Arabinogalactan Proteins Are the Possible Extracellular Molecules for Binding Exogenous Cerium(III) in the Acidic Environment Outside Plant Cells.

Qing Yang,Xiaohua Huang,Haiyan Wei,Lihong Wang,Jingfang He,Zhenbiao Yang

doi:10.3389/fpls.2019.00153

Abstract

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.

Highlights

Rare earth elements [REE(III)] are comprised of the lanthanide elements together with scandium and yttrium in the periodic table of elements (Redling, 2006)
The foremost unique response of plant leaf cells to Ce(III) bound outside leaf cells is the initiation of the pinocytosis in leaf cells (Wang et al, 2017c)
After the treatment of 80 μM Ce(III), the quantity of arabinogalactan proteins (AGP) on the plasma membrane was further increased (Figure 4C). These results are in accordance with the results of immune-Au labeling (Figure 3). All of these results indicated that with the initiation of the pinocytosis in leaf cells after treatment of Ce(III), the expression of AGP in leaf cells was promoted accompanied by the recruitment of AGP to outside leaf cells

Summary

Introduction

Rare earth elements [REE(III)] are comprised of the lanthanide elements (atomic number 57 to 71) together with scandium (atomic number is 21) and yttrium (atomic number is 39) in the periodic table of elements (Redling, 2006). REE(III) accumulated in the environment inevitably makes contact with plants in the ecosystem. Plants are the primary producers of the ecosystem, and can absorb and accumulate REE(III) from water, soil and atmosphere (Wang et al, 2014a; Zhuang et al, 2017). For protecting human health and the security of the ecosystem, it is urgent to establish the standard of the limit concentration of REE(III) in the ecosystem. To achieve this goal, it is necessary to clarify the mechanism of the biological effects of REE(III) on plants

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Conclusion