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<front>
<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Plant Sci.</journal-id>
<journal-title>Frontiers in Plant Science</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Plant Sci.</abbrev-journal-title>
<issn pub-type="epub">1664-462X</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.3389/fpls.2024.1497006</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Plant Science</subject>
<subj-group>
<subject>Review</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Multifaceted impacts of nanoparticles on plant nutrient absorption and soil microbial communities</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Zhang</surname>
<given-names>Hanfeng</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Zheng</surname>
<given-names>Tiantian</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wang</surname>
<given-names>Yue</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
<role content-type="https://credit.niso.org/contributor-roles/visualization/"/>
<role content-type="https://credit.niso.org/contributor-roles/data-curation/"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Li</surname>
<given-names>Ting</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Chi</surname>
<given-names>Qing</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/2816145"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/>
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<aff id="aff1">
<sup>1</sup>
<institution>National Key Laboratory of Cotton Bio-breeding and Integrated Utilization, School of Agricultural Sciences, Zhengzhou University</institution>, <addr-line>Zhengzhou</addr-line>, <country>China</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Henan Key Laboratory of Ion-Beam Green Agriculture Bioengineering, School of Agricultural Sciences, Zhengzhou University</institution>, <addr-line>Zhengzhou</addr-line>, <country>China</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by: Libin Zhou, Chinese Academy of Sciences (CAS), China</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by: Yin Li, Huazhong University of Science and Technology, China</p>
<p>Haixia Xu, Henan Agricultural University, China</p>
</fn>
<fn fn-type="corresp" id="fn001">
<p>*Correspondence: Qing Chi, <email xlink:href="mailto:qchi@zzu.edu.cn">qchi@zzu.edu.cn</email>
</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>13</day>
<month>11</month>
<year>2024</year>
</pub-date>
<pub-date pub-type="collection">
<year>2024</year>
</pub-date>
<volume>15</volume>
<elocation-id>1497006</elocation-id>
<history>
<date date-type="received">
<day>16</day>
<month>09</month>
<year>2024</year>
</date>
<date date-type="accepted">
<day>22</day>
<month>10</month>
<year>2024</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2024 Zhang, Zheng, Wang, Li and Chi</copyright-statement>
<copyright-year>2024</copyright-year>
<copyright-holder>Zhang, Zheng, Wang, Li and Chi</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</p>
</license>
</permissions>
<abstract>
<p>With the growth of the global population and the increasing scarcity of resources, the sustainability and efficiency improvement of agricultural production have become urgent needs. The rapid development of nanotechnology provides new solutions to this challenge, especially the application of nanoparticles in agriculture, which is gradually demonstrating its unique advantages and broad prospects. Nonetheless, various nanoparticles can influence plant growth in diverse manners, often through distinct mechanisms of action. Beyond their direct effects on the plant itself, they frequently alter the physicochemical properties of the soil and modulate the structure of microbial communities in the rhizosphere. This review focuses intently on the diverse methods through which nanoparticles can modulate plant growth, delving deeply into the interactions between nanoparticles and plants, as well as nanoparticles with soil and microbial communities. The aim is to offer a comprehensive reference for the utilization of functionalized nanoparticles in the agricultural sector.</p>
</abstract>
<kwd-group>
<kwd>nanoparticles</kwd>
<kwd>plants</kwd>
<kwd>nutrient uptake</kwd>
<kwd>soil</kwd>
<kwd>rhizosphere microbial communities</kwd>
</kwd-group>
<counts>
<fig-count count="4"/>
<table-count count="2"/>
<equation-count count="0"/>
<ref-count count="148"/>
<page-count count="15"/>
<word-count count="6824"/>
</counts>
<custom-meta-wrap>
<custom-meta>
<meta-name>section-in-acceptance</meta-name>
<meta-value>Technical Advances in Plant Science</meta-value>
</custom-meta>
</custom-meta-wrap>
</article-meta>
</front>
<body>
<sec id="s1" sec-type="intro">
<label>1</label>
<title>Introduction</title>
<p>In recent years, with the rapid development of agricultural technology and the increasing awareness of environmental protection, the demand for new materials and technologies in the field of agricultural production has become increasingly urgent (<xref ref-type="bibr" rid="B80">Moretti and Marucci, 2019</xref>; <xref ref-type="bibr" rid="B75">Magnabosco et&#xa0;al., 2023</xref>). The prolonged use of chemicals, pesticides, and fertilizers can indeed ease the challenges of food security in the long term. However, this practice poses risks such as contamination, soil fertility loss, non-target species impact, disease/insect resistance, biodiversity decline, and harm to humans/animals (<xref ref-type="bibr" rid="B137">Yousef et&#xa0;al., 2023</xref>; <xref ref-type="bibr" rid="B15">Chandrasekaran and Paramasivan, 2024</xref>). Consequently, there is an urgent need for innovative and efficient agricultural technologies to address the global challenges of food production and security (<xref ref-type="bibr" rid="B114">Thorakkattu et&#xa0;al., 2024</xref>).</p>
<p>Nanoparticles, often abbreviated as NPs, are regarded as materials ranging from 1 to 100 nm in size, and have different sizes, geometry, physical shape, mechanical strength and chemical composition, which have attracted people attention due to their wide application prospects (<xref ref-type="bibr" rid="B72">Lowry et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B92">Ravichandran et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B34">dos Santos et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B44">Garg et&#xa0;al., 2024</xref>; <xref ref-type="bibr" rid="B110">Sun et&#xa0;al., 2024</xref>). Nanotechnology has been widely applied across various sectors, including biomedicine, agriculture, and environmental remediation. The United Nations Food and Agriculture Organization (FAO) and the World Bank are actively encouraging the integration of nanotechnology into agricultural practices, with the development of sustainable agricultural systems being a central goal of current nanotechnological applications (<xref ref-type="bibr" rid="B28">De Chiffre et&#xa0;al., 2003</xref>; <xref ref-type="bibr" rid="B78">Mishra et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B58">Kah et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B4">Ahmad et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B119">Wang et&#xa0;al., 2022</xref>). Compared to traditional agricultural technology, nano-agricultural technology offers numerous advantages, closely linked to enhancements in production efficiency, reductions in input costs, and diminished ecotoxicity (<xref ref-type="bibr" rid="B102">Servin et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B58">Kah et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B140">Zhang et&#xa0;al., 2024</xref>). For example, zinc oxide, silver oxide nanoparticles had been explored as effective slow-release nanofertilizers, transport carriers, and bacteriostatic agents to provide plants with essential nutrients and inhibit pathogens, thus promoting plant growth and increasing crop yields (<xref ref-type="bibr" rid="B37">Elhaj Baddar and Unrine, 2018</xref>; <xref ref-type="bibr" rid="B111">Sun et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B104">Shireen Akhter Jahan et&#xa0;al., 2024</xref>). The application of nanoparticles to soil can influence its physical and chemical properties, the metabolic richness of plant roots, and the activity of the rhizosphere microbial community (<xref ref-type="bibr" rid="B30">Dimkpa et&#xa0;al., 2013</xref>; <xref ref-type="bibr" rid="B98">Sarma et&#xa0;al., 2024</xref>). Furthermore, the physical and chemical characteristics of soil, including texture, organic matter content, and pH level, inherently influence the migration and morphology of nanoparticles within the soil, which impact the bioavailability of nanoparticles (<xref ref-type="bibr" rid="B26">Cornelis et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B94">Reith and Cornelis, 2017</xref>; <xref ref-type="bibr" rid="B47">G&#xf3;mez-Sagasti et&#xa0;al., 2019</xref>). The ecological functions of nanoparticles and their environmental impacts are current research focal points. However, their effects on soil health and agricultural applications are of greater practical significance. In particular, the influence of nanoparticles on rhizosphere microorganisms and plant physiology is crucial for enhancing research into sustainable agricultural development strategies.</p>
<p>Land plants interact with soil microorganisms through their roots, making rhizosphere microbial community crucial for soil health and crop growth (<xref ref-type="bibr" rid="B31">Ding et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B146">Zhou et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B66">Kusiak et&#xa0;al., 2022</xref>). Compared to the perpendicular soil (soil not connected to the roots and soil falling after root shaking) (<xref ref-type="bibr" rid="B32">Ding et&#xa0;al., 2019</xref>), rhizosphere soil (the soil within 1 mm of the root surface) is teeming with a multitude of microorganisms exhibiting high biological and chemical activity, which is directly linked to the stability and productivity of agricultural production systems (<xref ref-type="bibr" rid="B62">Kaye et&#xa0;al., 2005</xref>; <xref ref-type="bibr" rid="B36">Edwards et&#xa0;al., 2015</xref>). Numerous recent studies have demonstrated the enhanced efficacy of nanoagents in regulating the plant rhizosphere microbiome compared to traditional non-nanometer approaches (<xref ref-type="bibr" rid="B6">Ahmed et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B5">Ahmed et&#xa0;al., 2023</xref>). Moreover, the regulation of microbiomes using nanoagents has the potential to enhance plant growth through a variety of mechanisms (<xref ref-type="bibr" rid="B6">Ahmed et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B5">Ahmed et&#xa0;al., 2023</xref>). Secondly, nanoparticles can indirectly promote plant nutrient absorption and ultimately promote plant growth by increasing the richness of rhizosphere microbiota (<xref ref-type="bibr" rid="B131">Xu et&#xa0;al., 2023</xref>). For example, pepper plants treated with Nano-selenium could significantly enhance the presence of beneficial microorganisms in the rhizosphere soil, including <italic>Gammaproteobacteria</italic>, <italic>Alphaproteobacteria</italic>, <italic>Bacteroidetes</italic>, <italic>Gemmatimonadetes</italic>, and <italic>Deltaproteobacteria</italic>, as well as <italic>Anaerolineae (</italic>
<xref ref-type="bibr" rid="B68">Li et&#xa0;al., 2022</xref>). These alterations in microbial communities lead to a substantial increase in soil enzyme content, soil metabolites such as fluorescein diacetate, urease, brassinosteroids, and p-hydroxybenzoic acid, and plant metabolites like rutin, luteolin, brassinosteroids, and abscisic acid, which enhanced the contribute to bolstering plant defense mechanisms and improving plant growth (<xref ref-type="bibr" rid="B68">Li et&#xa0;al., 2022</xref>). Rhizosphere microorganisms promoted plant growth by providing nutrients and hormones, while the metabolites secreted by plant roots could also change the species and number of rhizosphere microbial communities (<xref ref-type="bibr" rid="B54">Hwangbo et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B64">Khoiri et&#xa0;al., 2024</xref>). Consequently, the creation and application of suitable nanoparticles in agriculture are anticipated to not only improve but potentially supplant the use of chemical pesticides and fertilizers.</p>
<p>This review delves into the utilization of nanoparticles within agricultural production, examining how these particles can foster plant growth through various mechanisms: (i) enhancing nutrient absorption, (ii) facilitating controlled release of nutrients, (iii) enabling precise delivery of nutrients to targeted locations, and (iv) augmenting the population of beneficial microorganisms in the rhizosphere while suppressing those that are pathogenic and detrimental to plant development. Nanoparticles can stimulate plant growth both directly, by enhancing physiological processes, and indirectly, by modulating the beneficial microorganisms in the rhizosphere and altering soil conditions. Consequently, strategies driven by nanotechnology offer a promising and sustainable approach to boost crop growth and bolster crop resilience against stress factors.</p>
</sec>
<sec id="s2">
<label>2</label>
<title>Nanoparticles enhance nutrient absorption</title>
<p>Nanoparticles hold great potential for enhancing nutrient uptake, and certain nanoparticles can improve plant nutrient utilization efficiency by employing mechanisms such as directional delivery, sustained or controlled release (<xref ref-type="bibr" rid="B107">Solanki et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B35">Dutta et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B113">Taware et&#xa0;al., 2024</xref>) (<xref ref-type="fig" rid="f1">
<bold>Figure&#xa0;1</bold>
</xref>). During the promotion of plant nutrient uptake, nanoparticles can influence nutrient absorption in two ways. On the one hand, they can act as carriers for nutrients, and on the other, they can modulate soil microorganisms to enhance the plant&#x2019;s nutrient absorption capabilities (<xref ref-type="bibr" rid="B12">Bortoletto-Santos et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B63">Khan et&#xa0;al., 2022</xref>); Conversely, nutrient elements could be precisely delivered to various regions of plants via nanoparticle carriers, thereby enhancing the efficiency of nutrient utilization (<xref ref-type="bibr" rid="B39">Fincheira et&#xa0;al., 2021</xref>).</p>
<fig id="f1" position="float">
<label>Figure&#xa0;1</label>
<caption>
<p>Nanoparticle-based protective agents or carriers are designed to regulate the discharge of active compounds, enhance stability, and control the release rate, thereby achieving sustainable agricultural practices.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-15-1497006-g001.tif"/>
</fig>
<sec id="s2_1">
<label>2.1</label>
<title>Nanoparticles function as carriers for slow-release fertilizers, enhancing the absorption of nutrients by plant roots.</title>
<p>At present, nanoparticles find extensive application in the realms of energy, electronics, and architecture, yet their utilization in agriculture-related domains remains comparatively limited (<xref ref-type="bibr" rid="B29">de Silva et&#xa0;al., 2020</xref>). It possesses the potential for the slow release of fertilizers, owing to its diminutive size, substantial surface area, robust adsorption capacity, and the capability to control the release kinetics at the target site (<xref ref-type="bibr" rid="B45">Ghormade et&#xa0;al., 2011</xref>; <xref ref-type="bibr" rid="B148">Zulfiqar et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B7">Al-Mamun et&#xa0;al., 2021</xref>). The nanoparticles&#x2019; diminutive scale and elevated reactivity allow them to penetrate the plant cell wall with greater ease, thereby enhancing the transport and absorption of nutrients throughout the plant (<xref ref-type="bibr" rid="B24">Chhipa, 2017</xref>). Furthermore, it enhances fertilizer adsorption efficiency and stability, allowing slow, sustained nutrient release. This fosters plant growth, preserves beneficial microbiota diversity, mitigates eutrophication runoff, and prevents pollution (<xref ref-type="bibr" rid="B59">Kalwani et&#xa0;al., 2022</xref>).</p>
<p>Research conducted on nanofertilizers in aqueous environments revealed that a 40% urea-hydroxyapatite formulation demonstrated a controlled release of nitrogen, capable of sustaining the process for up to one week., while pure urea depleted within just a few minutes (<xref ref-type="bibr" rid="B65">Kottegoda et&#xa0;al., 2017</xref>). Likewise, the gradual and continuous release of urea from urea-silica nanohybrids prevents premature depletion of urea, ensuring effective and precise delivery of nitrogen and silica to the plant (<xref ref-type="bibr" rid="B29">de Silva et&#xa0;al., 2020</xref>).</p>
<p>Nanoparticles can also exert their slow-release function within soil media, markedly enhancing the efficiency of nutrient utilization. For instance, in the study of indigenous wheat irrigated nanohybrid, it was found that urea molecules were slowly released in doped Zn and Mg hydroxyapatite nanohybrids for up to two weeks, and this nanocompound containing only a 50% nitrogen dose maintained wheat crop yield and nitrogen nutrient uptake (<xref ref-type="bibr" rid="B103">Sharma et&#xa0;al., 2022</xref>). The recent research had revealed that a nanocarrier with a core and shell structure, composed of urea-loaded Metal-Organic Frameworks (MOFs) and silica, can facilitate the sustained release of nitrogen to crops. When utilizing urea/MIL-100(Fe)/silica heterojunction nanomaterials to treat potted rice, the nitrogen use efficiency of the rice was found to be 34.7% greater than that achieved with traditional urea treatment (<xref ref-type="bibr" rid="B126">Wu et&#xa0;al., 2024</xref>).</p>
<p>During the growth cycle of rice, urea-coated hydroxyapatite nanoparticles (urea coated hydroxyapatite nanoparticles, UHA) were released more slowly than conventional urea (<xref ref-type="bibr" rid="B10">Bhavani et&#xa0;al., 2020</xref>). Nano U-NPK(containing Ca, P, K, NO<sub>3</sub> and urea multi-nutrient nanofertilizer) not only ensures the slow release of the most crucial plant macronutrients(N, P, K), but also has the potential to reduce the nitrogen supply to plants by 40% (<xref ref-type="bibr" rid="B91">Ram&#xed;rez-Rodr&#xed;guez et&#xa0;al., 2020</xref>). Potassium-based nanoparticles (K<sub>2</sub>SiO<sub>3</sub>-NP, K<sub>18</sub>Mo<sub>8</sub>O<sub>33</sub>-NPs) compared with traditional potassium fertilizer, its utilization efficiency was about 40% higher in soybean growth, mainly due to the slow release effect of the nanoparticles, which can provide potassium ions for a longer time, effectively avoiding the toxic effect of large dose rapid delivery (<xref ref-type="bibr" rid="B118">Wang et&#xa0;al., 2024</xref>). The montmorillonite nano-hybrid composite was capable of decelerating the release rate of nitrogen across various pH conditions, extending its duration to foster plant growth (<xref ref-type="bibr" rid="B74">Madusanka et&#xa0;al., 2017</xref>). The latest study found that a special slow-release fertilizer: milk, could be made into high-fertilizer fertilizer rich in fulvic acid and potassium. The pot experiment results showed that the slow-release fertilizer was slow and more significant fertilizer effect than the traditional organic fertilizer and potassium fertilizer, and had good acid soil restoration effect (<xref ref-type="bibr" rid="B147">Zhu et&#xa0;al., 2024</xref>). In conclusion, tailored nanofertilizers have the potential to not only enhance plant growth but also to improve the soil&#x2019;s physiochemical properties, playing a pivotal role in the advancement of sustainable agriculture.</p>
</sec>
<sec id="s2_2">
<label>2.2</label>
<title>Nanoparticles are capable of precisely delivering nutrients</title>
<p>Nanoparticles had improved the nutrient uptake in plants through the precise application of chemical fertilizers and plant growth regulators, thereby fostering innovation within the agricultural sector and offering a novel strategic approach for precision agriculture (<xref ref-type="bibr" rid="B46">Ghosh et&#xa0;al., 2023</xref>; <xref ref-type="bibr" rid="B96">Saberi Riseh et&#xa0;al., 2024</xref>; <xref ref-type="bibr" rid="B106">Singh et&#xa0;al., 2024</xref>). Research had indicated that a seed coating composed of a zinc and urea hydroxyapatite nanohybrid can more precisely deliver plant nutrients and enhance the efficiency of nutrient utilization (<xref ref-type="bibr" rid="B3">Abeywardana et&#xa0;al., 2021</xref>). Under acidic soil conditions, innovative phosphate hydroxyapatite nanofertilizers, specifically Hydroxyapatite nanoparticles (HA-NPs), were administered to sunflower crops, demonstrating a significantly faster and more efficient phosphate uptake compared to conventional phosphate and triphosphate fertilizers (<xref ref-type="bibr" rid="B129">Xiong et&#xa0;al., 2018</xref>). The design of nanocarriers represents a pivotal avenue for future research into the precise delivery of nanoparticles. The strategic development of nanocarriers that can target tissues and organs within plants and organic matter will facilitate precise control over plant absorption, decrease input requirements, and minimize energy wastage.</p>
</sec>
</sec>
<sec id="s3">
<label>3</label>
<title>The Impact of nanoparticles on rhizosphere microbial communities</title>
<p>Nanoparticles engage in a range of physical, chemical, and biological processes, such as vulcanization, flocculation, precipitation, and adsorption, which enable them to interact with soil organic matter, plants, and root microorganisms (<xref ref-type="bibr" rid="B16">Chang et&#xa0;al., 2024</xref>). The study indicated that parameters including soil texture, pH, redox potential, organic matter content, and cation exchange capacity influence the chemical properties of nanoparticles (<xref ref-type="bibr" rid="B9">Ben-Moshe et&#xa0;al., 2013</xref>; <xref ref-type="bibr" rid="B42">Gao et&#xa0;al., 2019</xref>). When nanoparticles enter the soil system, they start to regulate the physiological, biochemical and genetic mechanisms of soil microorganisms; after entering the plant system, they were transferred to xylem tissue and then transported to other tissues to regulate the adaptability of the plant environment (<xref ref-type="bibr" rid="B5">Ahmed et&#xa0;al., 2023</xref>). In this section, we primarily explore the function and potential applications of nanoparticles in enhancing the rhizosphere soil microenvironment and fostering interactions among rhizosphere microbes.</p>
<sec id="s3_1">
<label>3.1</label>
<title>Nanoparticles for enhancing the soil microenvironment in the rhizosphere</title>
<p>Research indicated that nanoparticles could alter soil structure by decreasing the surface energy and enhancing the water repellency of soil particles, while also increasing soil water conductivity and aggregate stability (<xref ref-type="bibr" rid="B22">Chen et&#xa0;al., 2022</xref>). These changes could impact the soil water cycle, influencing aspects such as water retention and evaporation rates. Concurrently, alterations in soil structure could also modulate the distribution of soil pH levels and nutrient elements, subsequently influencing the beneficial microbial community within the rhizosphere (<xref ref-type="bibr" rid="B121">Wang et&#xa0;al., 2020</xref>). For example, the newly developed biochar-enriched phosphorus-doped aqueous solutions, in conjunction with iron ore nanoparticles, had the capability to alter the soil pH balance, concurrently enhancing the soil&#x2019;s organic matter and phosphorus concentrations (<xref ref-type="bibr" rid="B67">Li et&#xa0;al., 2022</xref>). Nanoparticles alter the structure, content, and diversity of advantageous microbial communities within plants, influencing the interaction within the plant-soil-microbial community system, and a robust soil structure further enhances the activity and nutrient cycling of soil microorganisms (<xref ref-type="bibr" rid="B100">Schj&#xf8;nning et&#xa0;al., 2011</xref>; <xref ref-type="bibr" rid="B27">Das et&#xa0;al., 2023</xref>; <xref ref-type="bibr" rid="B136">You et&#xa0;al., 2023</xref>; <xref ref-type="bibr" rid="B141">Zhang et&#xa0;al., 2023</xref>). Research had indicated that the application of carbon nanoparticles (CNPs) to soil could improve its water retention capacity, but also positively influence the functionality of soil microorganisms, thereby indirectly supporting plant growth (<xref ref-type="bibr" rid="B128">Xin et&#xa0;al., 2022</xref>). Concurrently, CNPs, which infiltrate plant roots via stomatal penetration or adhere to the epidermis, can stimulate soil microorganisms and enhance enzyme activities (<xref ref-type="bibr" rid="B128">Xin et&#xa0;al., 2022</xref>). This, in turn, can improve soil fertility and quality (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2</bold>
</xref>).</p>
<fig id="f2" position="float">
<label>Figure&#xa0;2</label>
<caption>
<p>Nanoparticles are transported to the soil.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-15-1497006-g002.tif"/>
</fig>
<p>Nanoparticles have the potential to foster the proliferation of microbial community diversity by altering the elemental composition of the soil (<xref ref-type="bibr" rid="B61">Karimian and Samiei, 2023</xref>). CNPs can significantly enhance the soil&#x2019;s nitrogen and phosphorus content, thereby fostering a thriving environment for microbial growth-related enzymes, which in turn promotes soil health and fertility (<xref ref-type="bibr" rid="B145">Zhao et&#xa0;al., 2021</xref>). Biologically synthesized nanoparticles exert a beneficial influence on organic carbon and microorganisms within soils used for corn cultivation, thereby accelerating plant growth (<xref ref-type="bibr" rid="B50">Haider et&#xa0;al., 2015</xref>). Innovative semi-polymer nanocomposite particles possess the capability to significantly augment the concentrations of both organic carbon and active organic carbon, thereby fostering the vigorous growth and development of plants (<xref ref-type="bibr" rid="B144">Zhao et&#xa0;al., 2019</xref>). The aforementioned studies indicate that nanoparticles have the potential to enhance soil structure, pH levels, and various other properties, which in turn can influence the interactions among plants, soil, and microbes. However, the precise manner in which these soil properties impact the interplay between these three elements warrants further investigation.</p>
</sec>
<sec id="s3_2">
<label>3.2</label>
<title>Nanoparticles promote the interaction between rhizosphere microorganisms and plants</title>
<p>The rhizosphere is regarded as the soil&#x2019;s most abundant reservoir of organic matter, serving as the primary zone for microbial proliferation and activity (<xref ref-type="bibr" rid="B93">Reinhold-Hurek et&#xa0;al., 2015</xref>). The rhizosphere microbial communities play a pivotal role in various beneficial plant growth processes, including nitrogen fixation, nutrient decomposition, and the synthesis of bioactive metabolites (<xref ref-type="bibr" rid="B11">Bi et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B18">Chauhan et&#xa0;al., 2023</xref>). Owing to their minute particle dimensions, surface functionalization, and unique chemical properties, nanoparticles are employed to enhance plant nutrient absorption and stress tolerance (<xref ref-type="bibr" rid="B73">Lv et&#xa0;al., 2019</xref>). Presently, the majority of research into the utilization of nanoparticles is centered on the plants alone, overlooking the impact of nanoparticles on soil microorganisms and their metabolites during this process.</p>
<p>The interaction between rhizosphere secretions and rhizosphere microorganisms is bidirectional, indicating that the metabolites excreted by plant roots play a role in shaping rhizosphere microbial communities; conversely, rhizosphere microorganisms are intimately connected to plant growth and health (<xref ref-type="bibr" rid="B108">Staley et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B53">Hu et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B117">Trivedi et&#xa0;al., 2020</xref>). Nevertheless, a considerable amount of uncertainty persists regarding the interplay between secretions and microbes in the rhizosphere.</p>
<p>The interaction between nanoparticles and plants can significantly promote the generation of metabolites in plant cells and the increase of rhizosphere secretions (<xref ref-type="bibr" rid="B41">Francis et&#xa0;al., 2024</xref>). These bioactive substances, once in contact with nanoparticles, indirectly have a profound impact on their key properties such as dispersion stability, aggregation state, and solubility, which has been confirmed in relevant research (<xref ref-type="bibr" rid="B77">McManus et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B14">Cervantes-Avil&#xe9;s et&#xa0;al., 2021</xref>). Specifically, biomolecules in plant cell metabolites and rhizosphere secretions (amino acids, sugars, phenolic compounds, and other secondary metabolites), Its functional groups have high reactivity and can quickly adsorb onto the surface of nanoparticles through competitive interactions, forming a surface ecological corona (eco-corona) (<xref ref-type="bibr" rid="B81">Nasser and Lynch, 2016</xref>; <xref ref-type="bibr" rid="B125">Wheeler et&#xa0;al., 2021</xref>). This ecological corona not only changes the physical and chemical properties of nanoparticles, but also further affects their migration, transformation, and biological effects in the soil environment, thus forming a complex ecological interaction network (<xref ref-type="bibr" rid="B60">Kang et&#xa0;al., 2024</xref>). This ecological corona phenomenon has a significant impact on the bioavailability of nanoparticles by crops, and its effect exhibits duality. In certain specific contexts, it may have a positive impact, promoting crop uptake and utilization of nanoparticle nutrients; However, in other cases, it may also have adverse effects, interfering with the normal physiological processes of crops. When ecological corona enhances the dispersion and stability of nanoparticles in soil or rhizosphere environment, it helps crop roots to more effectively contact and uptake these nanoparticles, thereby improving bioavailability and promoting crop growth and development. The organic acids in soybean rhizosphere secretions bind to the surface of nanoparticles (CeO<sub>2</sub>, Mn<sub>3</sub>O<sub>4</sub>, Cu(OH)<sub>2</sub>, MoO<sub>3</sub>), greatly reducing the bioavailability and delivery efficiency of these agricultural nano chemicals (<xref ref-type="bibr" rid="B14">Cervantes-Avil&#xe9;s et&#xa0;al., 2021</xref>). However, if ecological corona leads to an increase in the aggregation degree or a decrease in the solubility of nanoparticles, it may hinder the effective absorption of nanoparticles by crops. For example, the rhizosphere secretion of wheat increases the solubility of CuO nanoparticles in alkaline soil, thereby enhancing their bioavailability by crops (<xref ref-type="bibr" rid="B52">Hortin et&#xa0;al., 2020</xref>). Therefore, when using nanoparticles for agricultural production, it is necessary to fully consider the impact of ecological corona phenomenon on crop bioavailability. Through scientific and reasonable nanoparticle design and application strategies, the positive effects can be maximized while minimizing potential risks, in order to achieve sustainable development of agricultural production.</p>
<p>Research has indicated that nanoparticles frequently influence rhizosphere microorganisms by stimulating the secretion of root metabolites. For instance, the adsorption of zinc oxide nanoparticles (ZnO NPs) and their aged counterpart, s-ZnO NPs, onto the epidermis of legume roots triggers a stress response that results in the production of numerous root metabolites, including amino acids and terpenoids (<xref ref-type="bibr" rid="B70">Liu et&#xa0;al., 2023</xref>). These metabolites could directly impact soil organic matter or activate microbial decomposition of organic carbon, thereby enhancing the release and breakdown of organic carbon within the rhizosphere (<xref ref-type="bibr" rid="B70">Liu et&#xa0;al., 2023</xref>). Selenium nanoparticles (Se NPs) enhanced organic acid biosynthesis and transport genes in plants, directly enhance malate and citric acid secretion in rice roots, and then recruit sphingomonas and Streptomyces, to enhance their interaction with rice and promote the growth of rice (<xref ref-type="bibr" rid="B56">Jiao et&#xa0;al., 2023</xref>). The application of Silica dioxide nanoparticles (SiO<sub>2</sub> NPs) stimulated the synthesis, transport, and secretion of organic acids in rice roots, which provided a rich carbon source for rhizosphere microorganisms, increases the abundance of beneficial microorganisms such as <italic>Proproteobacteria</italic> and <italic>Actinobacteria</italic> in the rhizosphere by 15.2-80.5%, promotes the optimization of the bacterial community, and facilitates the absorption and growth of nitrogen in plants (<xref ref-type="bibr" rid="B139">Yue et&#xa0;al., 2023</xref>). It has been reported that compounds released by root exudates and rhizosphere microorganisms can form complexes with metal ions, thereby influencing their bioavailability to plants and microorganisms (<xref ref-type="bibr" rid="B23">Chen et&#xa0;al., 2017</xref>). Fe<sub>3</sub>O<sub>4</sub> nanoparticles encapsulated in citrate (CA) release a higher solubility of iron and interact with root exudates, which modulate plant hormones to stimulate root elongation, thereby enhancing plant growth (<xref ref-type="bibr" rid="B112">Sun et&#xa0;al., 2023</xref>). Consequently, nanoparticles can be employed to modulate rhizosphere secretions, thereby influencing the metabolic processes and community dynamics of rhizosphere microorganisms, which in turn can facilitate the emission of plant root exudates (<xref ref-type="bibr" rid="B109">Steinauer et&#xa0;al., 2016</xref>). The studies conducted clearly indicate that nanoparticles have the capacity to modify the rhizosphere microbiome, thereby enhancing the population of beneficial microbes. To fully harness the agricultural benefits, it is imperative to gain a more profound and holistic comprehension of how nanoparticles influence the interplay between root exudates and the rhizosphere microbiome.</p>
</sec>
<sec id="s3_3">
<label>3.3</label>
<title>Nanoparticles suppress plant pathogenic microorganisms</title>
<p>Plant diseases can pose a formidable threat to the productivity and quality of plants. Certain nanoparticles, harnessing their exceptional cell penetration abilities and unique surface properties, demonstrated a promising potential for inhibiting a diverse array of pathogenic microorganisms, thereby ultimately fulfilling the objective of managing and controlling plant diseases effectively (<xref ref-type="bibr" rid="B48">Gordienko et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B43">Gao et&#xa0;al., 2023</xref>; <xref ref-type="bibr" rid="B89">Rahimizadeh et&#xa0;al., 2023</xref>; <xref ref-type="bibr" rid="B99">Scandolera et&#xa0;al., 2024</xref>). The most widely studied nanoparticles currently are those of silver, copper, zinc, silicon, etc. These particles usually possess special physical and chemical properties that enable them to interact effectively with plant pathogens (directly destroying the cell membranes of plant pathogenic bacteria, causing lysis of the pathogenic cells and a decrease in pathogenic activity) and inhibit their growth and spread, thereby effectively reducing the incidence and severity of plant diseases (<xref ref-type="bibr" rid="B8">Andleeb et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B55">Jaithon et&#xa0;al., 2022</xref>). <xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3</bold>
</xref> enumerated the application of nanoparticles in five common plant diseases.</p>
<fig id="f3" position="float">
<label>Figure&#xa0;3</label>
<caption>
<p>The inhibitory effects of different nanoparticles on different plant diseases.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-15-1497006-g003.tif"/>
</fig>
<p>Research has indicated that nanoparticles predominantly contribute to the management of plant diseases by disrupting the morphological structure, sporulation capacity, and adhesion behavior of pathogens (<xref ref-type="table" rid="T1">
<bold>Table&#xa0;1</bold>
</xref>). Silver-associated nanoparticles currently stand out as the most effective in combating pathogenic microorganisms, with their antibacterial properties being particularly evident in organisms such as <italic>Ustilaginoidea virens</italic>, <italic>Ralstonia solanacearum</italic>, and <italic>Xanthomonas perforans (</italic>
<xref ref-type="bibr" rid="B86">Pis&#xe1;r&#x10d;ik et&#xa0;al., 2021</xref>). The antimicrobial efficacy of these silver nanoparticles was intricately linked to their unique physicochemical characteristics, including concentration, particle size, pH, and other factors (<xref ref-type="bibr" rid="B86">Pis&#xe1;r&#x10d;ik et&#xa0;al., 2021</xref>). For example, the growth inhibition of rice false smut fungus by nanosilver was concentration-dependent, and nanosilver at a median effective concentration could significantly inhibit the sporulation and pathogenicity of the fungus. In addition, Ag NPs reduced the H3K27me3 modification mediated by UvKmt6, leading to the upregulation of genes involved in biosynthesis of oryzalide, and the decrease in H3K27me3 levels is associated with the inhibition of mycelial growth (<xref ref-type="bibr" rid="B124">Wen et&#xa0;al., 2023</xref>). In addition to combating fungal and bacterial pathogens, silver nanoparticles could also diminish the concentration of Bean Yellow Mosaic Virus (BYMV) and alleviate disease severity in broad beans (<xref ref-type="bibr" rid="B2">Abdelkhalek et&#xa0;al., 2023</xref>). Nano biotechnology has revealed that copper nanoparticles, particularly tobacco-derived copper oxide nanoparticles (CuO NPs), exhibit a pronounced antibacterial effect that is concentration-dependent. Scanning electron microscopy (SEM) and transmission electron microscopy (TEM) observations have shown that CuO NPs can disrupt the hyphal cell wall, resulting in a rough and convex surface (<xref ref-type="bibr" rid="B20">Chen et&#xa0;al., 2022</xref>). Additionally, there is evidence of significant partial collapse and bending of the hyphae (<xref ref-type="bibr" rid="B20">Chen et&#xa0;al., 2022</xref>). This phenomenon occurs because CuO NPs aggregate and adhere to the hyphal cell wall, and may even penetrate the cell membrane (<xref ref-type="bibr" rid="B20">Chen et&#xa0;al., 2022</xref>). The direct contact between nanoparticles and the hyphae leads to the accumulation of reactive oxygen species (ROS) and a corresponding increase in hyphal superoxide dismutase (SOD) enzyme activity (<xref ref-type="bibr" rid="B20">Chen et&#xa0;al., 2022</xref>). A recent study showed that copper nanoparticles (Cu NPs) also play an important role in the inhibition of bacterial fruit spot disease in watermelon, also by inducing oxidative stress and destroying cell integrity (<xref ref-type="bibr" rid="B82">Noman et&#xa0;al., 2023</xref>). <xref ref-type="table" rid="T1">
<bold>Table&#xa0;1</bold>
</xref> offers a comprehensive overview of the utilization of nanoparticles as antimicrobial agents.</p>
<table-wrap id="T1" position="float">
<label>Table&#xa0;1</label>
<caption>
<p>Effect of various nanofertilizer/nanoparticles on pathogenic microbes and microbial functions.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="top" align="left">Nanomaterials/Nanoparticles</th>
<th valign="top" align="left">Particle size</th>
<th valign="top" align="left">Dose and mode of application</th>
<th valign="top" align="left">Effect on<break/>Pathogenic<break/>microbes</th>
<th valign="top" align="left">Effect on Pathogenic microbes functions/Effect on plant</th>
<th valign="top" align="left">Reference</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left">Metal Silver (Ag) related</td>
<td valign="top" align="left">2 nm</td>
<td valign="top" align="left">2.16 &#x3bc;g/mL, direct application to soil</td>
<td valign="top" align="left">Both the surface and intracellular organelles of <italic>Ustilaginoidea virens</italic> were disrupted, and affect mycelial growth, conidiation, and virulence of <italic>U</italic>. <italic>virens</italic>
</td>
<td valign="top" align="left">Affects several energy utilization and metabolic processes in <italic>Ustilaginoidea virens</italic>
</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B124">Wen et&#xa0;al., 2023</xref>)</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">21/29 &#xb1; 5 nm</td>
<td valign="top" align="left">400 &#x3bc;g/mL, direct application to soil</td>
<td valign="top" align="left">
<italic>Ralstonia solanacearum</italic> envelope is damaged, the cells bulge and form small pits.</td>
<td valign="top" align="left">The cellular metabolic activity and surface adhering ability of <italic>R. solanacearum</italic> were completely lost</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B51">Haroon et&#xa0;al., 2019</xref>)</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">18 nm</td>
<td valign="top" align="left">100 ppm, direct application to soil</td>
<td valign="top" align="left">Led to cell deformation and loss of the rod-shaped structure of the <italic>Xanthomonas perforans</italic>
</td>
<td valign="top" align="left">Significantly reduced the severity of bacterial spot disease</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B83">Ocsoy et&#xa0;al., 2013</xref>)</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">5-35 nm</td>
<td valign="top" align="left">20 &#xb5;g/mL, direct application to soil</td>
<td valign="top" align="left">
<italic>Ralstonia solanacearum</italic> cell wall and plasma membrane rupture, as well as nucleic acid material leakage</td>
<td valign="top" align="left">Inhibit the growth, community and swimming movement of <italic>Ralstonia solanacearum</italic>
</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B1">Abd Alamer et&#xa0;al., 2022</xref>)</td>
</tr>
<tr>
<td valign="top" align="left">Metal copper (Cu) related</td>
<td valign="top" align="left">10-100 nm</td>
<td valign="top" align="left">100 mg/L, direct application to soil</td>
<td valign="top" align="left">Cell wall damage of, such as rough and convex cell envelope, accompanied by obvious local collapse and distortion</td>
<td valign="top" align="left">Activated a series of defense enzyme activities in tobacco</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B20">Chen et&#xa0;al., 2022</xref>)</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">29.11-78.56 nm</td>
<td valign="top" align="left">100 &#xb5;g/mL, foliar spray</td>
<td valign="top" align="left">Induced oxidative stress, biofilm inhibition and cell integrity destruction in <italic>Acidovorax citrulli</italic>
</td>
<td valign="top" align="left">Regulate host&#x2019;s active immune response to inhibit watermelon<break/>bacterial fruit blotch</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B82">Noman et&#xa0;al., 2023</xref>)</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">200-500 nm</td>
<td valign="top" align="left">0.5 mg/mL, direct application to soil</td>
<td valign="top" align="left">Damage the cell membrane of <italic>Fusarium oxysporum f.</italic> sp. <italic>lycopersici</italic>, altering the permeability of the cell membrane, leading to the disintegration of the cell membrane, and eventually to cell death</td>
<td valign="top" align="left">Effectively treats Fusarium wilt while promoting the growth of tomato plants</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B71">Lopez-Lima et&#xa0;al., 2021</xref>)</td>
</tr>
<tr>
<td valign="top" align="left">Metal iron (Fe) related</td>
<td valign="top" align="left">86 nm</td>
<td valign="top" align="left">250 &#x3bc;g/mL, foliar spray</td>
<td valign="top" align="left">
<italic>Xanthomonas oryzae pv. oryzae</italic> cell membrane destruction, ROS formation, DNA damage, protein and enzyme degeneration, and leakage of intracellular contents ultimately lead to cell death</td>
<td valign="top" align="left">Maintaining ionic homeostasis,and improving the photosynthetic profile</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B6">Ahmed et&#xa0;al., 2022</xref>)</td>
</tr>
<tr>
<td valign="top" align="left">Metal zinc (Zn) related</td>
<td valign="top" align="left">30 nm</td>
<td valign="top" align="left">200 mg/L, direct application to soil or foliar spray</td>
<td valign="top" align="left">Direct antifungal activity against <italic>M. oryzae</italic> by inhibiting its conidiation and appressorium formation</td>
<td valign="top" align="left">Fight against blast disease,and enhance the tolerance of rice seedlings to abiotic stress</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B88">Qiu et&#xa0;al., 2023</xref>)</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">0.323 nm</td>
<td valign="top" align="left">100 &#x3bc;g/mL, foliar spray</td>
<td valign="top" align="left">Destroyed <italic>Pseudomonas syringae</italic> pv. tomato DC3000 membrane and induces deformation of the contents of the cytoplasm, leading eventually to cell death</td>
<td valign="top" align="left">Protect tomato against the bacterial speck pathogen,and promote plant growth</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B38">Elsharkawy et&#xa0;al., 2020</xref>)</td>
</tr>
<tr>
<td valign="top" align="left">Silica (Si) related</td>
<td valign="top" align="left">5-15 nm</td>
<td valign="top" align="left">0.2 g/L, foliar spray</td>
<td valign="top" align="left">
<italic>Fusarium oxysporum</italic> f. sp. <italic>lycopersici</italic> and <italic>Alternaria solani</italic> showed disturbed and fragmented mycelium</td>
<td valign="top" align="left">Enhance plant growth, photosynthetic pigments and reduce the disease indices</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B84">Parveen and Siddiqui, 2022</xref>)</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">80-100 nm</td>
<td valign="top" align="left">300 mg/L, foliar spray</td>
<td valign="top" align="left">
<italic>Phytophthora infestans</italic> structurally distorted with terminal deformity and local shrinkage</td>
<td valign="top" align="left">Prevented the appearance of small brown spots and aerial mycelium on the potato tubers</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B21">Chen et&#xa0;al., 2023</xref>)</td>
</tr>
<tr>
<td valign="top" align="left">Chitosan nanoparticles</td>
<td valign="top" align="left">NA</td>
<td valign="top" align="left">1g/L,inoculated into the ginger rhizomes wound</td>
<td valign="top" align="left">Inhibited the mycelial growth and spore germination of <italic>Fusarium solani</italic>
</td>
<td valign="top" align="left">The antioxidant defense system of ginger at a high level in response to hence reduced disease indices</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B142">Zhang et&#xa0;al., 2024</xref>)</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn>
<p>#NA, Not available.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<p>In conclusion, the antimicrobial properties of nanoparticles are derived from their unique physical structure and chemical reactivity. Nonetheless, despite their demonstrated efficacy in inhibiting pathogenic microorganisms, practical applications must take into account their stability, biocompatibility, environmental impact, and cost-effectiveness.</p>
</sec>
<sec id="s3_4">
<label>3.4</label>
<title>Nanoparticles boost the efficacy of probiotic microorganisms</title>
<p>Numerous nanoparticles have the potential to improve nutrient transport and soil fertility by modulating the function, species diversity, or population size of the microbial community within the rhizosphere (<xref ref-type="bibr" rid="B122">Wei et&#xa0;al., 2020</xref>). Foliar application or direct application of nanoparticle solutions could influence the function of rhizosphere microbial communities in plant root nutrient uptake, nitrogen regulation, and the regulation of related enzyme activities, thereby impacting plant growth and development (<xref ref-type="fig" rid="f4">
<bold>Figure&#xa0;4</bold>
</xref>) (<xref ref-type="bibr" rid="B127">Wu et&#xa0;al., 2023</xref>).</p>
<fig id="f4" position="float">
<label>Figure&#xa0;4</label>
<caption>
<p>Nanoparticles enhance the activity of beneficial microbes within the rhizosphere, modulate soil metabolic processes, and subsequently foster plant growth and development.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-15-1497006-g004.tif"/>
</fig>
<p>Throughout the phase of accelerated plant growth, the high nutrient demand entices a larger concentration of rhizosphere microorganisms, which play a crucial role in the plants&#x2019; nutrient absorption (<xref ref-type="bibr" rid="B17">Chaparro et&#xa0;al., 2014</xref>). Simultaneously, the interplay between nanoparticles and rhizosphere microorganisms could enhance plant growth and improve soil health (<xref ref-type="bibr" rid="B116">Tripathi et&#xa0;al., 2024</xref>). The research indicated that in the developmental phase of rice seedlings, selenium nanoparticles (Se NPs) enhance the abundance of sphingomonas and various other bacterial species, while also encouraging the secretion of root exudates (<xref ref-type="bibr" rid="B56">Jiao et&#xa0;al., 2023</xref>). These combined influenced synergistically modulate nutrient uptake and foster the growth of rice plants (<xref ref-type="bibr" rid="B56">Jiao et&#xa0;al., 2023</xref>).In <italic>Brassica chinensis L.</italic>, there exists a comparable regulatory function throughout the growth process (<xref ref-type="bibr" rid="B120">Wang et&#xa0;al., 2022</xref>). The symbiotic relationship between rhizosphere microorganisms and plants enhanced the bioavailability of nutrients within the rhizosphere soil, thereby augmenting the plants&#x2019; nutrient uptake capabilities (<xref ref-type="bibr" rid="B130">Xu et&#xa0;al., 2023</xref>). The application of zinc oxide quantum dots (ZnO QDs) during the growth phase of pumpkins aids in enhancing beneficial microorganisms within the endophytic and rhizosphere environments, thus promoting nutrient uptake and plant growth (<xref ref-type="bibr" rid="B131">Xu et&#xa0;al., 2023</xref>). It has been shown that the 50 mg/kg of Fe<sub>7</sub>(PO<sub>4</sub>)<sub>6</sub> nanoparticle treatment of tomato will increase the relative abundance of beneficial microorganisms associated with nutrient accumulation, which will accelerate nutrient accumulation (<xref ref-type="bibr" rid="B57">Jiao et&#xa0;al., 2024</xref>).</p>
<p>Numerous studies have demonstrated that the availability of soil nitrogen and the uptake of nitrogen by plants play a crucial role in determining crop yield. Concurrently, the absorption, excretion, and transformation of soil nitrogen are largely contingent upon the interactions within the rhizosphere microbial communities (<xref ref-type="bibr" rid="B134">Yang et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B138">Yu et&#xa0;al., 2019</xref>). The effective and sustainable supply of nitrogen in the rhizosphere soil mainly depends on specific rhizosphere microbial communities that convert inert nitrogen into nitrogen compounds. Therefore, nitrogen transformation driven by rhizosphere microbial communities was a significant determinant of plant nitrogen uptake (<xref ref-type="bibr" rid="B79">Moreau et&#xa0;al., 2019</xref>). For example, the application of FeNPs to alfalfa increased the diversity of the rhizosphere microbial community, further enhancing the nitrogen-fixing ability of the roots (<xref ref-type="bibr" rid="B143">Zhang et&#xa0;al., 2024</xref>). Silver nanoparticles (AgNPs) enhanced the population of rhizosphere bacteria, including <italic>Saccharimonadia</italic> (also known as Plant Growth Promoting Rhizobacteria, or PGPR) (<xref ref-type="bibr" rid="B101">Sellstedt et&#xa0;al., 2013</xref>; <xref ref-type="bibr" rid="B40">Francioli et&#xa0;al., 2021</xref>). Certain strains of these bacteria facilitate atmospheric nitrogen fixation, while others contribute to plant growth and aid in nutrient transformation (<xref ref-type="bibr" rid="B101">Sellstedt et&#xa0;al., 2013</xref>; <xref ref-type="bibr" rid="B40">Francioli et&#xa0;al., 2021</xref>). <xref ref-type="table" rid="T2">
<bold>Table&#xa0;2</bold>
</xref> offers a comprehensive overview of the enhancement of diverse nanoparticles on various beneficial microbes within the rhizosphere, along with their affirmative impacts on plant growth.</p>
<table-wrap id="T2" position="float">
<label>Table&#xa0;2</label>
<caption>
<p>Effect of various nanoparticles on rhizospheric microorganisms and microbial functions.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="top" align="left">Nanoparticles</th>
<th valign="top" align="left">Particle size</th>
<th valign="top" align="left">Name of the plant</th>
<th valign="top" align="left">Dose and mode of application</th>
<th valign="top" align="left">Effect on rhizosphere microorganisms</th>
<th valign="top" align="left">Effect on rhizosphere microorganisms functions</th>
<th valign="top" align="left">Effect on plant</th>
<th valign="top" align="left">Reference</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left">Metal Silver (Ag) related</td>
<td valign="top" align="left">20 nm</td>
<td valign="top" align="left">Rice</td>
<td valign="top" align="left">1 mg/kg,<break/>direct application to soil</td>
<td valign="top" align="left">Increase the number of putative beneficial soil bacteria, <italic>eg</italic>, <italic>Frankiales</italic>, <italic>Rhizobiales</italic>, <italic>Chitinophagales</italic>, and <italic>Saccharimonadia</italic>
</td>
<td valign="top" align="left">Improved biogeochemical cycling of nitrogen, carbon etc.</td>
<td valign="top" align="left">Promote tillering and increase grain yield</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B133">Yan et&#xa0;al., 2022</xref>)</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">30-60 nm</td>
<td valign="top" align="left">
<italic>Triticum aestivum</italic>
</td>
<td valign="top" align="left">10 ppm,<break/>direct application to soil</td>
<td valign="top" align="left">Increase the number of putative beneficial soil bacteria, such as <italic>Pseudomonas</italic> spp. <italic>and Arthrobacter</italic> spp.</td>
<td valign="top" align="left">Enhanced nitrogen fixation</td>
<td valign="top" align="left">Increased growth and yield of plant</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B87">Przemieniecki et&#xa0;al., 2024</xref>)</td>
</tr>
<tr>
<td valign="top" align="left">Metal copper (Cu) related</td>
<td valign="top" align="left">28 &#xb1; 14 nm</td>
<td valign="top" align="left">
<italic>Triticum aestivum</italic>
</td>
<td valign="top" align="left">0.5 mg/kg,<break/>direct application to soil</td>
<td valign="top" align="left">The abundance of <italic>Sphingobacterium</italic>, <italic>Pseudomonas</italic>and other bacteria communities increased</td>
<td valign="top" align="left">Improved nitrogen fixation and reduced denitrification process</td>
<td valign="top" align="left">Enhance plant photosynthesis</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B49">Guan et&#xa0;al., 2020</xref>)</td>
</tr>
<tr>
<td valign="top" align="left">Metal iron (Fe) related</td>
<td valign="top" align="left">83 nm</td>
<td valign="top" align="left">Tomato</td>
<td valign="top" align="left">50 mg/kg, direct application to soil</td>
<td valign="top" align="left">Enhance the abundance of beneficial genera in the rhizosphere, particularly <italic>Nitrospira</italic>, <italic>Sphingomonas</italic>, <italic>Massilia</italic>, <italic>Bryobacter</italic>, <italic>Chithonibacter</italic>, <italic>RB41</italic> and <italic>Rubellimicrobium</italic>
</td>
<td valign="top" align="left">Enhanced nitrogen fixation</td>
<td valign="top" align="left">Significantly enhanced nutrient uptake, improved flowering development, and ultimately increased nutritional quality and tomato yield</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B57">Jiao et&#xa0;al., 2024</xref>)</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">4&#x2013;10 nm</td>
<td valign="top" align="left">
<italic>Glycine max</italic>
</td>
<td valign="top" align="left">30 mg/L,<break/>foliar spray</td>
<td valign="top" align="left">Enhanced rhizobial activity</td>
<td valign="top" align="left">Enhanced nitrogen fixation</td>
<td valign="top" align="left">Improved the soybean yield and promoted the nutritional quality</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B13">Cao et&#xa0;al., 2022</xref>)</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">NA</td>
<td valign="top" align="left">
<italic>Medicago sativa</italic> L.</td>
<td valign="top" align="left">10 mg/L, seed soaking or foliar spray</td>
<td valign="top" align="left">Increase the number of putative beneficial soil bacteria, such as <italic>Proteobacteria, Firmicutes, Actinobacteria, and Bacteroidetes</italic>
</td>
<td valign="top" align="left">Improved nitrogen fixation and reduced denitrification process</td>
<td valign="top" align="left">Enhance photosynthesis and promote growth</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B143">Zhang et&#xa0;al., 2024</xref>)</td>
</tr>
<tr>
<td valign="top" align="left">Metal zinc (Zn) related</td>
<td valign="top" align="left">4.06 nm</td>
<td valign="top" align="left">
<italic>Cucurbita moschata</italic> Duch.</td>
<td valign="top" align="left">0.61 mmol/L,<break/>foliar spray</td>
<td valign="top" align="left">Increased abundance of <italic>Steroidobacter</italic> and <italic>Paenibacillus</italic>
</td>
<td valign="top" align="left">Improve nitrogen metabolism</td>
<td valign="top" align="left">Promote plant growth, nutrient absorption, and tolerance to stress</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B131">Xu et&#xa0;al., 2023</xref>)</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">22-28 nm</td>
<td valign="top" align="left">
<italic>Medicago truncatula</italic>
</td>
<td valign="top" align="left">100 mg/kg,<break/>direct application to soil</td>
<td valign="top" align="left">Increase the number of putative beneficial soil bacteria,such as <italic>Haliangium</italic>, <italic>norank_f:BIrii41</italic>, <italic>Gaiella</italic>, <italic>norank_f:Gemmatimonadaceae</italic> and <italic>Lysobacter</italic>
</td>
<td valign="top" align="left">Improve the underground carbon cycle and the breakdown of cellulose</td>
<td valign="top" align="left">Promote plant growth</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B70">Liu et&#xa0;al., 2023</xref>)</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">18 nm</td>
<td valign="top" align="left">
<italic>Sorghum bicolor</italic> var. 251</td>
<td valign="top" align="left">5 mg/kg, direct application to soil</td>
<td valign="top" align="left">Microbial quantity and activity were enhanced</td>
<td valign="top" align="left">Improve nitrogen metabolism</td>
<td valign="top" align="left">Accelerate plant growth and increase yield</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B25">Christian et&#xa0;al., 2019</xref>)</td>
</tr>
<tr>
<td valign="top" align="left">Selenium (Se) related</td>
<td valign="top" align="left">3&#x2013;18 nm</td>
<td valign="top" align="left">
<italic>Oryza sativa</italic> L.</td>
<td valign="top" align="left">0.1 mg/kg,<break/>direct application to soil</td>
<td valign="top" align="left">Increase the number of putative beneficial soil bacteria, such as <italic>Streptomyces</italic> and <italic>Sphingomonas</italic>
</td>
<td valign="top" align="left">Improves the adhesion of beneficial bacteria to roots</td>
<td valign="top" align="left">Promote plant growth</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B56">Jiao et&#xa0;al., 2023</xref>)</td>
</tr>
<tr>
<td valign="top" align="left">Silica (Si) related</td>
<td valign="top" align="left">20 nm</td>
<td valign="top" align="left">
<italic>Brassica chinensis</italic> L.</td>
<td valign="top" align="left">Each dose is 1 mg,foliar spray</td>
<td valign="top" align="left">Increased abundance of <italic>Paenibacillus</italic>, <italic>Rhodobacteraceae</italic>, <italic>Chaetomium</italic> while abundance of silicate <italic>Rhodoplane</italic> was reduced</td>
<td valign="top" align="left">Improved biogeochemical cycling of nitrogen, carbon</td>
<td valign="top" align="left">Promote root growth</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B115">Tian et&#xa0;al., 2020</xref>)</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">8 nm</td>
<td valign="top" align="left">
<italic>O. sativa</italic> L.</td>
<td valign="top" align="left">50 mg/kg,<break/>direct application to soil</td>
<td valign="top" align="left">Increase the number of putative beneficial soil bacteria,such as <italic>Proteobacteria, Actinobacteriota</italic> etc.</td>
<td valign="top" align="left">Improved nitrogen fixation and reduced denitrification process</td>
<td valign="top" align="left">Promote the growth and yield of rice through enhancement of tillering</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B139">Yue et&#xa0;al., 2023</xref>)</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn>
<p>#NA, Not available.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<p>Although numerous studies have extensively reported the positive effects of nanoparticles on plant and rhizosphere microbial community diversity, there are still some studies suggesting that the effects of nanoparticles on plants and microorganisms may exhibit dose-dependent effects, especially under high concentration conditions, where they may have inhibitory effects on plant growth and some rhizosphere microbial communities (<xref ref-type="bibr" rid="B97">Sagha&#xef; et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B95">Ren et&#xa0;al., 2024</xref>). For example, in plant growth experiments, low concentrations of ZnO nanoparticles promoted the growth of <italic>Vigna radiata</italic> and <italic>Cicer arietinum</italic> seedlings. Treatment concentrations of nanoparticles higher than 20 ppm and 1 ppm, respectively, would inhibit plant growth (<xref ref-type="bibr" rid="B76">Mahajan et&#xa0;al., 2011</xref>). At the same time, 1.2 mM low concentration ZnO nanoparticles can also promote the germination and metabolic activity of <italic>Solanum lycopersicum</italic>, while the germination and metabolic activity of plants above this concentration are inhibited (<xref ref-type="bibr" rid="B105">Singh et&#xa0;al., 2016</xref>). High concentrations of nanoparticles not only affect seed germination and plant growth rate, but also affect the level of edible nutrients. Low concentrations of TiO<sub>2</sub> nanoparticles (50 mg/L) can increase the level of nutrients in <italic>Coriandrum sativum</italic> L., while high concentrations can reduce the decrease in edible nutrient content and inhibit growth. In terms of microbial activity, it usually follows a dose-dependent pattern, which is also related to the type of nanoparticles (<xref ref-type="bibr" rid="B135">Yang et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B69">Lin et&#xa0;al., 2022</xref>). Low dose nanoparticles may have beneficial effects on soil rhizosphere microorganisms by promoting metabolism and energy conversion. For example, treating <italic>Medicago truncatula</italic> with 5 mg/kg of Ag and 50 mg/kg of Zn, and Ti nanoparticles significantly increased the types and total amount of soil rhizosphere microorganisms (<xref ref-type="bibr" rid="B19">Chen et&#xa0;al., 2017</xref>). Low dose (10 mg/kg) ZnO nanoparticles promote the proliferation of Cyanobacteria in the rhizosphere of <italic>Lactuca sativa</italic> L., but 100 mg/kg ZnO has no significant effect on this colony under the same treatment (<xref ref-type="bibr" rid="B132">Xu et&#xa0;al., 2018</xref>). Therefore, excessive application of nanoparticles is likely to disrupt the balance of soil ecosystems. In order to fully utilize the benefits of nanoparticles and reduce their potential risks, it is necessary to conduct in-depth research on the interaction mechanism between nanoparticles and microorganisms, and explore reasonable usage methods and dosages. At the same time, it is necessary to strengthen the environmental risk assessment and supervision of nanoparticles to ensure their safe application.</p>
<p>There are also specific effects between microbes and soil enzymes (<xref ref-type="bibr" rid="B85">Philippot et&#xa0;al., 2024</xref>). A variety of soil enzymes play a crucial role in biochemical processes, facilitating the breakdown of complex organic matter and the mobilization of nutrients, while also influencing the functionality of certain microorganisms (<xref ref-type="bibr" rid="B123">Wen et&#xa0;al., 2024</xref>). In soils rich in organic matter, a greater abundance of microorganisms correlates with heightened enzyme activity, thereby enhancing the interaction between these two components (<xref ref-type="bibr" rid="B33">Donald et&#xa0;al., 2018</xref>). The utilization of ZnO nanoparticle to mung bean plants increased the diversity of soil phosphatase and phytase activities and microorganisms, and improved the level of phosphorus acquisition, while also enhancing soil health and nutrient cycle (<xref ref-type="bibr" rid="B90">Raliya et&#xa0;al., 2016</xref>). Studies have shown that the absorption of nitrogen, phosphorus and potassium in 200 mg/kg CNPs was significantly increased by 185%, 30.4% and 193%, respectively (<xref ref-type="bibr" rid="B128">Xin et&#xa0;al., 2022</xref>). The increase of plant roots was higher than that of branches, and carbon nanoparticles enhanced the activity of most soil enzymes, thus affecting the soil microbial function, thus indirectly regulating plant growth (<xref ref-type="bibr" rid="B128">Xin et&#xa0;al., 2022</xref>). These studies enable us to gain deeper insights into the ways in which nanoparticles can enhance plant nutrient absorption. However, the mechanisms underlying the complex interactions among nanoparticles, plant roots, and soil have yet to be fully investigated.</p>
</sec>
</sec>
<sec id="s4" sec-type="conclusions">
<label>4</label>
<title>Conclusion</title>
<p>The above research results indicate that nanoparticles play an important role in promoting plant nutrient absorption and rhizosphere microbial communities. There is a close connection and synergistic effect between the two, jointly affecting the growth and development of plants, as well as the stability and sustainability of ecosystems. Nanoparticles can promote plant nutrient absorption by loading nutrients and accurately deliver nutrients to different parts of the plant, thereby improving nutrient utilization efficiency. Concurrently, nanoparticles also play a pivotal role in modulating rhizosphere microorganisms. They not only foster plant growth and enhance yield by combating pathogenic microorganisms that are detrimental to plants, but also alter the composition of the rhizosphere microbial community by modifying soil physical and chemical properties and root exudates, ultimately influencing the growth and development of plants.</p>
<p>Nanoparticles enhance plant growth and development by facilitating nutrient uptake, modulating rhizosphere microorganisms, and enhancing soil physiochemical properties, among other benefits, with a focus on their positive effects on plants. Further research into the interactions between roots and microbes in the rhizosphere influenced by nanoparticles will elucidate the mechanisms behind plant phenotypic alterations induced by nanoparticles. This will also shed light on the manipulation of the plant rhizosphere microbiome by nanoparticles, paving the way for more sustainable agricultural practices.</p>
<p>Various types of nanoparticles have played important roles in plant growth, but metal nanoparticles have the widest application prospects in agricultural production. They can serve as pesticide carriers, improve pesticide utilization, and reduce environmental pollution; At the same time, it can also serve as a trace element or plant growth regulator, promoting plant growth and improving yield and quality. In addition, metal nanoparticles have shown great potential in environmental monitoring and biosensing, providing timely and accurate environmental data for agricultural production. Although there are still some challenges in practical applications, such as assessing environmental effects and biosafety, as well as optimizing production costs, with the continuous development and improvement of nanotechnology, the application of metal nanoparticles in agriculture will become more extensive and in-depth, making important contributions to agricultural production and sustainable development.</p>
<p>Nanoparticles have the potential to directly influence plant growth and indirectly affect the surrounding ecological environment, thereby ensuring the sustainable development of agriculture and fostering the green revolution. Moving forward, it is imperative to conduct additional research to uncover the effects of nanoparticles (NPs) on higher plants, particularly crops and vegetables, when applied to soils with varying properties. This should include an exploration of the molecular mechanisms of NPs uptake, transformation, and its impact on growth parameters, as well as the interaction mechanisms between NPs and rhizosphere microbes. Concurrently, greater focus should be placed on the interplay among rhizosphere microbial communities, soil, NPs, and plants. Further studies are necessary to ascertain the beneficial effects of NPs. Moreover, long-term investigations into cereal crops and other key crops are essential to establish correlations between NP dosage, soil type, and ecological impacts. Such research is crucial for reducing reliance on chemical pesticides and fertilizers and for securing the future sustainable development of agriculture.</p>
<p>In summary, this review encapsulates the outcomes of nanoparticles in enhancing plant growth and modulating the rhizosphere microbiome via various mechanisms, offering a foundation for the synergistic integration of future research endeavors in the realms of nanoscience, sustainable agriculture, and environmental science.</p>
</sec>
</body>
<back>
<sec id="s5" sec-type="author-contributions">
<title>Author contributions</title>
<p>HZ: Writing &#x2013; review &amp; editing, Writing &#x2013; original draft. TZ: Writing &#x2013; original draft. YW: Writing &#x2013; original draft, Visualization, Data curation. TL: Writing &#x2013; review &amp; editing. QC: Writing &#x2013; review &amp; editing.</p>
</sec>
<sec id="s6" sec-type="funding-information">
<title>Funding</title>
<p>The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This research was funded by National Natural Science Foundation of China (32101661); Natural Science Foundation of Henan Province, China (Grant No. 212300410276); Open Project of State Key Laboratory of Cotton Biology (CB2024A35).</p>
</sec>
<sec id="s7" sec-type="COI-statement">
<title>Conflict of interest</title>
<p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p>
</sec>
<sec id="s9" sec-type="disclaimer">
<title>Publisher&#x2019;s note</title>
<p>All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.</p>
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