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A Major Latex-Like Protein Is a Key Factor in Crop Contamination by Persistent Organic Pollutants

Research Center for Environmental Genomics (H.I.), Graduate School of Agricultural Science (H.I., M.S., N.K.), Faculty of Agriculture (H.I., J.G.), and Center for Collaborative Research and Technology Development, Center for Applied Structural Science (K.Y., H.T.), Kobe University, Kobe, Hyogo 657–8501, Japan; and

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Research Center for Environmental Genomics (H.I.), Graduate School of Agricultural Science (H.I., M.S., N.K.), Faculty of Agriculture (H.I., J.G.), and Center for Collaborative Research and Technology Development, Center for Applied Structural Science (K.Y., H.T.), Kobe University, Kobe, Hyogo 657–8501, Japan; and

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Research Center for Environmental Genomics (H.I.), Graduate School of Agricultural Science (H.I., M.S., N.K.), Faculty of Agriculture (H.I., J.G.), and Center for Collaborative Research and Technology Development, Center for Applied Structural Science (K.Y., H.T.), Kobe University, Kobe, Hyogo 657–8501, Japan; and

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Research Center for Environmental Genomics (H.I.), Graduate School of Agricultural Science (H.I., M.S., N.K.), Faculty of Agriculture (H.I., J.G.), and Center for Collaborative Research and Technology Development, Center for Applied Structural Science (K.Y., H.T.), Kobe University, Kobe, Hyogo 657–8501, Japan; and

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Chemical Analysis Research Center, National Institute for Agro-Environmental Sciences, Tsukuba, Ibaraki 305–8604, Japan (H.E.)

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Plant Physiology , Volume 161, Issue 4, April 2013, Pages 2128–2135, https://doi.org/10.1104/pp.112.213645

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Characterization of two cDNA clones for mRNAs expressed during ripening of melon ( Cucumis melo L.) fruits
The effects of repeated planting, planting density, and specific transfer pathways on PCB uptake by Cucurbita pepo grown in field conditions
Transcriptome characterization and high throughput SSRs and SNPs discovery in Cucurbita pepo (Cucurbitaceae)
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding
Xylem sap protein composition is conserved among different plant species
Transcriptomic and proteomic analyses of pericycle cells of the maize primary root
Cytokinin-induced structural adaptability of a Lupinus luteus PR-10 protein
X-ray and NMR structure of Bet v 1, the origin of birch pollen allergy
The absorption and translocation of polychlorinated biphenyl congeners by Cucurbita pepo ssp pepo

Dieldrin residue in the soil and cucumber from agricultural field in Tokyo
Survey of organochlorine pesticides in horticultural soils and there grown Cucurbitaceae
Soil-plant transfer of polychlorinated dibenzo- p -dioxins and dibenzofurans to vegetables of the cucumber family (Cucurbitaceae)
Differential uptake for dioxin-like compounds by zucchini subspecies
Congener specificity in the accumulation of dioxins and dioxin-like compounds in zucchini plants grown hydroponically
A simple method for displaying the hydropathic character of a protein
Uptake of weathered DDT in vascular plants: potential for phytoremediation
Melon phloem-sap proteome: developmental control and response to viral infection
Crystal structure of a hypoallergenic isoform of the major birch pollen allergen Bet v 1 and its likely biological function as a plant steroid carrier
Structure-selective accumulation of polychlorinated biphenyls in Cucurbita pepo

Factors affecting the phytoaccumulation of weathered, soil-borne organic contaminants: analyses at the ex planta and in planta sides of the plant root
Plant uptake and translocation of highly weathered, soil-bound technical chlordane residues: data from field and rhizotron studies
The major birch allergen, Bet v 1, shows affinity for a broad spectrum of physiological ligands
Dieldrin-dissolving abilities of the xylem saps of several plant families, particularly Cucurbita pepo L
Dieldrin uptake and translocation in plants growing in hydroponic medium
Possible involvement of leaf gibberellins in the clock-controlled expression of XSP30 , a gene encoding a xylem sap lectin, in cucumber roots
Differential uptake of dieldrin and endrin from soil by several plant families and Cucurbita genera
The Bet v 1 fold: an ancient, versatile scaffold for binding of large, hydrophobic ligands
Vascular tissue-specific gene expression of xylem sap glycine-rich proteins in root and their localization in the walls of metaxylem vessels in cucumber
Organic substances in xylem sap delivered to above-ground organs by the roots
High-performance affinity beads for identifying drug receptors
Cloning cDNAs for genes preferentially expressed during fruit growth in cucumber
Polychlorinated dibenzo- p -dioxins, dibenzofurans, and dioxin-like polychlorinated biphenyls in rice plants: possible contaminated pathways
Subspecies-level variation in the phytoextraction of weathered p,p ′-DDE by Cucurbita pepo

© 2013 American Society of Plant Biologists. All Rights Reserved.
© The Author(s) 2013. Published by Oxford University Press on behalf of American Society of Plant Biologists. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
© 2013 American Society of Plant Biologists. All Rights Reserved.

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Online ISSN 1532-2548 Print ISSN 0032-0889 Copyright © 2022 American Society of Plant Biologists

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This work was supported by Sekisui Chemical Co., Ltd., and by the Ministry of Education, Culture, Sports, Science, and Technology of Japan (Grant-in-Aid for Scientific Research A no. 23241028).
Corresponding author; e-mail hinui@kobe-u.ac.jp .
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors ( www.plantphysiol.org ) is: Hideyuki Inui ( hinui@kobe-u.ac.jp ).
The online version of this article contains Web-only data.
Open Access articles can be viewed online without a subscription.
Hideyuki Inui, Mami Sawada, Junya Goto, Kiyoshi Yamazaki, Noriko Kodama, Hiroki Tsuruta, Heesoo Eun, A Major Latex-Like Protein Is a Key Factor in Crop Contamination by Persistent Organic Pollutants , Plant Physiology , Volume 161, Issue 4, April 2013, Pages 2128–2135, https://doi.org/10.1104/pp.112.213645
This is the first report, to our knowledge, to reveal important factors by which members of the Cucurbitaceae family, such as cucumber ( Cucumis sativus ), watermelon ( Citrullus lanatus ), melon ( Cucumis melo ), pumpkin ( Cucurbita pepo ), squash ( C. pepo ), and zucchini ( C. pepo ), are selectively polluted with highly toxic hydrophobic contaminants, including organochlorine insecticides and dioxins. Xylem sap of C. pepo ssp. pepo , which is a high accumulator of hydrophobic compounds, solubilized the hydrophobic compound pyrene into the aqueous phase via some protein(s). Sodium dodecyl sulfate-polyacrylamide gel electrophoresis of xylem sap of two C. pepo subspecies revealed that the amount of 17-kD proteins in C. pepo ssp. pepo was larger than that in C. pepo ssp. ovifera , a low accumulator, suggesting that these proteins may be related to the translocation of hydrophobic compounds. The protein bands at 17 kD contained major latex-like proteins (MLPs), and the corresponding genes MLP-PG1 , MLP-GR1 , and MLP-GR3 were cloned from the C. pepo cultivars Patty Green and Gold Rush. Expression of the MLP-GR3 gene in C. pepo cultivars was positively correlated with the band intensity of 17-kD proteins and bioconcentration factors toward dioxins and dioxin-like compounds. Recombinant MLP-GR3 bound polychlorinated biphenyls immobilized on magnetic beads, whereas recombinant MLP-PG1 and MLP-GR1 did not. These results indicate that the high expression of MLP-GR3 in C. pepo ssp. pepo plants and the existence of MLP-GR3 in their xylem sap are related to the efficient translocation of hydrophobic contaminants. These findings should be useful for decreasing the contamination of fruit of the Cucurbitaceae family as well as the phytoremediation of hydrophobic contaminants.
Numerous agricultural fields and crops have been contaminated with persistent organic pollutants ( POPs ), including dioxins, such as polychlorinated dibenzo- p -dioxins ( PCDDs ) and polychlorinated dibenzofurans ( PCDFs ); dioxin-like compounds, such as coplanar polychlorinated biphenyls ( PCBs ) and the insecticide dichlorodiphenyltrichloroethane; drins, such as aldrin, dieldrin, and endrin; and chlordane ( Hashimoto, 2005 ; Uegaki et al., 2006 ; Hilber et al., 2008 ). POPs show carcinogenicity, teratogenicity, immunotoxicity, and estrogenicity toward humans and wildlife after accumulation through the food chain. Despite the fact that the use of PCBs and these insecticides was prohibited several decades ago, environmental and crop contamination remains a problem due to their high hydrophobicity and chemical stability.
Members of the Cucurbitaceae family, such as cucumber ( Cucumis sativus ), watermelon ( Citrullas lanatus ), melon ( Cucumis melo ), pumpkin ( Cucurbita pepo ), and zucchini ( C. pepo ), are some of the major crops in the world. Previous studies reported that members of the Cucurbitaceae family, particularly C. pepo , which includes pumpkin and zucchini, accumulated higher levels of PCDDs and PCDFs ( Hülster et al., 1994 ; Inui et al., 2008 ), 2,2-bis( p -chlorophenyl) 1,1-dichloroethylene ( p , p ′-DDE ; White et al., 2003 ), PCBs ( Aslund et al., 2008 ; Inui et al., 2008 ), chlordane ( Mattina et al., 2004 ), and drins ( Otani et al., 2007 ) compared with the levels in other plant species. Thus, it appears that the Cucurbitaceae family has unique mechanisms of POP uptake and translocation. Lunney et al. (2004) reported that the shoots of pumpkin and zucchini plants showed much higher concentrations of dichlorodiphenyltrichloroethane than those of tall fescue ( Festuca arundinacea ), alfalfa ( Medicago sativa ), and ryegrass ( Lolium multiflorum ), whereas concentrations in roots were similar among these plants. Likewise, significant differences were found between C. pepo ssp. pepo and ssp. ovifera in concentrations of dioxins and dioxin-like compounds in the aerial parts, whereas the concentrations in their roots were similar ( Inui et al., 2011 ). These results suggest that the mechanisms causing the high accumulation of POPs in C. pepo plants mainly occur during translocation from the roots to the aerial parts.
The transport of substances such as nutrients and signal molecules over long distances in higher land plants is mediated by the vascular bundles, which consist of phloem and xylem strands. In addition to inorganic salts, organic nutrients such as amino acids, sugars, and organic acids are translocated through the xylem from the roots to the aerial parts ( Satoh, 2006 ). Furthermore, the fact that POPs such as chlordane, dieldrin, and PCBs were detected in xylem sap of C. pepo suggests that their accumulation in the aerial parts of plants occurs during the translocation from roots to aerial parts in xylem sap ( Mattina et al., 2004 ; Murano et al., 2010b ; Greenwood et al., 2011 ). A recent study revealed that there were protein-like materials with the ability to dissolve dieldrin in xylem sap ( Murano et al., 2010a ). However, these materials have yet to be identified, and the mechanisms underlying the high transport ability and high accumulation of POPs in C. pepo plants are not fully understood.
In this study, to clarify the molecular mechanisms of the efficient uptake and high accumulation of POPs by C. pepo plants, xylem sap proteins related to the transport of POPs in xylem sap were identified. The aim of this research is to provide a means of preventing cucumber, melon, watermelon, pumpkin, and zucchini fruits from being contaminated by POPs .
Pyrene-adsorbed Tenax was incubated with each xylem sap from nine C. pepo cultivars, and fluorescence from pyrene in the supernatant, which is desorbed from the Tenax and glass tube, was measured. The time for the incubation of pyrene-adsorbed Tenax with xylem sap was decided as 4 h because a solubilization activity of cv Patty Green ( PG ) and cv Magda ( MG ) at 4 h was almost saturated ( Supplemental Fig. S1 ). There were differences in the pyrene solubilization activities of xylem sap among the nine tested C. pepo cultivars ( Fig. 1A ). The activity of water was lower than those of all xylem sap samples. The activity of PG xylem sap was the lowest among cultivars, whereas that of MG was three times higher than that of PG . To inactivate proteins in xylem sap, the xylem sap of MG was boiled. The activity of boiled MG sap was similar to that of PG sap. The pyrene solubilization activities of xylem sap were significantly positively correlated with bioconcentration factors ( BCFs ) of PCBs ( Matsuo et al., 2011 ; r = 0.781 [Pearson’s correlation coefficient], P < 0.05; Fig. 1B ). The solubilization act
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