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Calcium Binding by Arabinogalactan Polysaccharides Is Important for Normal Plant Development.

ABSTRACT: Arabinogalactan proteins (AGPs) are a family of plant extracellular proteoglycans involved in many physiological events. AGPs are often anchored to the extracellular side of the plasma membrane and are highly glycosylated with arabinogalactan (AG) polysaccharides, but the molecular function of this glycosylation remains largely unknown. The β-linked glucuronic acid (GlcA) residues in AG polysaccharides have been shown in vitro to bind to calcium in a pH-dependent manner. Here, we used Arabidopsis (Arabidopsis thaliana) mutants in four AG β-glucuronyltransferases (GlcAT14A, -B, -D, and -E) to understand the role of glucuronidation of AG. AG isolated from glcat14 triple mutants had a strong reduction in glucuronidation. AG from a glcat14a/b/d triple mutant had lower calcium binding capacity in vitro than AG from wild-type plants. Some mutants had multiple developmental defects such as reduced trichome branching. glcat14a/b/e triple mutant plants had severely limited seedling growth and were sterile, and the propagation of calcium waves was perturbed in roots. Several of the developmental phenotypes were suppressed by increasing the calcium concentration in the growth medium. Our results show that AG glucuronidation is crucial for multiple developmental processes in plants and suggest that a function of AGPs might be to bind and release cell-surface apoplastic calcium.

SUBMITTER: Lopez-Hernandez F

PROVIDER: S-EPMC7534474 | biostudies-literature | 2020 Oct

REPOSITORIES: biostudies-literature

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Calcium Binding by Arabinogalactan Polysaccharides Is Important for Normal Plant Development.

Lopez-Hernandez Federico F Tryfona Theodora T Rizza Annalisa A Yu Xiaolan L XL Harris Matthew O B MOB Webb Alex A R AAR Kotake Toshihisa T Dupree Paul P

The Plant cell 20200806 10

Arabinogalactan proteins (AGPs) are a family of plant extracellular proteoglycans involved in many physiological events. AGPs are often anchored to the extracellular side of the plasma membrane and are highly glycosylated with arabinogalactan (AG) polysaccharides, but the molecular function of this glycosylation remains largely unknown. The β-linked glucuronic acid (GlcA) residues in AG polysaccharides have been shown in vitro to bind to calcium in a pH-dependent manner. Here, we used Arabidopsi ...[more]

PMID: 32769130

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Project description:Rare earth elements [REE(III)] increasingly accumulate in the atmosphere and can be absorbed by plant leaves. Our previous study showed that after treatment of REE(III) on plant, REE(III) is first bound by some extracellular molecules of plant cells, and then the endocytosis of leaf cells will be initiated, which terminates the endocytic inertia of leaf cells. Identifying the extracellular molecules for binding REE(III) is the crucial first step to elucidate the mechanism of REE(III) initiating the endocytosis in leaf cells. Unfortunately, the molecules are unknown. Here, cerium(III) [Ce(III)] and Arabidopsis served as a representative of REE(III) and plants, respectively. By using interdisciplinary methods such as confocal laser scanning microscopy, immune-Au and fluorescent labeling, transmission electron microscope (TEM), X-ray photoelectron spectroscopy (XPS), ultraviolet-visible spectroscopy, circular dichroism spectroscopy, fluorescent spectrometry and molecular dynamics simulation, we obtained two important discoveries: first, the arabinogalactan proteins (AGP) inside leaf cells were sensitively increased in protein expression and recruited onto the plasma membrane; second, to verify whether AGP can bind to Ce(III) in the acidic environment outside leaf cells, by choosing fasciclin-like AGP11 (AtFLA11) as a representative of AGP, we found that Ce(III) can form stable [Ce(H2O)7](III)-AtFLA11 complexes with an apparent binding constant of 1.44 × 10-6 in simulated acidic environment outside leaf cells, in which the secondary and tertiary structure of AtFLA11 was changed. The structural change in AtFLA11 and the interaction between AtFLA11 and Ce(III) were enhanced with increasing the concentration of Ce(III). Therefore, AtFLA11 can serve as Lewis bases to coordinately bind to Ce(III), which broke traditional chemical principle. The results confirmed that AGP can be the possible extracellular molecules for binding to exogenous Ce(III) outside leaf cells, and provided references for elucidating the mechanism of REE(III) initiating the endocytosis in leaf cells.

Project description:Arabinogalactans (AGs) are structural polysaccharides of the plant cell wall. A small proportion of the AGs are associated with hemicellulose and pectin. Furthermore, AGs are associated with proteins forming the so-called arabinogalactan proteins (AGPs), which can be found in the plant cell wall or attached through a glycosylphosphatidylinositol (GPI) anchor to the plasma membrane. AGPs are a family of highly glycosylated proteins grouped with cell wall proteins rich in hydroxyproline. These glycoproteins have important and diverse functions in plants, such as growth, cellular differentiation, signaling, and microbe-plant interactions, and several reports suggest that carbohydrate components are crucial for AGP functions. In beneficial plant-microbe interactions, AGPs attract symbiotic species of fungi or bacteria, promote the development of infectious structures and the colonization of root tips, and furthermore, these interactions can activate plant defense mechanisms. On the other hand, plants secrete and accumulate AGPs at infection sites, creating cross-links with pectin. As part of the plant cell wall degradation machinery, beneficial and pathogenic fungi and bacteria can produce the enzymes necessary for the complete depolymerization of AGs including endo-β-(1,3), β-(1,4) and β-(1,6)-galactanases, β-(1,3/1,6) galactanases, α-L-arabinofuranosidases, β-L-arabinopyranosidases, and β-D-glucuronidases. These hydrolytic enzymes are secreted during plant-pathogen interactions and could have implications for the function of AGPs. It has been proposed that AGPs could prevent infection by pathogenic microorganisms because their degradation products generated by hydrolytic enzymes of pathogens function as damage-associated molecular patterns (DAMPs) eliciting the plant defense response. In this review, we describe the structure and function of AGs and AGPs as components of the plant cell wall. Additionally, we describe the set of enzymes secreted by microorganisms to degrade AGs from AGPs and its possible implication for plant-microbe interactions.

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Calcium Binding by Arabinogalactan Polysaccharides Is Important for Normal Plant Development.

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Calcium Binding by Arabinogalactan Polysaccharides Is Important for Normal Plant Development.

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