Adaptation and Growth of Tomato Cells on the Herbicide 2,6-Dichlorobenzonitrile Leads to Production of Unique Cell Walls Virtually Lacking a Cellulose-Xyloglucan Network

Shedletzky, Esther; Shmuel, Miri; Delmer, Deborah P.; Lamport, Derek T. A.

doi:10.1104/pp.94.3.980

Cited by 138 publications

(104 citation statements)

References 24 publications

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“…The decrease in pectin DM has been reported in several mutants with disrupted cellulose synthesis or modified cellulose ultrastructure (Shedletzky et al, 1990;Encina et al, 2001;Manfield et al, 2004;Sullivan et al, 2011). It has been suggested that calcium-mediated cross linking of HG can compensate, to some extent, for the reduced load-bearing capacity of the disrupted cellulosic network.…”

Section: Modulation Of Mucilage Structure By Glucomannanmentioning

confidence: 99%

CELLULOSE SYNTHASE-LIKE A2, a Glucomannan Synthase, Is Involved in Maintaining Adherent Mucilage Structure in Arabidopsis Seed

Shi

et al. 2014

Plant Physiol.

135

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Mannans are hemicellulosic polysaccharides that are considered to have both structural and storage functions in the plant cell wall. However, it is not yet known how mannans function in Arabidopsis (Arabidopsis thaliana) seed mucilage. In this study, CELLULOSE SYNTHASE-LIKE A2 (CSLA2; At5g22740) expression was observed in several seed tissues, including the epidermal cells of developing seed coats. Disruption of CSLA2 resulted in thinner adherent mucilage halos, although the total amount of the adherent mucilage did not change compared with the wild type. This suggested that the adherent mucilage in the mutant was more compact compared with that of the wild type. In accordance with the role of CSLA2 in glucomannan synthesis, csla2-1 mucilage contained 30% less mannosyl and glucosyl content than did the wild type. No appreciable changes in the composition, structure, or macromolecular properties were observed for nonmannan polysaccharides in mutant mucilage. Biochemical analysis revealed that cellulose crystallinity was substantially reduced in csla2-1 mucilage; this was supported by the removal of most mucilage cellulose through treatment of csla2-1 seeds with endo-b-glucanase. Mutation in CSLA2 also resulted in altered spatial distribution of cellulose and an absence of birefringent cellulose microfibrils within the adherent mucilage. As with the observed changes in crystalline cellulose, the spatial distribution of pectin was also modified in csla2-1 mucilage. Taken together, our results demonstrate that glucomannans synthesized by CSLA2 are involved in modulating the structure of adherent mucilage, potentially through altering cellulose organization and crystallization.Mannan polysaccharides are a complex set of hemicellulosic cell wall polymers that are considered to have both structural and storage functions. Based on the particular chemical composition of the backbone and the side chains, mannan polysaccharides are classified into four types: pure mannan, glucomannan, galactomannan, and galactoglucomannan (Moreira and Filho, 2008;Wang et al., 2012;Pauly et al., 2013). Each of these polysaccharides is composed of a b-1,4-linked backbone containing Man or a combination of Glc and Man residues. In addition, the mannan backbone can be substituted with side chains of a-1,6-linked Gal residues. Mannan polysaccharides have been proposed to cross link with cellulose and other hemicelluloses via hydrogen bonds (Fry, 1986;Iiyama et al., 1994;Obel et al., 2007;Scheller and Ulvskov, 2010). Furthermore, it has been reported that heteromannans with different levels of substitution can interact with cellulose in diverse ways (Whitney et al., 1998). Together, these observations indicate the complexity of mannan polysaccharides in the context of cell wall architecture.CELLULOSE SYNTHASE-LIKE A (CSLA) enzymes have been shown to have mannan synthase activity in vitro. These enzymes polymerize the b-1,4-linked backbone of mannans or glucomannans, depending on the substrates (GDP-Man and/or GDP-Glc) provided (Richmond and Some...

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Section: Modulation Of Mucilage Structure By Glucomannanmentioning

confidence: 99%

CELLULOSE SYNTHASE-LIKE A2, a Glucomannan Synthase, Is Involved in Maintaining Adherent Mucilage Structure in Arabidopsis Seed

Shi

et al. 2014

Plant Physiol.

135

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“…Alterations in cellulose synthesis can affect cell wall extensibility, which impacts on plant growth. Studies of the effects of cellulose biosynthesis inhibitors revealed that cultured plant cells can survive in the absence of cellulose (Shedletzky et al, 1990). The walls of these cells are effectively devoid of cellulose, and much of this absence appears to be compensated by increased levels of pectin.…”

Section: Cell Wall Composition and Extensibilitymentioning

confidence: 99%

Knockout of the AtCESA2 Gene Affects Microtubule Orientation and Causes Abnormal Cell Expansion in Arabidopsis

Chu¹,

Chen²,

Zhang³

et al. 2006

Plant Physiol.

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Complete cellulose synthesis is required to form functional cell walls and to facilitate proper cell expansion during plant growth. AtCESA2 is a member of the cellulose synthase A family in Arabidopsis (Arabidopsis thaliana) that participates in cell wall formation. By analysis of transgenic seedlings, we demonstrated that AtCESA2 was expressed in all organs, except root hairs. The atcesa2 mutant was devoid of AtCESA2 expression, leading to the stunted growth of hypocotyls in seedlings and greatly reduced seed production in mature plants. These observations were attributed to alterations in cell size as a result of reduced cellulose synthesis in the mutant. The orientation of microtubules was also altered in the atcesa2 mutant, which was clearly observed in hypocotyls and petioles. Complementary expression of AtCESA2 in atcesa2 could rescue the mutant phenotypes. Together, we conclude that disruption of cellulose synthesis results in altered orientation of microtubules and eventually leads to abnormal plant growth. We also demonstrated that the zinc finger-like domain of AtCESA2 could homodimerize, possibly contributing to rosette assemblies of cellulose synthase A within plasma membranes.

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“…The observed inhibition of mitosis caused by Dhp treatment is probably not simply a consequence of generally altered wall structure, since dichlorobenzonitrile-adapted cells with a radically altered wall organization (i.e. no cellulose) grow and divide normally (Shedletzky et al, 1990).…”

Section: Hyp Biosynthesis Is Required For Development Of Wall Tensilementioning

confidence: 99%

3,4-Dehydroproline Inhibits Cell Wall Assembly and Cell Division in Tobacco Protoplasts

1994

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We investigated the function of cell wall hydroxyproline-rich glycoproteins by observing the effects of a selective inhibitor of prolyl hydroxylase, 3,4-dehydro-i-proline (Dhp), on wall regeneration by Nicofiana fabacum mesophyll cell protoplasts. Protoplasts treated with micromolar concentrations of Dhp do not develop osmotic stability and do not initiate mitosis. l h e architecture of regenerated cell walls was examined using deep-etch, freezefracture electron microscopy of rapidly frozen tobacco cells. Untreated protoplasts assemble a dense fibrillar cell wall consisting of laterally associating subelementary fibrils. In contrast, treatment of protoplasts with Dhp alters the structure of the regenerated wall fibrils in severa1 ways: first, the microfibrils are coated with globular knobs; second, some larger fiber bundles have an open ribbonlike appearance; and third, the smallest subelementary fibrils were not visible. Tobacco cells develop an abnormal morphology as a consequence of this abnormal cell wall structure. Thus, inhibition of prolyl hydroxylase results in the regeneration of a cell wall with abnormal structural and functional properties. These data provide experimental evidence that hydroxyproline-rich glycoproteins are important for the structural integrity of primary cell walls and for the correct assembly of other wall polymers, and that wall structure is an important regulator of cell division and cell morphology.The cell wall is a complex composite layer constructed of polysaccharides, proteins, and proteoglycans that surround the plasma membrane of plant cells. The tensile strength of the wall is thought to be provided by cellulose fibrils to which a xyloglucan gel is specifically hydrogen bonded. These gelcoated fibers are embedded in an independent gel matrix composed of neutra1 and acidic polysaccharides and structural proteins and glycoproteins. To date, four distinct classes of Hyp-containing wall polymers have been described (extensins, AGPs, RPRPs, and Solanaceae lectins). Structural Hyp-containing proteins, glycoproteins, and proteoglycans may be important in controlling cell growth, cell differentiation, and disease resistance, but the precise molecular role(s) of any of these polymers in wall structure remains speculative (see Vamer and

show abstract

Adaptation and Growth of Tomato Cells on the Herbicide 2,6-Dichlorobenzonitrile Leads to Production of Unique Cell Walls Virtually Lacking a Cellulose-Xyloglucan Network

Cited by 138 publications

References 24 publications

CELLULOSE SYNTHASE-LIKE A2, a Glucomannan Synthase, Is Involved in Maintaining Adherent Mucilage Structure in Arabidopsis Seed

CELLULOSE SYNTHASE-LIKE A2, a Glucomannan Synthase, Is Involved in Maintaining Adherent Mucilage Structure in Arabidopsis Seed

Knockout of the AtCESA2 Gene Affects Microtubule Orientation and Causes Abnormal Cell Expansion in Arabidopsis

3,4-Dehydroproline Inhibits Cell Wall Assembly and Cell Division in Tobacco Protoplasts

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