. Most previously identified korrigan1 mutants show severe phenotypes such as embryo lethality; therefore, the role of GH9A1 in cellulose synthesis remains unclear. Here, we report a novel A577V missense mutation, designated jiaoyao1 (jia1), in the second of the glycosyl hydrolase family 9 active site signature motifs in GH9A1. jia1 is defective in cell expansion in dark-grown hypocotyls, roots, and adult plants. Consistent with its defect in cell expansion, this mutation in GH9A1 resulted in reduced cellulose content and reduced CSC velocity at the plasma membrane. Green fluorescent protein-GH9A1 is associated with CSCs at multiple locations, including the plasma membrane, Golgi, trans-Golgi network, and small CESA-containing compartments or microtubuleassociated cellulose synthase compartments, indicating a tight association between GH9A1 and CSCs. GH9A1 A577V abolishes the endoglucanase activity of GH9A1 in vitro but does not affect its interaction with CESAs in vitro, suggesting that endoglucanase activity is important for cellulose synthesis. Interestingly, jia1 results in both cellulose microfibril and microtubule disorganization. Our study establishes the important role of endoglucanase in cellulose synthesis and cellulose microfibril organization in plants.

show abstract

Structural Organization and a Standardized Nomenclature for Plant Endo-1,4-β-Glucanases (Cellulases) of Glycosyl Hydrolase Family 9

Cited by 97 publications

References 20 publications

Group III-AXTHGenes of Arabidopsis Encode Predominant Xyloglucan Endohydrolases That Are Dispensable for Normal Growth

Group III-AXTHGenes of Arabidopsis Encode Predominant Xyloglucan Endohydrolases That Are Dispensable for Normal Growth

The XTH Gene Family: An Update on Enzyme Structure, Function, and Phylogeny in Xyloglucan Remodeling

Thejiaoyao1Mutant Is an Allele ofkorrigan1That Abolishes Endoglucanase Activity and Affects the Organization of Both Cellulose Microfibrils and Microtubules inArabidopsis

Contact Info

Product

Resources

About