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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.2022.1018646</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>Biochar: An emerging recipe for designing sustainable horticulture under climate change scenarios</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Zulfiqar</surname>
<given-names>Faisal</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/603474"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Moosa</surname>
<given-names>Anam</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1965990"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Nazir</surname>
<given-names>Muhammad Mudassir</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1033745"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ferrante</surname>
<given-names>Antonio</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>4</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/109906"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ashraf</surname>
<given-names>Muhammad</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>5</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/336769"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Nafees</surname>
<given-names>Muhammad</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1803085"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Chen</surname>
<given-names>Jianjun</given-names>
</name>
<xref ref-type="aff" rid="aff6">
<sup>6</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/199433"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Darras</surname>
<given-names>Anastasios</given-names>
</name>
<xref ref-type="aff" rid="aff7">
<sup>7</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1798057"/>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Siddique</surname>
<given-names>Kadambot H.M.</given-names>
</name>
<xref ref-type="aff" rid="aff8">
<sup>8</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/266236"/>
</contrib>
</contrib-group>
<aff id="aff1">
<sup>1</sup>
<institution>Department of Horticultural Sciences, Faculty of Agriculture and Environment, The Islamia University of Bahawalpur</institution>, <addr-line>Bahawalpur</addr-line>, <country>Pakistan</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Department of Plant Pathology, Faculty of Agriculture and Environment, The Islamia University of Bahawalpur</institution>, <addr-line>Bahawalpur</addr-line>, <country>Pakistan</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>Department of Agronomy, College of Agriculture and Biotechnology, Zhejiang University</institution>, <addr-line>Hangzhou</addr-line>, <country>China</country>
</aff>
<aff id="aff4">
<sup>4</sup>
<institution>Department of Agricultural and Environmental Sciences, Universit&#xe0; degli Studi di Milano</institution>, <addr-line>Milan</addr-line>, <country>Italy</country>
</aff>
<aff id="aff5">
<sup>5</sup>
<institution>Institute of Molecular Biology and Biotechnology, The University of Lahore</institution>, <addr-line>Lahore</addr-line>, <country>Pakistan</country>
</aff>
<aff id="aff6">
<sup>6</sup>
<institution>Mid-Florida Research and Education Center, Environmental Horticulture Department, Institute of Food and Agricultural Science, University of Florida</institution>, <addr-line>Apopka, FL</addr-line>, <country>United States</country>
</aff>
<aff id="aff7">
<sup>7</sup>
<institution>Department of Agriculture, University of the Peloponnese</institution>, <addr-line>Kalamata</addr-line>, <country>Greece</country>
</aff>
<aff id="aff8">
<sup>8</sup>
<institution>The UWA Institute of Agriculture, The University of Western Australia</institution>, <addr-line>Perth, WA</addr-line>, <country>Australia</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by: Ravinder Kumar, Central Potato Research Institute (ICAR), India</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by: Iqra Noor, Huazhong Agricultural University, China; Amir Hameed, Government College University, Pakistan</p>
</fn>
<fn fn-type="corresp" id="fn001">
<p>*Correspondence: Faisal Zulfiqar, <email xlink:href="mailto:ch.faisal.zulfiqar@gmail.com">ch.faisal.zulfiqar@gmail.com</email>; Kadambot H.M. Siddique, <email xlink:href="mailto:kadambot.siddique@uwa.edu.au">kadambot.siddique@uwa.edu.au</email>
</p>
</fn>
<fn fn-type="other" id="fn002">
<p>This article was submitted to Plant Abiotic Stress, a section of the journal Frontiers in Plant Science</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>05</day>
<month>12</month>
<year>2022</year>
</pub-date>
<pub-date pub-type="collection">
<year>2022</year>
</pub-date>
<volume>13</volume>
<elocation-id>1018646</elocation-id>
<history>
<date date-type="received">
<day>13</day>
<month>08</month>
<year>2022</year>
</date>
<date date-type="accepted">
<day>17</day>
<month>11</month>
<year>2022</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2022 Zulfiqar, Moosa, Nazir, Ferrante, Ashraf, Nafees, Chen, Darras and Siddique</copyright-statement>
<copyright-year>2022</copyright-year>
<copyright-holder>Zulfiqar, Moosa, Nazir, Ferrante, Ashraf, Nafees, Chen, Darras and Siddique</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>The interest in sustainable horticulture has recently increased, given anthropogenic climate change. The increasing global population will exacerbate the climate change situation induced by human activities. This will elevate global food demands and the vulnerability of horticultural systems, with severe concerns related to natural resource availability and usage. Sustainable horticulture involves adopting eco-friendly strategies to boost yields while maintaining environmental conservation. Biochar (BC), a carbon-rich material, is widely used in farming to improve soil physical and chemical properties and as an organic substitute for peat in growing media. BC amendments to soil or growing media improve seedling growth, increase photosynthetic pigments, and enhances photosynthesis, thus improving crop productivity. Soil BC incorporation improves abiotic and biotic stress tolerance, which are significant constraints in horticulture. BC application also improves disease control to an acceptable level or enhance plant resistance to pathogens. Moreover, BC amendments in contaminated soil decrease the uptake of potentially hazardous metals, thus minimizing their harmful effects on humans. This review summarizes the most recent knowledge related to BC use in sustainable horticulture. This includes the effect of BC on enhancing horticultural crop production and inducing resistance to major abiotic and biotic stresses. It also discuss major gaps and future directions for exploiting BC technology.</p>
</abstract>
<kwd-group>
<kwd>sustainability</kwd>
<kwd>pyrolysis</kwd>
<kwd>abiotic stresses</kwd>
<kwd>oxidative stress</kwd>
<kwd>sustainable agriculture</kwd>
<kwd>growing media</kwd>
</kwd-group>
<counts>
<fig-count count="6"/>
<table-count count="1"/>
<equation-count count="0"/>
<ref-count count="98"/>
<page-count count="16"/>
<word-count count="7382"/>
</counts>
</article-meta>
</front>
<body>
<sec id="s1" sec-type="intro">
<title>Introduction</title>
<p>Horticulture is a vital multidisciplinary sector that differs from common agriculture in terms of crops, more intensive production systems, and final profit margins. Horticultural crops include fruits and nuts, vegetables and herbs, ornamental flowering plants, trees and shrubs, lawns, and medicinal plants. Some crops are grown in containers on substrates or in growing media in greenhouses. Container substrates largely comprise organic matter, including peat moss, pine bark, coconut fiber (coir), and composted materials (<xref ref-type="bibr" rid="B10">Chen and Wei, 2018</xref>). Some crops are grown in soils under protected culture, and others are grown in open fields. The sector is progressively moving toward &#x201c;sustainable intensification,&#x201d; producing more biomass or food while maintaining environmental sustainability. Horticultural intensification is urgently needed as the global food demand between 2010 and 2050 is projected to increase by 35%&#x2013;56% (<xref ref-type="bibr" rid="B77">van Dijk et&#xa0;al., 2021</xref>). Moreover, climate change is expected given the planet&#x2019;s steadily growing human population. Therefore, advanced restoration approaches are required because various anthropogenic activities have increased greenhouse gas (GHG) emissions and temperatures, resulting in abnormal precipitation patterns and other climate disturbances (<xref ref-type="bibr" rid="B70">Sharma et&#xa0;al., 2022</xref>).</p>
<p>In recent years, renewable energy use has increased due to changing climatic conditions and energy demands (<xref ref-type="bibr" rid="B92">Zhang et&#xa0;al., 2022</xref>). Climate change has brought new challenges to horticulture since the quality of horticultural crops depends on several climatic factors (<xref ref-type="bibr" rid="B70">Sharma et&#xa0;al., 2022</xref>). For example, how to produce high-quality horticultural produce sustainably, improve crop tolerance to high (heat), chilling, or freezing temperatures, sustain crop growth under drought stress, reduce peat moss use in container substrates as peat mining releases considerable GHGs (<xref ref-type="bibr" rid="B13">Cleary et&#xa0;al., 2005</xref>), and maintain crop productivity with minimal damage from insects or pathogens (<xref ref-type="bibr" rid="B30">Gregory et&#xa0;al., 2009</xref>)&#x2014;all of which require new strategies to improve food production to ensure global food security (<xref ref-type="bibr" rid="B92">Zhang et&#xa0;al., 2022</xref>). Producing horticultural crops by amending soils or container substrates with selected BC has great potential for counteracting the challenge of climate change and producing horticultural products in an environmentally friendly manner.</p>
<p>Biochar is a solid charcoal-like carbonaceous material produced through a thermochemical conversion process of organic biomass under the quasi-absence of oxygen at temperatures ranging from 350 to 900&#xb0;C, a process referred to as pyrolysis (<xref ref-type="bibr" rid="B46">Lehmann and Joseph, 2009</xref>; <xref ref-type="bibr" rid="B19">Fan et&#xa0;al., 2021</xref>). This process converts the agricultural, industrial, or urban organic matter into different fractions of solid (biochar), gas (syngas), and liquid (bio-oil) products (<xref ref-type="fig" rid="f1">
<bold>Figure&#xa0;1</bold>
</xref>). The physical and chemical properties of BC vary substantially depending on feedstocks, temperatures, pyrolysis methods, and feedstock modifications (<xref ref-type="bibr" rid="B91">Yu et&#xa0;al., 2019</xref>). The physical properties of BC include surface area, density and porosity, pore size and volume, hydrophobicity, and water-holding capacity. In general, surface area, porosity, and pore volume increase with increased pyrolysis temperature. Biochar surface area ranges from 100 to 800 m<sup>2</sup>/g, and porosity ranges from 50% to 70%. Bulk density is rather low, &lt;0.6 g/cm<sup>3</sup> (<xref ref-type="bibr" rid="B91">Yu et&#xa0;al., 2019</xref>). Hydrophobicity is associated with surface function groups, and water-holding capacity depends on porosity. Chemical properties of BC include pH, cation exchange capacity, elemental composition, and surface functionality. Biochar pH and cation exchange capacity increase with increasing pyrolysis temperatures. Biochar pH varies from 5.9 to 12.3 (average 8.9). The elemental composition of BC depends on feedstock and pyrolysis temperature. The BC surface is important as various biological and chemical activities are related to surface functional groups, free radicals, surface charge, and structure-related functionality (<xref ref-type="bibr" rid="B91">Yu et&#xa0;al., 2019</xref>). Functional groups include acyl, amido, azyl, carbonyl, carboxyl, ether, ester, hydroxyl, and sulfonic (<xref ref-type="bibr" rid="B83">Yang et&#xa0;al., 2019</xref>), with critical roles in regulating pH, cation exchange capacity, nutrient and gas adsorption, contaminant degradation, and soil microbial community interactions.</p>
<fig id="f1" position="float">
<label>Figure&#xa0;1</label>
<caption>
<p>Illustration of biochar (BC) manufactured from various solid waste materials (left) and the transformation of these waste materials into useful products <italic>via</italic> pyrolysis (middle) and the associated horticultural benefits (right).</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-13-1018646-g001.tif"/>
</fig>
<p>Biochar has a multifunctional role, including GHG sequestration, improving soil properties, seed germination, crop yield and quality of horticulture produce, and increasing crop tolerance to abiotic and biotic stresses (<xref ref-type="bibr" rid="B44">Kochanek et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B5">Almaroai and Eissa, 2020</xref>; <xref ref-type="bibr" rid="B96">Zulfiqar et&#xa0;al., 2021a</xref>; <xref ref-type="bibr" rid="B97">Zulfiqar et&#xa0;al., 2021b</xref>; <xref ref-type="bibr" rid="B35">Ibrahim et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B41">Ji et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B76">Taqdees et&#xa0;al., 2022</xref>) (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2</bold>
</xref>). This review summarizes current progress on using BC to improve soil and substrate properties, seed germination, root growth, water and nutrient absorption, photosynthesis, crop yield, and tolerance to plant pathogens. The review also illustrates how BC can mitigate the adverse impacts of abiotic stresses on horticultural crops under climate change and discusses research gaps and the prospects of BC use for achieving high-quality maximum yields.</p>
<fig id="f2" position="float">
<label>Figure&#xa0;2</label>
<caption>
<p>Multifunctional role of BC in horticulture sector demonstrates a positive impact of BC for ensuring food security under the threat of climate change.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-13-1018646-g002.tif"/>
</fig>
</sec>
<sec id="s2">
<title>Biochar application sequestrates greenhouse gases, improves soil properties, and reduces peat moss use in substrates</title>
<sec id="s2_1">
<title>Sequestration of greenhouse gases</title>
<p>Production of BC reduces CO<sub>2</sub> in the atmosphere because the decay or decomposition of organic materials naturally omits CO<sub>2</sub> into the atmosphere, while converting those materials into carbon-neutral products eliminates the decomposition process. <xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3</bold>
</xref> illustrates how BC is made from different agricultural materials. <xref ref-type="bibr" rid="B80">Woolf et&#xa0;al. (2010)</xref> showed that sustainable implementation of BC could offset up to 12% of global anthropogenic CO<sub>2</sub>. Composting manure is a major GHG source, but incorporating 10% (w/w) BC during composting reduced GHG emissions substantially (<xref ref-type="bibr" rid="B88">Yin et&#xa0;al., 2021</xref>). Application of BC to soil facilities for carbon capture and storage (CCS) is associated with carbon sequestration, soil, and water remediation, decreased GHG emissions, improved soil fertility, crop production, and waste management and recycling (<xref ref-type="bibr" rid="B33">Haider et&#xa0;al., 2022</xref>). Compared to other organic materials, the internal structure of BC has a remarkably high degree of stability, providing long-term soil fertility (<xref ref-type="bibr" rid="B3">Agegnehu et&#xa0;al., 2017</xref>). Mixing BC in soil at 13.5 t/ha (3% of the upper 30&#xa0;cm layer) can provide carbon storage space for two centuries (<xref ref-type="bibr" rid="B59">Matovic, 2011</xref>). Biochar application to horticultural fields will also contribute to CCS. However, one study showed that BC application increased soil CO<sub>2</sub> fluxes and reduced N<sub>2</sub>O fluxes with no effect on CH<sub>4</sub> fluxes (<xref ref-type="bibr" rid="B34">He et&#xa0;al., 2017</xref>). The variable results could be attributed to multiple factors, including the differences in physical and chemical properties of BC and soil, variations in crop species in the tested field, climate differences, and the duration of the reported studies. The incorporation of BC into horticultural substrates mitigates CO<sub>2</sub>, CH<sub>4</sub>, and N<sub>2</sub>O emissions. In a microcosm incubation study, total CO<sub>2</sub>, CH<sub>4</sub>, and N<sub>2</sub>O emissions decreased by 50%, 21%, and 66%, respectively, in a substrate amended with biochar compared to one without BC (<xref ref-type="bibr" rid="B48">L&#xe9;vesque et&#xa0;al., 2018</xref>).</p>
<fig id="f3" position="float">
<label>Figure&#xa0;3</label>
<caption>
<p>Various biochars made from agricultural waste material in a pyrolysis reactor.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-13-1018646-g003.tif"/>
</fig>
</sec>
<sec id="s2_2">
<title>Improved soil physical, chemical, and biological properties</title>
<p>Biochar application can improve soil physical, chemical, and biological properties (<xref ref-type="bibr" rid="B91">Yu et&#xa0;al., 2019</xref>) (<xref ref-type="fig" rid="f4">
<bold>Figure&#xa0;4</bold>
</xref>). A meta-analysis indicated that BC amendment decreased soil bulk density by 3%&#x2013;31% (mean 7.6%) in 19 of 22 soils (<xref ref-type="bibr" rid="B65">Omondi et&#xa0;al., 2016</xref>). Fruit production usually occurs in hilly and low mountain areas where soil compaction is a problem. <xref ref-type="bibr" rid="B66">Peake et&#xa0;al. (2014)</xref> reported that BC addition reduced soil compaction by more than 10%. Soil bulk density is negatively associated with soil porosity, so a decreased bulk density increases soil porosity. Biochar application can increase soil porosity by 8.4% (<xref ref-type="bibr" rid="B65">Omondi et&#xa0;al., 2016</xref>) and improve soil structural quality and aggregation (<xref ref-type="bibr" rid="B7">Blanco-Canqui, 2017</xref>). In general, soil water retention improves with reduced bulk density, increased porosity, and improved structural quality.</p>
<fig id="f4" position="float">
<label>Figure&#xa0;4</label>
<caption>
<p>A visual demonstration of biochar impacts on soil properties.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-13-1018646-g004.tif"/>
</fig>
<p>Biochar application can increase pH in acidic soils, improve soil organic carbon, increase nutrient holding capacity due to the role of functional groups, reduce the adverse effects of heavy metal adsorption, and increase the nutrient elements supplied by the BC (<xref ref-type="bibr" rid="B91">Yu et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B9">Chang et&#xa0;al., 2021</xref>). A meta-analysis of 59 reports published from 2012 to 2021 showed that BC application increased soil pH, cation exchange capacity, and organic carbon by 46%, 20%, and 27%, respectively (<xref ref-type="bibr" rid="B71">Singh et&#xa0;al., 2022</xref>). Biochar application to soils also increased the relative abundance of bacteria involved in soil carbon and nitrogen cycles, soil organic carbon decomposition, and plant disease suppression and significantly increased invertase and catalase activities (<xref ref-type="bibr" rid="B50">Li et&#xa0;al., 2021</xref>). Biochar application resulted in favorable conditions for soil microorganisms, improving microbial biomass carbon (C<sub>mic</sub>) (<xref ref-type="bibr" rid="B56">Luo et&#xa0;al., 2014</xref>). Biochar application has been reported to relate to unique characteristics of BC, including altered root growth strategy, rhizosphere soil nutrient availability (<xref ref-type="bibr" rid="B51">Liu et&#xa0;al., 2022</xref>), and improved soil enzyme activities (<xref ref-type="bibr" rid="B49">Li et&#xa0;al., 2022a</xref>).</p>
</sec>
<sec id="s2_3">
<title>Biochar as a component of container substrates</title>
<p>Peat is commonly used for horticultural purposes. However, the resultant depletion of peatlands has led to an increasing environmental concern about non-renewable resource peat extraction (<xref ref-type="bibr" rid="B93">Zulfiqar et&#xa0;al., 2019a</xref>; <xref ref-type="bibr" rid="B98">Zulfiqar et&#xa0;al., 2019b</xref>). Hence, there is a continuous search for sustainable growing media substitutes, such as biochar (<xref ref-type="fig" rid="f5">
<bold>Figure&#xa0;5</bold>
</xref>). <xref ref-type="bibr" rid="B23">Ferlito et&#xa0;al. (2020)</xref> evaluated conifer wood BC as a growing medium component for citrus nurseries. The authors found that BC (25%) could be used in growing media comprising 50% sandy volcanic soil and 25% black peat or combined with compost (1:1) for healthy citrus production. In <italic>Lavandula angustifolia</italic> potted plants, <xref ref-type="bibr" rid="B22">Fascella et&#xa0;al. (2020)</xref> incorporated different BC concentrations (0, 25, 50, 75, and 100%, by volume) into peat mixtures. The treatments with 25, 50, and 75% BC improved agronomic traits and flower production in <italic>L. angustifolia</italic>. In lettuce (<italic>Lactuca sativa</italic>), <xref ref-type="bibr" rid="B63">Mendez et&#xa0;al. (2017)</xref> replaced 10% (by vol.) of peat with sewage sludge BC, improving biomass production by 184%&#x2013;270% compared with 100% peat-based substrate due to enhanced microbial activities and NPK concentrations. <xref ref-type="bibr" rid="B12">Choi et&#xa0;al. (2018)</xref> reported that growing medium mixes comprising 20% pine bark and 80% BC (by vol.) boosted fresh and dry weights in chrysanthemum (<italic>Chrysanthemum nankingense</italic>) compared to the control with no BC. In the potted houseplant <italic>Syngonium podophyllum</italic>, <xref ref-type="bibr" rid="B98">Zulfiqar et&#xa0;al. (2019b)</xref> reported that BC incorporation (up to 20%) improved plant growth by improving leaf gas exchange, NPK concentrations, total soluble proteins, and soluble phenolics in leaves. <xref ref-type="bibr" rid="B47">L&#xe9;vesque et&#xa0;al. (2020)</xref> reported improved growth of tomato and sweet pepper in peat-based growing media incorporating 10% or 15% (v/v) BC, with improved plant water use efficiencies, N and P uptake efficiencies, and increased fruit dry weights. In potted <italic>Alpinia zerumbet</italic>, <xref ref-type="bibr" rid="B97">Zulfiqar et&#xa0;al. (2021b)</xref> evaluated the impact of BC incorporation in a peat&#x2013;perlite-based growing medium; growth improved with 30% BC (v/v) alone or in combination with 5% compost by regulating NPK uptake and leaf gas exchange traits. In <italic>Rhododendron delavayi</italic> Franch., <xref ref-type="bibr" rid="B8">Bu et&#xa0;al. (2022)</xref> evaluated the impact of two BC (v/v) applications in peat-based growing media, reporting improved plant and root growth, photosynthesis, and contents of carotenoids, polyphenols, and anthocyanins. The authors suggested using peat-based substrates containing 20% wood chip BC or 30%&#x2013;40% rice husk BC for good growth.</p>
<fig id="f5" position="float">
<label>Figure&#xa0;5</label>
<caption>
<p>Biochar inclusion as an organic component of growing media could replace the non-renewable resource (peat), resulting in a sustainable and environmentally friendly soilless growing media.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-13-1018646-g005.tif"/>
</fig>
<p>Leaching nutrients, particularly N and P, from container substrates is a concern in ornamental plant production (<xref ref-type="bibr" rid="B10">Chen and Wei, 2018</xref>), as continuous leaching year-round can cause surface and/or groundwater contamination. Engineered Mg-enriched biochar can adsorb &gt;100 mg P/g substrate (<xref ref-type="bibr" rid="B86">Yao et&#xa0;al., 2013</xref>), and Mg- and Fe-enriched LDH (layered double hydroxide) biochar can adsorb nitrate close to 25 mg/g (<xref ref-type="bibr" rid="B82">Xue et&#xa0;al., 2016</xref>). Biochar application to soil can reduce nitrate and ammonium leaching (<xref ref-type="bibr" rid="B42">Karhu et&#xa0;al., 2021</xref>). Thus, selected biochars could be used to sustain nutrients in substrates and soils and reduce leaching.</p>
</sec>
</sec>
<sec id="s3">
<title>Biochar improves seed germination of horticultural crops</title>
<p>Seed germination is an integral process in horticultural production, defining initial crop growth vigor and plant density to achieve optimal production and profit margins (<xref ref-type="bibr" rid="B94">Zulfiqar, 2021</xref>). Studies related to BC impacts on germination vary from inhibitory to stimulatory in nature depending on feedstock, pyrolysis temperature, quantity used, and crop species. Generally, positive impacts are related to low rather than high BC doses (<xref ref-type="bibr" rid="B6">Bai et&#xa0;al., 2022</xref>). Incorporating BC into soil or growing media can improve or alter porosity and water-holding capacity, enhancing seed germination <italic>via</italic> improved water availability. Salts and phytotoxins in BC negatively affect seed germination by inducing osmotic stress. BC triggers seed germination by releasing karakins, or germination hormones (<xref ref-type="bibr" rid="B44">Kochanek et&#xa0;al., 2016</xref>). BC incorporation also affects the physio-chemical properties of soil, promoting seed germination. For example, <xref ref-type="bibr" rid="B37">Jabborova et&#xa0;al. (2021b)</xref> reported that seed germination of sweet basil (<italic>Ocimum basilicum</italic>) doubled with 1% BC incorporation, while 2% and 3% BC increased germination by 28%&#x2013;30%, compared with the control without BC. Not only pure BC but BC combined with various nanoparticles also promotes seed germination. <xref ref-type="bibr" rid="B76">Taqdees et&#xa0;al. (2022)</xref> reported that BC enriched with silicon nanoparticles (Si-BC) and zinc nanoparticles (Zn-BC) enhanced the seed germination of salt-stressed radish. Thus, BC can play a vital role in the seed germination of different horticultural crops under normal and stressed conditions. However, the extent of seed germination improvement depends on BC application rate, BC type, plant species, and environmental conditions.</p>
</sec>
<sec id="s4">
<title>Biochar regulates plant water, nutrient relations and enhances root growth of horticultural crops</title>
<p>Plant water relations, such as water potential, osmotic potential, and turgor potential, depend on water availability and uptake and the quantity of soluble solutes. Moreover, the addition or application of organic or inorganic solutes may alter plant water relations. For example, <xref ref-type="bibr" rid="B32">Guo et&#xa0;al. (2021a)</xref> reported improved root hydraulic conductance and leaf water potential (&#x3a8;l) in water-stressed tomato grown on a sandy loam soil incorporated with miscanthus straw BC. In another study, <xref ref-type="bibr" rid="B45">Langeroodi et&#xa0;al. (2019)</xref> reported improved leaf relative water content in pumpkin in response to BC application under water deficit irrigation. Furthermore, tomato plants under deficit and partial root-zone drying irrigation supplemented with BC increased relative water content and water use efficiency (<xref ref-type="bibr" rid="B4">Akhtar et&#xa0;al., 2014</xref>). Despite the results above, further investigations are needed to confirm whether BC supplementation alters plant water relations parameters.</p>
<p>BC incorporation into soils and soilless growing media for horticultural crops sensitive to nutritional deficiencies can be an effective strategy to improve plant nutrition under non-stressed and stressed conditions. In drought-stressed faba bean (<italic>Vicia faba</italic> L.), BC application improved leaf N, P, K, and Ca<sup>2+</sup> contents and decreased leaf Na<sup>+</sup> content and the Na<sup>+</sup>/K<sup>+</sup> ratio (<xref ref-type="bibr" rid="B1">Abd El-Mageed et&#xa0;al., 2021</xref>). Leaf and root mineral nutrients increased in response to BC application in cabbage (<italic>Brassica oleracea</italic> var. capitata) under deficit irrigation (<xref ref-type="bibr" rid="B87">Yildirim et&#xa0;al., 2021</xref>). <xref ref-type="bibr" rid="B84">Yang and Zhang (2022)</xref> reported that BC supply affected soil nitrogen cycling by inhibiting related bacteria, leading to enhanced N, P, K, and Mn uptake in Chinese cherry (<italic>Prunus pseudocerasus</italic>). In the tea plant (<italic>Camellia sinensis</italic> Kuntze), BC improved leaf and stem P, K, and Mg concentrations while reducing heavy metals such as Mn and Cu by altering soil pH (<xref ref-type="bibr" rid="B85">Yan et&#xa0;al., 2021</xref>). Under deficit and partial root-zone drying irrigation, BC increased the leaf C:N ratio in tomato plants but had no significant impact on N and C (<xref ref-type="bibr" rid="B4">Akhtar et&#xa0;al., 2014</xref>). The enhanced nutrient uptake by plants could be attributed to the increased nutrient supply provided by applied BC, BC-mediated changes in the rhizosphere that improved soil microbial communities, and increased bioavailability of nutrient elements.</p>
<p>Incorporating BC in soil and soilless growing media positively affects root growth traits. <xref ref-type="bibr" rid="B11">Chiomento et&#xa0;al. (2021)</xref> reported improved root size and biomass of strawberry (<italic>Fragaria</italic> &#xd7; <italic>ananassa</italic> Duch.) treated with the combined application of BC and <italic>Claroideoglomus etunicatum</italic> compared to untreated plants. Likewise, in sweet basil, <xref ref-type="bibr" rid="B37">Jabborova et&#xa0;al. (2021b)</xref> reported that BC application enhanced total root length, root surface area, root volume, and root diameter compared with control plants. Biochar application increased root and shoot weights, root length and volume, and root/shoot ratio of summer savory (<italic>Satureja hortensis</italic> L.) under normal and salt-stressed conditions (<xref ref-type="bibr" rid="B61">Mehdizadeh et&#xa0;al., 2020</xref>). Improved root length was also reported in salt-stressed cowpea (<italic>Vigna unguiculata</italic> (L.) Walp.) in response to BC application (<xref ref-type="bibr" rid="B20">Farooq et&#xa0;al., 2020</xref>). Similarly, <xref ref-type="bibr" rid="B78">Wang et&#xa0;al. (2019)</xref> studied the impact of BC on apple seedlings, reporting higher root surface area (58%), root length (57%), and root volume (63%) than control plants. Moreover, apple seedling root respiration increased with increasing rates of BC application, with 745, 863, 960, and 1,239 nmol O<sub>2</sub>/min/g FW in the 0, 5, 20, and 80 g/kg BC treatments, respectively. The above-mentioned studies indicate that BC application affects root growth, a vital trait for promoting overall plant growth. However, how BC metabolically affects root growth remains unknown and requires further research.</p>
</sec>
<sec id="s5">
<title>Biochar alters phytohormones and improves the photosynthesis of horticultural crops</title>
<sec id="s5_1">
<title>Altering phytohormones in horticultural crops under normal and stressed conditions</title>
<p>Applied BC can interact with plant growth regulators, enhancing plant growth. In a study conducted with Chinese cherry &#x201c;Manaohong&#x201d; (<italic>P. pseudocerasus</italic>), BC application increased indoleacetic acid (IAA), gibberellin A3 (GA), and zeatin levels and decreased abscisic acid (ABA) levels compared to non-treated plants. Moreover, high-throughput sequencing analysis showed the activation of IAA and inactivation of ABA signal transduction at the gene level, revealing that BC improves plant growth by regulating phytohormone signaling (<xref ref-type="bibr" rid="B84">Yang and Zhang, 2022</xref>). <xref ref-type="bibr" rid="B45">Langeroodi et&#xa0;al. (2019)</xref> reported that BC application decreased ABA in pumpkin seedlings under deficit irrigation relative to control plants. <xref ref-type="bibr" rid="B4">Akhtar et&#xa0;al. (2014)</xref> reported that a cotton seed shell and <italic>Oryza sativa</italic> husk BC mixture decreased ABA in potted tomato plants subjected to deficit and partial root-zone drying irrigation. While more research is needed, the positive interactions of BC with IAA, GA, and zeatin may indicate that phytohormone availability could increase plant growth.</p>
</sec>
<sec id="s5_2">
<title>Influencing biosynthesis of photosynthetic pigments</title>
<p>Photosynthetic pigments affect plant photosynthetic rates and are vital determinants of healthy growth and productivity. Application of BC to horticultural crops enhances photosynthetic pigments and rates under normal and stressed conditions. For instance, <xref ref-type="bibr" rid="B84">Yang and Zhang (2022)</xref> reported increased chlorophyll content of the ornamental plant <italic>Centaurea cyanus</italic> L. in response to BC supplementation relative to control plants. Likewise, BC and humic acid treatments improved chlorophyll content in calendula (<italic>Calendula officinalis</italic> L.) compared to controls (<xref ref-type="bibr" rid="B43">Karimi et&#xa0;al., 2020</xref>). In fenugreek (<italic>Trigonella foenum-graecum</italic>), <xref ref-type="bibr" rid="B36">Jabborova et&#xa0;al. (2021a)</xref> reported that BC increased chlorophyll pigments by 30% and carotenoids by 60%. In <italic>Berberis integerrima</italic>, BC applications recovered the chlorophyll contents in Cd-stressed plants compared to non-treated plants. <xref ref-type="bibr" rid="B38">Jabborova et&#xa0;al. (2021c)</xref> also reported that BC increased chlorophyll pigments by 35% in ginger (<italic>Zingiber officinale</italic>) compared to the control. In salt-stressed cowpea (<italic>V. unguiculata</italic> (L.) Walp.), BC improved chlorophyll content by 6% and by 76% when combined with osmopriming (<xref ref-type="bibr" rid="B20">Farooq et&#xa0;al., 2020</xref>). In drought-stressed perennial ryegrass (<italic>Lolium perenne</italic> L.), rice husk BC improved chlorophyll content and drought stress tolerance. <italic>S. podophyllum</italic> plants grown in soilless growing media amended with BC had increased chlorophyll content compared to the non-amended control (<xref ref-type="bibr" rid="B98">Zulfiqar et&#xa0;al., 2019b</xref>). In tomatoes, <xref ref-type="bibr" rid="B58">Massa et&#xa0;al. (2019)</xref> reported decreased chlorophyll SPAD values under normal and nutritional stress conditions using BC. Similarly, <xref ref-type="bibr" rid="B97">Zulfiqar et&#xa0;al. (2021b)</xref> reported decreased chlorophyll content in <italic>A. zerumbet</italic> in response to BC supplementation in a soilless growing medium. SPAD values were also higher in tea plants in response to BC application than in untreated plants (<xref ref-type="bibr" rid="B85">Yan et&#xa0;al., 2021</xref>). In sweet basil, BC applications, especially at higher concentrations (2% and 3%), improved chlorophyll contents compared to low concentrations (1%) and control plants (<xref ref-type="bibr" rid="B37">Jabborova et&#xa0;al., 2021b</xref>). In sum, BC applications can improve photosynthetic pigments in different plants. However, further studies are needed to elucidate the specific mechanism involved.</p>
</sec>
<sec id="s5_3">
<title>Improving leaf gas exchange characteristics</title>
<p>As mentioned above, BC application generally increases photosynthetic pigment contents and thus enhances leaf gas exchange characteristics. For example, <xref ref-type="bibr" rid="B31">Guo et&#xa0;al. (2021b)</xref> showed that BC application to tomato plants under deficit irrigation improved leaf gas exchange, as exemplified by the higher <italic>P<sub>n</sub>
</italic>, <italic>T<sub>r</sub>
</italic>, and <italic>g<sub>s</sub>
</italic> than control plants. <xref ref-type="bibr" rid="B79">Wang et&#xa0;al. (2021)</xref> reported that BC significantly improved Pn, Tr, gs, and water use efficiency in field-grown peanut. In cabbage seedlings under water deficit, a low BC concentration (5%) enhanced <italic>g</italic>
<sub>s</sub>, <italic>P<sub>n</sub>, C<sub>i</sub>
</italic>, and <italic>T<sub>r</sub>
</italic> more than a high BC concentration (10%). A wheat straw-based BC application upregulated leaf gas exchange traits (<italic>g<sub>s</sub>
</italic>, <italic>P<sub>n</sub>
</italic>, <italic>C<sub>i</sub>
</italic>, and <italic>Tr</italic>) and carboxylation use efficiency in <italic>A. zerumbet</italic> grown in a sandy loam soil (<xref ref-type="bibr" rid="B96">Zulfiqar et&#xa0;al., 2021a</xref>). In tea, BC application improved the photosynthetic rate by 17% compared to untreated control plants (<xref ref-type="bibr" rid="B85">Yan et&#xa0;al., 2021</xref>). <xref ref-type="bibr" rid="B45">Langeroodi et&#xa0;al. (2019)</xref> reported that BC improved leaf gas exchange traits in pumpkin (<italic>Cucurbita pepo</italic>) relative to control plants. Likewise, cotton seed shell and rice husk BC increased the leaf photosynthetic rate in potted tomato plants subjected to deficit and partial root-zone drying irrigation (<xref ref-type="bibr" rid="B4">Akhtar et&#xa0;al., 2014</xref>).</p>
</sec>
</sec>
<sec id="s6">
<title>Biochar improves horticultural crop growth, yield, and produce quality</title>
<p>Plant growth and development rely on the health of initial starting materials, such as seeds or propagules, soil water and nutrient availability, water and nutrient absorption, and photosynthesis under the required light and temperature conditions. Biochar application to soil or growing media at an appropriate rate improves seedling growth, affects some phytohormones, and increases photosynthetic pigments and photosynthesis. As a result, studies have shown that exogenous BC application improves growth and yield in plants grown under non-stressed or stressed conditions. For example, <xref ref-type="bibr" rid="B97">Zulfiqar et&#xa0;al. (2021b)</xref> reported improved growth characteristics (plant height, tiller number, shoot diameter, and leaf number) in an important medicinal plant, <italic>A. zerumbet</italic>, in response to wheat straw-based BC alone and combined with compost. <xref ref-type="bibr" rid="B36">Jabborova et&#xa0;al. (2021a)</xref> found that BC application improved plant height, leaf length, leaf number, and leaf width in sweet basil relative to control plants. <xref ref-type="bibr" rid="B78">Wang et&#xa0;al. (2019)</xref> reported improved plant height, root and shoot dry weights, and root/shoot ratio in apple seedlings in response to different BC doses. Moreover, BC application to sandy soil improved the growth, dry matter, and pod yield of green pea (<italic>Pisum sativum</italic> L.) under low water availability (<xref ref-type="bibr" rid="B90">Youssef et&#xa0;al., 2018</xref>). In a field study, 2,544&#x2013;2,625 kg/ha of BC-based fertilizer improved fertilizer efficiency and provided economic benefits in eggplant production relative to traditional fertilization practices (<xref ref-type="bibr" rid="B92">Zhang et&#xa0;al., 2022</xref>). However, the optimum BC application rates for economic profit are site- and crop-specific. For example, in a 3-year field experiment on sugar beet production, 10 t/ha BC had the maximal economical profit, increasing net profit by 6.94 billion dollars compared with no BC application (<xref ref-type="bibr" rid="B53">Li et&#xa0;al., 2022b</xref>). BC incorporation into soilless growing media is increasing due to environmental concerns associated with peat use in potted plant production. Incorporating up to 50% BC maintains the growth of containerized plants and reduces peat use (<xref ref-type="bibr" rid="B69">Regmi et&#xa0;al., 2022</xref>). Biochar not only improves plant growth and yield under normal, non-stressed conditions but also under different stresses, as discussed in the next section.</p>
<p>Despite improving crop growth and yield, BC also improves product quality. In tomato, cotton seed shell, and <italic>O. sativa</italic> husk BC increased fruit quality in terms of titratable acidity in potted tomato plants subjected to deficit and partial root-zone drying irrigation. Similarly, <xref ref-type="bibr" rid="B2">Agbna et&#xa0;al. (2017)</xref> reported increased titratable acidity, vitamin C content, and sugar/acid content ratios in tomato fruits in response to BC addition under different irrigation levels without affecting total soluble sugars. In another study, <xref ref-type="bibr" rid="B74">Suthar et&#xa0;al. (2018)</xref> reported that bamboo biochars pyrolyzed at 300 &#xb0;C and amended at 3% or 450 &#xb0;C and amended at 1% promoted tomato plant growth and significantly increased glucose, fructose, soluble solids, and ascorbic acid contents and sugar-to-acid ratios in fruits compared to other treatments, including the control with no biochar. Improved growth and fruit quality were related to higher concentrations of NO<sub>3</sub>, P, Ca, and Mg in the growing medium. In polluted soil, BC application increased the total acidity, total soluble sugars, vitamin C, and lycopene in tomato fruit compared to no biochar (<xref ref-type="bibr" rid="B5">Almaroai and Eissa, 2020</xref>). Application of BC increased total sugars and flavonoids by 8% in sweet basil compared to control plants (<xref ref-type="bibr" rid="B37">Jabborova et&#xa0;al., 2021b</xref>). In field experiments, BC-based fertilizer amendments increased eggplant yield and quality, including vitamin C and soluble sugar contents (<xref ref-type="bibr" rid="B92">Zhang et&#xa0;al., 2022</xref>).</p>
</sec>
<sec id="s7">
<title>Biochar enhances the stress tolerance of horticultural crops</title>
<p>Environmental conditions such as drought, salt, heavy metals, low or high temperatures, and acidic stress impair plant growth and productivity, adversely affecting overall agricultural sustainability and threatening global food security. Biochar supplementation is an efficient and cost-effective management tool for improving crop productivity in terms of increasing yield and quality. A few studies have focused on the application of BC to plants grown under stress conditions, reporting the beneficial effects of BC on regulating the myriad metabolic processes involved in growth promotion (<xref ref-type="table" rid="T1">
<bold>Table&#xa0;1</bold>
</xref>). <xref ref-type="fig" rid="f6">
<bold>Figure&#xa0;6</bold>
</xref> is a schematic illustration of the positive effects of BC on horticultural crops under abiotic stress.</p>
<table-wrap id="T1" position="float">
<label>Table&#xa0;1</label>
<caption>
<p>The ameliorative effect of biochar on horticultural crops grown under different environmental stresses.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="top" align="left">Name</th>
<th valign="top" align="center">Stress type and level; experiment type</th>
<th valign="top" align="center">Feedstock and concentration used</th>
<th valign="top" align="center">Pyrolysis temperature</th>
<th valign="top" align="center">Functions under stress</th>
<th valign="top" align="center">References</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left">Faba beans (<italic>Vicia faba</italic>)</td>
<td valign="top" align="left">Drought stress (100, 80, and 60% evapotranspiration; field experiment</td>
<td valign="top" align="left">3:100 (w/w) combination of citric acid, and citrus wood biochar; 0, 5, or 10&#xa0;ton ha<sup>&#x2212;1</sup>
</td>
<td valign="top" align="left">Information not mentioned</td>
<td valign="top" align="left">
<list list-type="bullet">
<list-item>
<p>Improved plant growth and physiological responses</p>
</list-item>
<list-item>
<p>Enhanced contents of N, P, K, and Ca.</p>
</list-item>
</list>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B1">Abd El-Mageed et&#xa0;al., 2021</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Pumpkin (<italic>Cucurbita pepo</italic> L.).</td>
<td valign="top" align="left">Drought stress (60%, 75%, and 90%); field experiment</td>
<td valign="top" align="left">Maize-straw biochar 0, 5, 10 and 20&#xa0;ton biochar ha<sup>&#x2212;1</sup>
</td>
<td valign="top" align="left">350&#xb0;C<break/>For 7 days</td>
<td valign="top" align="left">
<list list-type="bullet">
<list-item>
<p>Increased chlorophyll</p>
</list-item>
<list-item>
<p>Enhanced uptake of nutrients</p>
</list-item>
<list-item>
<p>Reduced reactive oxygen species</p>
</list-item>
</list>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B45">Langeroodi et&#xa0;al. (2019)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Tomato (<italic>Solanum lycopersicum</italic>)</td>
<td valign="top" align="left">Deficit irrigation and partial root drying</td>
<td valign="top" align="left">Mixture of rice husk and shell of cotton seed biochar; 0% and 5% by weight</td>
<td valign="top" align="left">400&#xb0;C</td>
<td valign="top" align="left">
<list list-type="bullet">
<list-item>
<p>Improved photosynthesis</p>
</list-item>
<list-item>
<p>Enhanced relative water content and water use efficiency</p>
</list-item>
<list-item>
<p>Improved fruit yield and quality</p>
</list-item>
<list-item>
<p>Decreased membrane stability index</p>
</list-item>
<list-item>
<p>Decreased ABA content.</p>
</list-item>
</list>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B4">Akhtar et&#xa0;al. (2014)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Cabbage (<italic>Brassica oleracea</italic>)</td>
<td valign="top" align="left">Drought stress (100% and 50% irrigation); pot experiment</td>
<td valign="top" align="left">Commercial biochar comprising 60% sewage sludge and 40% domestic wastes; 0%, 5%, or 10%</td>
<td valign="top" align="left">1st stage reactor was kept at 150&#xb0;C under 5&#x2013;8 bar<break/>Pressure; 2nd<break/>stage reactor (hydrolysis)<break/>(250&#xb0;C) and<break/>pressure (50&#xa0;bar); 3rd stage reactor (cracker): 550&#xb0;C),</td>
<td valign="top" align="left">
<list list-type="bullet">
<list-item>
<p>Recovered plant growth</p>
</list-item>
<list-item>
<p>Improved leaf gas exchange traits</p>
</list-item>
<list-item>
<p>Reduced MDA, H<sub>2</sub>O<sub>2</sub>, proline, and sucrose content</p>
</list-item>
<list-item>
<p>Enhanced mineral nutrient content of leaf and root</p>
</list-item>
</list>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B87">Yildirim et&#xa0;al. (2021)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Summer<break/>savory (<italic>Satureja hortensis</italic> L.)</td>
<td valign="top" align="left">Salt stress (0, 3, 5, and 7 dS m<sup>&#x2212;1</sup>); pot experiment</td>
<td valign="top" align="left">Woody branches of <italic>Morus alba</italic> L.; 0, 1% and 2% of total pot</td>
<td valign="top" align="left">530&#xb0;C<break/>temperature for 14 h</td>
<td valign="top" align="left">
<list list-type="bullet">
<list-item>
<p>Improved fresh and dry biomass</p>
</list-item>
<list-item>
<p>Improved root morphological traits</p>
</list-item>
<list-item>
<p>Enhanced leaf SPAD value</p>
</list-item>
<list-item>
<p>Increased proline content</p>
</list-item>
<list-item>
<p>Decreased membrane injury</p>
</list-item>
<list-item>
<p>Reduced Na<sup>+</sup> and Cl<sup>-</sup> contents</p>
</list-item>
</list>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B61">Mehdizadeh et&#xa0;al. (2020)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">
<italic>Potato</italic> (<italic>Solanum tuberosum</italic>)</td>
<td valign="top" align="left">Salt stress; field experiment</td>
<td valign="top" align="left">Rice husk; 825 kg/ha</td>
<td valign="top" align="left">Pyrolyzed in an oven at 350&#xb0;C for 24 h</td>
<td valign="top" align="left">
<list list-type="bullet">
<list-item>
<p>Improved plant growth</p>
</list-item>
<list-item>
<p>Enhanced leaf gas exchange traits</p>
</list-item>
<list-item>
<p>Enhanced gibberellic acid and decreased abscisic acid</p>
</list-item>
</list>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B57">Mahmoud et&#xa0;al. (2022)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Cow pea (<italic>Vigna unguiculata</italic> (L.) Walp.)</td>
<td valign="top" align="left">Salt stress; 10 dS m<sup>&#x2212;1</sup>; pot experiment</td>
<td valign="top" align="left">Mango wood biochar; plastic pots (150&#xa0;mm &#xd7; 90&#xa0;mm) filled with peat<break/>moss having biochar (25&#xa0;g per pot)</td>
<td valign="top" align="left">500&#xb0;C for 30 min</td>
<td valign="top" align="left">
<list list-type="bullet">
<list-item>
<p>Improved shoot length, root length, plant biomass and leaf area</p>
</list-item>
<list-item>
<p>Improved chlorophyll contents, amylase activity, total soluble sugars</p>
</list-item>
<list-item>
<p>Decreased Na+ uptake, MDA, and</p>
</list-item>
</list>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B20">Farooq et&#xa0;al. (2020)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">(<italic>Brassica oleracea</italic> var.<break/>capitata)</td>
<td valign="top" align="left">Salt stress; 0 and 150 mM NaCl; pot experiment</td>
<td valign="top" align="left">60%<break/>sewage sludge and 40% domestic wastes; 0%, 2.5%, and 5% by soil weight</td>
<td valign="top" align="left">Depolymerization at 150 &#xb0;C under 5&#x2013;8 bar pressure; Hydrolysis at high temperature (250&#xb0;C) and pressure (50&#xa0;bar), cracker stage at 550&#xb0;C</td>
<td valign="top" align="left">
<list list-type="bullet">
<list-item>
<p>Improved plant growth and biomass</p>
</list-item>
<list-item>
<p>Enhanced chlorophyll</p>
</list-item>
<list-item>
<p>Decreased MDA, H<sub>2</sub>O<sub>2</sub>, sucrose and proline</p>
</list-item>
<list-item>
<p>Enhanced leaf nutrient elements</p>
</list-item>
<list-item>
<p>Decreased Na and Cl content in plant</p>
</list-item>
</list>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B18">Ekinci et&#xa0;al. (2022)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Tomato (<italic>Solanum lycopersicum</italic>)</td>
<td valign="top" align="left">Metal contaminated soil; Field experiment</td>
<td valign="top" align="left">Maize stalks biochar; 0, 5, or 10&#xa0;ton ha<sup>&#x2212;1</sup>
</td>
<td valign="top" align="left">Muffle furnace, set at a heating rate of 15&#xb0;C<break/>min<sup>&#x2013;1</sup> for 2.5&#xa0;h at a peak temperature of 450&#xb0;C.</td>
<td valign="top" align="left">
<list list-type="bullet">
<list-item>
<p>Improved chlorophyll contents</p>
</list-item>
<list-item>
<p>Improved yield and fruit quality</p>
</list-item>
<list-item>
<p>Decreased uptake of heavy metals in both plant parts and fruits</p>
</list-item>
</list>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B5">Almaroai and Eissa (2020)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Lettuce (<italic>Lactuca sativa</italic> L.)</td>
<td valign="top" align="left">Copper contaminated soil; pot experiment</td>
<td valign="top" align="left">Orchard pruning feedstock based commercial biochar; 1% biochar (w/w)</td>
<td valign="top" align="left">550&#xb0;C, slow-pyrolysis</td>
<td valign="top" align="left">
<list list-type="bullet">
<list-item>
<p>Restored antioxidant activity and flavonoids</p>
</list-item>
<list-item>
<p>Increased total phenols, phenolic acids and anthocyanins</p>
</list-item>
</list>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B67">Quartacci et&#xa0;al. (2017)</xref>
</td>
</tr>
</tbody>
</table>
</table-wrap>
<fig id="f6" position="float">
<label>Figure&#xa0;6</label>
<caption>
<p>Positive impact of BC incorporation on plants under normal and stressed conditions.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-13-1018646-g006.tif"/>
</fig>
<sec id="s7_1">
<title>Enhancing drought tolerance</title>
<p>Incorporating BC into growing media or soil can improve crop tolerance to drought stress. Wood pellets BC added to a growing medium (30% v/v) improved tomato seedling tolerance to drought (<xref ref-type="bibr" rid="B64">Mulcahy et&#xa0;al., 2013</xref>). <xref ref-type="bibr" rid="B2">Agbna et&#xa0;al. (2017)</xref> reported that water-stressed tomato plots amended with 25 t/ha of wheat straw BC had similar fruit yields as unstressed control plots, accompanied by increased plant height, leaf numbers, and fresh and dry plant weights. <xref ref-type="bibr" rid="B15">Egamberdieva et&#xa0;al. (2017)</xref> evaluated BC-based <italic>Bradyrhizobium</italic> inoculum on the growth of drought-stressed lupin (<italic>Lupinus angustifolius</italic> L.), noting improved drought tolerance associated with revived growth, increased nutrient uptake, and improved symbiotic performance. <xref ref-type="bibr" rid="B52">Li et&#xa0;al. (2018)</xref> reported that 30 t/ha BC and deficit irrigation saved water without affecting total tomato productivity in a field experiment. In the same experiment, increasing the maize straw BC application rate from 10 to 40 t/ha increased plant dry biomass and fruit yield. However, higher BC application rates had no positive effect or decreased plant growth and yield. Moreover, a cost&#x2013;benefit analysis showed that BC applications of 10, 20, and 40 t/ha positively affected net profit. In contrast, 60 t/ha negatively affected net profit compared with the unamended control. A quadratic function fitting net profit and BC application rate showed an optimal application rate of 27 t/ha (<xref ref-type="bibr" rid="B52">Li et&#xa0;al., 2018</xref>).</p>
<p>In a two-year study on pumpkin (<italic>C. pepo</italic>) under reduced irrigation, <xref ref-type="bibr" rid="B45">Langeroodi et&#xa0;al. (2019)</xref> reported that BC-amended plants had decreased ROS, an elevated antioxidant defense system, and improved photosynthesis and overall growth relative to unamended plants. <xref ref-type="bibr" rid="B17">Egamberdieva et&#xa0;al. (2020b)</xref> evaluated the impact of maize BC on drought-stressed broad beans (<italic>V. faba</italic> L.), reporting improved growth, yield, and nutrient uptake relative to unamended plants. <xref ref-type="bibr" rid="B1">Abd El-Mageed et&#xa0;al. (2021)</xref> studied the impact of acidified BC on drought-stressed <italic>V. faba</italic> under field conditions in a two-year experiment, reporting that BC addition improved plant growth relative to unamended soil. Biochar application to drought-stressed cabbage plants ameliorated the adverse effects of drought stress by increasing leaf water relative content and photosynthetic activities, with a 5% BC application improving shoot and root fresh and dry weights compared to unamended control plants (<xref ref-type="bibr" rid="B87">Yildirim et&#xa0;al., 2021</xref>). <xref ref-type="bibr" rid="B1">Abd El-Mageed et&#xa0;al. (2021)</xref> reported a 39% increase in seed yield of drought-stressed <italic>V. faba</italic> in BC-amended soil under field conditions compared with unamended soil. In a greenhouse experiment, <xref ref-type="bibr" rid="B4">Akhtar et&#xa0;al. (2014)</xref> reported that 5% (w/w) cotton seed shell and <italic>O. sativa</italic> husk BC increased the fruit yield of potted tomato plants subjected to 30% deficit and partial root-zone drying irrigation by 6% and 13%, respectively, compared to fully irrigated control plants. Improved drought tolerance with BC application could be attributed to increased porosity and pore volume in BC-amended soil, increasing the capacity to hold available water under drought stress. Further research is needed to address the effect of different soil porosities and pore volumes with BC application on crop growth under drought stress.</p>
</sec>
<sec id="s7_2">
<title>Enhancing salt tolerance</title>
<p>An estimated 831 million ha of arable land globally is affected by salinity and is expected to increase due to ongoing irrigated farmland growth and climate change (<xref ref-type="bibr" rid="B81">Wu et&#xa0;al., 2022</xref>). Growing crops on saline soils in locations where water supply is frequently limited is necessary to fulfill the food demands of an expanding population (<xref ref-type="bibr" rid="B94">Zulfiqar, 2021</xref>). Biochar incorporation into soil can help ameliorate the adverse impacts of salt stress on plants (<xref ref-type="bibr" rid="B14">Egamberdieva et&#xa0;al., 2022</xref>). For example, <xref ref-type="bibr" rid="B61">Mehdizadeh et&#xa0;al. (2020)</xref> reported that BC application improved growth and leaf mineral nutrients and decreased leaf Na<sup>+</sup> and Cl<sup>&#x2013;</sup> contents in salt-stressed summer savory. In cowpea (<italic>V. unguiculata</italic> (L.) Walp.), BC application improved salt stress tolerance by elevating chlorophyll content, amylase activity, and total soluble sugars and decreasing Na<sup>+</sup> and MDA contents and total antioxidant activity (<xref ref-type="bibr" rid="B20">Farooq et&#xa0;al., 2020</xref>). In salt-stressed spinach, combined <italic>Trichoderma</italic> and BC ameliorated the adverse effect of salt stress by decreasing ROS, altering phytohormones, and improving the physiological condition of plants (<xref ref-type="bibr" rid="B72">Sofy et&#xa0;al., 2021</xref>). <xref ref-type="bibr" rid="B26">Ghassemi-Golezani and Farhangi-Abriz (2021)</xref> reported enhanced salt tolerance in safflower (<italic>Carthamus tinctorius</italic> L.) in response to BC-based metal oxide nanocomposites of manganese (Mn) and magnesium (Mg), with improved root growth, root density, plant height, plant biomass, leaf area, chlorophyll content, branch and flower numbers, potassium, Mg, and Mn contents, duration of the reproductive stage, and seed and oil yields and decreased Na<sup>+</sup> content. BC can also improve plant&#x2019;s ability to cope with salt-induced oxidative stress. For example, <xref ref-type="bibr" rid="B73">Song et&#xa0;al. (2022)</xref> recently reported that organic amendment incorporation, including BC, to salt-affected soil reduced oxidative stress and improved morpho-physiological conditions by promoting Na<sup>+</sup> exclusion and K<sup>+</sup> accumulation in hybrid <italic>Pennisetum</italic>, relieving stomatal restriction, increasing leaf pigment levels, electron transport efficiency, net photosynthesis, and root activity, and reducing oxidative damage.</p>
<p>In another study, <xref ref-type="bibr" rid="B25">Ghassemi-Golezani and Abdoli (2022)</xref> evaluated the impact of BC-based rhizobacteria for mitigating salt stress in rapeseed (<italic>Brassica napus</italic> L.), reporting improved nutrient contents, non-enzymatic antioxidants, main and lateral root lengths and weights, main/lateral root length ratio, specific root length, root diameter, shoot length and weight, leaf area, chlorophyll content, and seed and oil yields, and reduced sodium contents, ROS generation, lipid peroxidation, and enzymatic antioxidant activities in plant tissues. <xref ref-type="bibr" rid="B27">Ghassemi-Golezani and Rahimzadeh (2022)</xref> tested BC-based nutritional nanocomposites for improving salt stress tolerance in dill (<italic>Anethum graveolens</italic>), reporting decreased sodium contents that reduced the levels of osmolytes, antioxidant enzyme activities, ROS, lipid peroxidation, NADP reduction, ABA, jasmonic acid, and salicylic acid in leaves. Moreover, BC addition, particularly BC-based nanocomposites, to salt-affected soil enhanced plant organ biomass, photosynthetic pigments, leaf K, Fe, and Zn contents, leaf water content, hill reaction, ATPase activities, oxygen evolution rate, endogenous indole-3-acetic acid, and essential oil yield (<xref ref-type="bibr" rid="B27">Ghassemi-Golezani and Rahimzadeh, 2022</xref>). <xref ref-type="bibr" rid="B18">Ekinci et&#xa0;al. (2022)</xref> also observed BC-induced salt stress tolerance in cabbage seedlings (<italic>B. oleracea</italic> var. capitata), decreasing malondialdehyde (MDA), hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>), proline, and sucrose contents while increasing leaf and root nutrient contents of cabbage seedlings (except Na and Cl) and regulating ABA contents. BC incorporation also causes osmotic adjustments in plants under salt stress. For instance, BC application ameliorated salt stress in borage (<italic>Borago officinalis</italic> L), a moderately salt-tolerant medicinal plant, by improving plant water status and osmotic adjustment capacity linked to increased photosynthetic pigments, antioxidant activation, osmolyte accumulation, and increased K<sup>+</sup> content and K<sup>+</sup>/Na<sup>+</sup> ratio (<xref ref-type="bibr" rid="B21">Farouk and AL-Huqail, 2022</xref>). Biochar-ameliorated salt stress tolerance could be due to: (1) BC increasing the available water holding capacity of soil and improving soil chemical properties by limiting Na availability to plant roots; (2) BC generally contains high K; and (3) both factors leading to increased K uptake and decreased Na uptake, ameliorating the adverse effects of Na. However, molecular research on BC-mediated salt tolerance is needed to provide more detailed information on salt stress tolerance driven by BC amendment.</p>
</sec>
<sec id="s7_3">
<title>Enhancing tolerance to heavy metals</title>
<p>Heavy metal pollution in soil has become more challenging with increasing urbanization and rapid improvements in agricultural and industrial technologies, posing major threats to human health and the environment. Biochar has gained popularity as a potential substance for successfully immobilizing heavy metals in polluted soil and, thus, reducing their uptake by plants. Controlling metal absorption in horticultural crops is critical for human consumption and maintaining the productivity and quality of horticultural produce. In this context, many studies have found that BC helps reduce heavy metal stress in horticulture crops. <xref ref-type="bibr" rid="B67">Quartacci et&#xa0;al. (2017)</xref> reported that BC addition to contaminated soil restored flavonoids and antioxidant activity and increased phenolic acids, total phenols, and anthocyanins compared to the control. <xref ref-type="bibr" rid="B5">Almaroai and Eissa (2020)</xref> reported that BC decreased the transfer of heavy metals (Pb and Cd) from non-edible parts to edible parts of tomato (<italic>Solanum lycopersicum</italic>) grown in metal-polluted soil, increasing tomato yield by 20%&#x2013;30%. <xref ref-type="bibr" rid="B35">Ibrahim et&#xa0;al. (2022)</xref> tested three BC types (<italic>Casuarina</italic>, mango, and Salix as feedstocks) for their impact on summer squash (<italic>C. pepo</italic> L.) grown in contaminated soil. <italic>Casuarina</italic>-based BC applied at low concentration (2%) had the highest growth rate, while the high concentration (4%) decreased root and shoot uptake of Cd, Co, Cr, Cu, Ni, Pb, and Zn by regulating soil pH, organic matter, and electrical conductivity. Moreover, the 4% <italic>Casuarina</italic>-based BC had the highest reduction in the bioconcentration and translocation factors of these heavy metals. Thus, BC amendment in contaminated soils can improve yield and the quality of produce by reducing the uptake of heavy metals such as Cd, Cu, and Zn (<xref ref-type="bibr" rid="B75">Tahervand et&#xa0;al., 2022</xref>), presenting a novel phytoremediation strategy for contaminated soils by phytostabilizing toxic metals <italic>in situ</italic> while reducing their bioavailability to crops and leaching into groundwater.</p>
</sec>
<sec id="s7_4">
<title>Enhancing tolerance to acidic soils</title>
<p>Acidic soils are known for their lower crop productivity than neutral or alkaline soils, which is attributed to poor fertility, mineral toxicity (e.g., Al, Mn, and Fe), and other nutrient deficiencies. Some horticultural fruit crops and landscape plants often grow in acidic soils, significantly affecting their growth. Biochar can elevate soil pH due to its alkalinity. A BC amendment can also increase plant tolerance to soil acidity. For example, <xref ref-type="bibr" rid="B85">Yan et&#xa0;al. (2021)</xref> reported that BC application improved the growth of tea plants by enhancing leaf area, photosynthesis, and mineral nutrients in acidic soil. <xref ref-type="bibr" rid="B89">Yin et&#xa0;al. (2022)</xref> compared the effects of BC and hydrochar made from cow manure and reed straw on the growth of lettuce under acid soil conditions, reporting that cow manure-based BC amendments improved lettuce growth by increasing soil pH, P and available K contents, soil bacterial activity, and the abundance of beneficial bacteria compared to reed straw and hydrochar.</p>
</sec>
</sec>
<sec id="s8">
<title>Biochar improves plant disease resistance</title>
<p>Biochar application can improve plant tolerance and resistance to plant pathogens. BC contains butyric acid, ethylene glycol, 2-phenoxyethanol, benzoic acid, quinines, o-cresol, hydroxyl-propionic acid, and propylene glycol that impact soil microbiota growth. Soil amendments with low BC concentrations can suppress susceptible disease-causing species through the compounds mentioned above, which ultimately improve plant resistance and crop productivity (<xref ref-type="bibr" rid="B29">Graber et&#xa0;al., 2010</xref>; <xref ref-type="bibr" rid="B24">Frenkel et&#xa0;al., 2017</xref>). Soil BC amendment can lead to disease resistance and vulnerability in horticultural crops due to changes in plant metabolic pathways (<xref ref-type="bibr" rid="B41">Ji et&#xa0;al., 2022</xref>). BC-induced disease suppression or resistance is highly dose-dependent and BC-specific. As a strong absorbent of organic compounds from soil, BC alleviated root rot disease in Chinese ginseng (<italic>Panax ginseng</italic>) (<xref ref-type="bibr" rid="B51">Liu et&#xa0;al., 2022</xref>). In another study, BC addition to soil decreased <italic>Botrytis cinerea-</italic>induced fungal diseases of <italic>Capsicum annuum</italic> and <italic>S. lycopersicum</italic> (<xref ref-type="bibr" rid="B60">Mehari et&#xa0;al., 2015</xref>). In tomatoes, <xref ref-type="bibr" rid="B68">Rasool et&#xa0;al. (2021)</xref> noted that BC induced the expression of defense-associated genes, including jasmonic acid related <italic>PI2</italic>, <italic>TomloxD</italic>, salicylic acid-related <italic>PR1a</italic>, <italic>PR2</italic>, and ethylene-responsive <italic>Pti4</italic>, phenolics, CAT, and POX, to ameliorate infection-induced damage from <italic>Alternaria solani</italic> in tomatoes. <xref ref-type="bibr" rid="B51">Liu et&#xa0;al. (2022)</xref> reported that a BC amendment increased apple seedling growth through the absorption of apple replant disease-causing abiotic factor (phloridzin) from soil. Exogenously applying BC to <italic>F. ananassa</italic> improved resistance against <italic>B. cinerea</italic>, <italic>Podosphaera apahanis</italic>, and <italic>Colletotrichum acutatum</italic> (<xref ref-type="bibr" rid="B62">Meller Harel et&#xa0;al., 2012</xref>). Furthermore, in <italic>Asparagus officinalis</italic>, BC supplementation to soil decreased <italic>Fusarium</italic> root rot infection by 50% more than unamended soil (<xref ref-type="bibr" rid="B28">G&#x142;uszek et&#xa0;al., 2017</xref>).</p>
<p>
<xref ref-type="bibr" rid="B16">Egamberdieva et&#xa0;al. (2020a)</xref> reported that the combined effect of BC and endophytic bacteria improved growth and controlled root rot disease incidence in Fusarium-infested narrow-leafed lupin (<italic>L. angustifolius</italic> L.). Molecular analysis revealed that BC application to tomato plants provided resistance against root rot and Fusarium crown by exerting a priming effect on gene expression. The study showed that BC application upregulated the pathways and genes associated with plant defense and growth, such as auxins, brassinosteroids, cytokinins, jasmonic acid, and the synthesis of cell walls, flavonoids, and phenylpropanoids (<xref ref-type="bibr" rid="B39">Jaiswal et&#xa0;al., 2020</xref>). In another study, <xref ref-type="bibr" rid="B40">Jaiswal et&#xa0;al. (2019)</xref> reported pre-emergence damping-off disease control with BC application in nursery plants. Improved disease resistance is often associated with improved soil bacterial communities (<xref ref-type="bibr" rid="B78">Wang et&#xa0;al., 2019</xref>). Application of peanut shell and wheat straw biochars to soil significantly reduced the disease index of bacterial wilt caused by <italic>Ralstonia solanacearum</italic> by 28.6% and 65.7%, respectively (<xref ref-type="bibr" rid="B55">Lu et&#xa0;al., 2016</xref>). Biochar can offset fungal and bacterial diseases and thwart viral diseases. For example, <xref ref-type="bibr" rid="B54">Luigi et&#xa0;al. (2022)</xref>, using the RT-qPCR technique and <sup>&#x2212;&#x394;&#x394;</sup>Ct analysis, noted that BC addition to soil reduced spotted wilt virus and potato spindle tuber viroid (PSTVd) infection rates and virus replication in tomato.</p>
</sec>
<sec id="s9" sec-type="conclusions">
<title>Conclusions and prospects</title>
<p>Horticultural intensification is urgently needed to feed the increasing global human population. In the post-pandemic-induced financial crisis, increased horticultural production is also needed to keep the industry profitable under the challenges of climate change and poor sustainability. Biochar is an organic material with huge potential for use as a sustainable material to meet such urgent targets in horticulture. This review discusses recent studies on the possible positive outcomes of BC in horticulture, especially those related to plant physio-biochemical mechanisms. However, studies are needed to evaluate different feedstocks at different concentrations and functional group modifications to meet specific needs for BC application. Moreover, molecular studies are needed to better understand BC-induced positive impacts on different plants. Most studies have been performed in pots; hence, future studies should be field-oriented and across more than one growing season to better evaluate BC-induced outcomes. Nano-forms of BC should be tested in horticulture. Using raw BC in soils or growing media is financially unrealistic due to the high initial costs; hence, appropriate technology needs to be developed for economic BC production to meet the long-term horticultural industry&#x2019;s needs. Moreover, the increase in industrialization has exacerbated the heavy metal issue, and BC strategies should be designed to minimize the uptake of hazardous materials in fruits and vegetables. Moreover, in most developing countries, vegetable production is often close to major towns to meet local market needs and reduce transportation costs. However, it frequently relies on town sewage water, a source of heavy metals and pollutants. Hence, testing BC with sewage water for the safe production of horticultural produce would be a breakthrough technology. In addition, BC in a processed form, such as BC-based slow-release fertilizers or peat alternative growing media, should be commercialized for sustainable horticulture. Studies should also be carried out combining BC application with microbial and non-microbial bio-stimulants to open new opportunities for enhancing horticultural production. In summary, the horticulture sector can increase productivity with profitability and sustainability using BC-amendment technologies.</p>
</sec>
<sec id="s10" sec-type="author-contributions">
<title>Author contributions</title>
<p>FZ conceived the idea, prepared the first draft, and revised the manuscript. All authors listed have made a substantial, direct, and intellectual contribution to the work and approved it for publication.</p>
</sec>
<sec id="s11" 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="s12" 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>
</sec>
</body>
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