Realising the promise of arbuscular mycorrhizal fungal biofertilisers through more applied research

IF 8.3 1区 生物学 Q1 PLANT SCIENCES New Phytologist Pub Date : 2024-12-23 DOI:10.1111/nph.20363
Matthias J. Salomon, Stephanie J. Watts-Williams
{"title":"Realising the promise of arbuscular mycorrhizal fungal biofertilisers through more applied research","authors":"Matthias J. Salomon, Stephanie J. Watts-Williams","doi":"10.1111/nph.20363","DOIUrl":null,"url":null,"abstract":"<div>Arbuscular mycorrhizal fungi (AMF) have been recognised for decades as critical contributors to sustainable agriculture. By forming symbiotic relationships with plant roots, AMF can enhance nutrient uptake, improve abiotic and biotic stress tolerance, and generally promote soil health (Fitter <i>et al</i>., <span>2011</span>). Since the 1980s, their potential has been explored extensively, with researchers advocating the management of mycorrhizal communities through applications such as biofertilisers. This is of particular interest in areas where natural AMF communities are absent, or their function is limited. The promise held by managing AMF for enhancing crop yield and nutrition was largely developed through countless research articles advocating their potential benefits. However, despite this extensive research, their real-world application has consistently fallen short, especially with commercially available inoculants. In an article recently published in <i>New Phytologist</i>, Koziol <i>et al</i>. (<span>2024b</span>, doi: 10.1111/nph.20278) provide a comprehensive evaluation of commercial AMF inoculants over the last 20 years through meta-analysis. The findings present a clear conclusion that commercially produced AMF inoculants have not delivered on the long-standing promise of improving sustainable agriculture. Significant quality issues were found, suggesting a disconnect between the expectations formed through laboratory studies and the outcomes realised by commercial products. <blockquote><p>‘To truly harness the potential of AMF biofertilisers in sustainable agriculture, we must bridge the gap between conceptual AMF studies and practical applications.’</p>\n<div></div>\n</blockquote>\n</div>\n<p>Overall, the findings of Koziol <i>et al</i>. (<span>2024b</span>) are sobering, highlighting fundamental quality issues with commercial AMF inoculants. At the most basic level, these products are often ineffective from the onset due to insufficient numbers of viable propagules by the time they reach consumers. This lack of viability means that many inoculants fail to establish any symbiotic arbuscular mycorrhizal relationship through the colonisation of plant roots, which is critical for the realisation of the expected benefits. Koziol <i>et al</i>. (<span>2024b</span>) found that the application of 84% of commercial inoculants resulted in insufficient (&lt; 5%) mycorrhizal root colonisation. Ten observations resulted in the complete opposite of the desired effect of the product — crop mortality following application. Despite decades of AMF biofertiliser being marketed, these basic shortcomings have persisted, pointing to a systemic failure in their production, quality assurance and retail. This also points to the absence of clear quality assurance guidelines and frameworks, which is contributing to the persistence of these issues (Salomon <i>et al</i>., <span>2022</span>). However, it is not impossible to produce effective inoculants. Koziol <i>et al</i>. (<span>2024b</span>) also highlighted that most laboratory-produced inoculants have demonstrated successful mycorrhizal root colonisation, as have a small number of commercial products. This highlights that it is indeed possible to produce commercial AMF biofertilisers that align closer with expectations.</p>\n<p>The implications of these findings are substantial and extend beyond the academic world to various other considerations around agriculture and sustainability. The end-user of AMF biofertilisers are often left with products that do not fulfil their promises, resulting in economic losses and unrealised environmental benefits. Koziol <i>et al</i>. (<span>2024b</span>) estimated that if 88% of commercial AMF products are either unable to colonise roots, or are ineffective at promoting crop yields, then $876 million USD is wasted globally by primary producers. The ongoing presence of ineffective products in the market undermines trust in this biotechnological tool, making it harder for genuine products to be identified and accepted. These failures not only affect agricultural practices but also risk tarnishing the reputation of mycorrhizal research itself. As a result, we have seen missed opportunities for progress over several decades.</p>\n<p>A ‘chicken and egg’ dilemma remains over who is responsible for advancing applied AMF research, where both academia and industry could deflect responsibility onto the other. Advocating from an academic standpoint, one could argue that meaningful progress requires proactive efforts, and academia is well-positioned to initiate these changes. This means that the science behind AMF biofertilisers could be advanced to a point where producers can no longer justify the persistent shortcomings of ineffective products due to a lack of knowledge.</p>\n<p>Achieving this goal demands a shift in scientific focus. For decades, countless conceptual studies have explored the effects of AMF on plant and soil systems, often concluding that soils should be managed to boost natural AMF communities or that inoculation with AMF species could enhance crop outcomes. However, significant knowledge gaps hinder our ability to realise these suggestions. To truly harness the potential of AMF biofertilisers in sustainable agriculture, we must bridge the gap between conceptual AMF studies and practical applications. The scientific community must move beyond merely advocating for AMF use, and instead address the practical challenges that limit their effectiveness in real-world settings. A few newer studies, such as Lutz <i>et al</i>. (<span>2023</span>), have worked in this direction by predicting AMF establishment after the inoculation of a broad range of agricultural soils. This is just one area of research that seems long overdue and should have been prioritised decades ago. Many other scientific foundations for AMF biofertilisers remain underdeveloped, still relying heavily on preliminary and decades-old research.</p>\n<p>Based on the current state of the AMF biofertiliser industry, several very basic research directives are urgently needed (Fig. 1 for summary). One of the biggest shortcomings highlighted by Koziol <i>et al</i>. (<span>2024b</span>) is the lack of viability during storage. Research should examine how different production methods, storage conditions, and carrier materials impact propagule viability. Also, understanding the inoculation potential of spores, compared to infected root pieces and hyphal fragments, is critical for improving AMF biofertiliser quality. Another key aspect is determining the optimal spore density required per plant or per square meter to ensure effective root colonisation and plant growth promotion. This should be combined with spore viability testing to identify reliable methods, such as water agar germination or spore metabolic staining, that can help predict successful colonisation. Additionally, evaluating whether AMF can persist over multiple growing seasons and how factors such as soil management practices (especially fallow periods, fungicide application), crop rotations (that may include nonhost crops such as canola) and climate (rainfall, temperature) impact AMF persistence and overall functionality. It is also essential to consider the risks associated with AMF biofertilisers, such as the potential displacement of native AMF communities and the unintended introduction of pathogens (Schwartz <i>et al</i>., <span>2006</span>; Koziol <i>et al</i>., <span>2024a</span>). This necessitates conducting genetic analyses of inoculated agricultural soils as well as the commercial AMF inoculum to assess their compatibility, potential risks, and ensure biosecurity. Such research directives will help predict and model AMF establishment, providing a foundational framework that can be integrated with further studies, for example, improving functional traits of the mycorrhizal community.</p>\n<figure><picture>\n<source media=\"(min-width: 1650px)\" srcset=\"/cms/asset/2d18ba35-252c-4cae-8127-4d7a4833db01/nph20363-fig-0001-m.jpg\"/><img alt=\"Details are in the caption following the image\" data-lg-src=\"/cms/asset/2d18ba35-252c-4cae-8127-4d7a4833db01/nph20363-fig-0001-m.jpg\" loading=\"lazy\" src=\"/cms/asset/93ea5953-5c4c-49be-aa79-4361eb45b1e5/nph20363-fig-0001-m.png\" title=\"Details are in the caption following the image\"/></picture><figcaption>\n<div><strong>Fig. 1<span style=\"font-weight:normal\"></span></strong><div>Open in figure viewer<i aria-hidden=\"true\"></i><span>PowerPoint</span></div>\n</div>\n<div>Proposed research directives aimed at advancing arbuscular mycorrhizal fungi (AMF) biofertiliser development. Key areas of focus include researching the infectious potential of various AMF propagules (spores, root pieces, hyphae), the risks associated with biofertiliser application, the persistence of AMF in the field post-inoculation, the viability of propagules following storage, and the determination of application rates necessary to achieve effective root colonisation.</div>\n</figcaption>\n</figure>\n<p>What might initially seem like trivial research tasks are complicated by the various environmental factors that significantly influence AMF behaviour. This means that research must be conducted across diverse AMF species and environmental or production systems to build a robust body of knowledge. This is similar to what has been done in other areas of AMF research, such as its impact on plant nutrition. Although debates remain regarding concepts like the previously termed ‘mutualism–parasitism continuum’ (Bennett &amp; Groten, <span>2022</span>), the research community has largely reached a consensus on the common modes of AMF action when it comes to plant nutrition. The aim should be to achieve a similar strong knowledge base for research areas more closely related to AMF biofertilisers. Although we advocate that academia is well-positioned to undertake this research, it does not need to do so alone. This shift towards applied research is also well-suited for industry collaboration or partnerships with regulatory agencies, where both parties can benefit from shared knowledge and resources to establish effective solutions.</p>\n<p>We can look to the commercial rhizobia inoculant industry as an exemplar of how well bioinoculants can be researched and applied. Symbiotic nitrogen fixation in legume roots by rhizobia bacteria shares many of the same principles and promises for sustainable agriculture as do AMF. Yet, in contrast to the commercial AMF inoculant industry, the rhizobia inoculant industry is well regulated, and has thus benefited from rigorous quality control frameworks and science-based research and development programs to improve bacterial strains and methods for field-based application (Bullard <i>et al</i>., <span>2005</span>). As a result, commercial rhizobia products reliably nodulate host crop roots and confer significant benefits to crop yield and nutrition, while also increasing soil mineral N which can reduce the need for N fertiliser application.</p>\n<p>As researchers of AMF, there is currently a window of opportunity for us to capitalise on the momentum of the recent studies of Lutz <i>et al</i>. (<span>2023</span>), Koziol <i>et al</i>. (<span>2024b</span>), and others. With increasing pressure from research institutions on their researchers to collaborate with, and solicit funding from, industry partners, we are well poised to prioritise practical research that supports global, systematic improvements in the AMF inoculant industry, towards the ultimate goal of furthering sustainable agricultural practice. To do this successfully will involve establishing ethical and transparent collaborations with the bioinoculant industry, and the willingness of the industry to work towards the common goal of releasing reliable AMF inoculum products. The potential environmental and societal impacts of leading the AMF inoculant industry in the right direction will be substantial and will benefit researchers, industry and growers alike.</p>","PeriodicalId":214,"journal":{"name":"New Phytologist","volume":"1 1","pages":""},"PeriodicalIF":8.3000,"publicationDate":"2024-12-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"New Phytologist","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1111/nph.20363","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
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Abstract

Arbuscular mycorrhizal fungi (AMF) have been recognised for decades as critical contributors to sustainable agriculture. By forming symbiotic relationships with plant roots, AMF can enhance nutrient uptake, improve abiotic and biotic stress tolerance, and generally promote soil health (Fitter et al., 2011). Since the 1980s, their potential has been explored extensively, with researchers advocating the management of mycorrhizal communities through applications such as biofertilisers. This is of particular interest in areas where natural AMF communities are absent, or their function is limited. The promise held by managing AMF for enhancing crop yield and nutrition was largely developed through countless research articles advocating their potential benefits. However, despite this extensive research, their real-world application has consistently fallen short, especially with commercially available inoculants. In an article recently published in New Phytologist, Koziol et al. (2024b, doi: 10.1111/nph.20278) provide a comprehensive evaluation of commercial AMF inoculants over the last 20 years through meta-analysis. The findings present a clear conclusion that commercially produced AMF inoculants have not delivered on the long-standing promise of improving sustainable agriculture. Significant quality issues were found, suggesting a disconnect between the expectations formed through laboratory studies and the outcomes realised by commercial products.

‘To truly harness the potential of AMF biofertilisers in sustainable agriculture, we must bridge the gap between conceptual AMF studies and practical applications.’

Overall, the findings of Koziol et al. (2024b) are sobering, highlighting fundamental quality issues with commercial AMF inoculants. At the most basic level, these products are often ineffective from the onset due to insufficient numbers of viable propagules by the time they reach consumers. This lack of viability means that many inoculants fail to establish any symbiotic arbuscular mycorrhizal relationship through the colonisation of plant roots, which is critical for the realisation of the expected benefits. Koziol et al. (2024b) found that the application of 84% of commercial inoculants resulted in insufficient (< 5%) mycorrhizal root colonisation. Ten observations resulted in the complete opposite of the desired effect of the product — crop mortality following application. Despite decades of AMF biofertiliser being marketed, these basic shortcomings have persisted, pointing to a systemic failure in their production, quality assurance and retail. This also points to the absence of clear quality assurance guidelines and frameworks, which is contributing to the persistence of these issues (Salomon et al., 2022). However, it is not impossible to produce effective inoculants. Koziol et al. (2024b) also highlighted that most laboratory-produced inoculants have demonstrated successful mycorrhizal root colonisation, as have a small number of commercial products. This highlights that it is indeed possible to produce commercial AMF biofertilisers that align closer with expectations.

The implications of these findings are substantial and extend beyond the academic world to various other considerations around agriculture and sustainability. The end-user of AMF biofertilisers are often left with products that do not fulfil their promises, resulting in economic losses and unrealised environmental benefits. Koziol et al. (2024b) estimated that if 88% of commercial AMF products are either unable to colonise roots, or are ineffective at promoting crop yields, then $876 million USD is wasted globally by primary producers. The ongoing presence of ineffective products in the market undermines trust in this biotechnological tool, making it harder for genuine products to be identified and accepted. These failures not only affect agricultural practices but also risk tarnishing the reputation of mycorrhizal research itself. As a result, we have seen missed opportunities for progress over several decades.

A ‘chicken and egg’ dilemma remains over who is responsible for advancing applied AMF research, where both academia and industry could deflect responsibility onto the other. Advocating from an academic standpoint, one could argue that meaningful progress requires proactive efforts, and academia is well-positioned to initiate these changes. This means that the science behind AMF biofertilisers could be advanced to a point where producers can no longer justify the persistent shortcomings of ineffective products due to a lack of knowledge.

Achieving this goal demands a shift in scientific focus. For decades, countless conceptual studies have explored the effects of AMF on plant and soil systems, often concluding that soils should be managed to boost natural AMF communities or that inoculation with AMF species could enhance crop outcomes. However, significant knowledge gaps hinder our ability to realise these suggestions. To truly harness the potential of AMF biofertilisers in sustainable agriculture, we must bridge the gap between conceptual AMF studies and practical applications. The scientific community must move beyond merely advocating for AMF use, and instead address the practical challenges that limit their effectiveness in real-world settings. A few newer studies, such as Lutz et al. (2023), have worked in this direction by predicting AMF establishment after the inoculation of a broad range of agricultural soils. This is just one area of research that seems long overdue and should have been prioritised decades ago. Many other scientific foundations for AMF biofertilisers remain underdeveloped, still relying heavily on preliminary and decades-old research.

Based on the current state of the AMF biofertiliser industry, several very basic research directives are urgently needed (Fig. 1 for summary). One of the biggest shortcomings highlighted by Koziol et al. (2024b) is the lack of viability during storage. Research should examine how different production methods, storage conditions, and carrier materials impact propagule viability. Also, understanding the inoculation potential of spores, compared to infected root pieces and hyphal fragments, is critical for improving AMF biofertiliser quality. Another key aspect is determining the optimal spore density required per plant or per square meter to ensure effective root colonisation and plant growth promotion. This should be combined with spore viability testing to identify reliable methods, such as water agar germination or spore metabolic staining, that can help predict successful colonisation. Additionally, evaluating whether AMF can persist over multiple growing seasons and how factors such as soil management practices (especially fallow periods, fungicide application), crop rotations (that may include nonhost crops such as canola) and climate (rainfall, temperature) impact AMF persistence and overall functionality. It is also essential to consider the risks associated with AMF biofertilisers, such as the potential displacement of native AMF communities and the unintended introduction of pathogens (Schwartz et al., 2006; Koziol et al., 2024a). This necessitates conducting genetic analyses of inoculated agricultural soils as well as the commercial AMF inoculum to assess their compatibility, potential risks, and ensure biosecurity. Such research directives will help predict and model AMF establishment, providing a foundational framework that can be integrated with further studies, for example, improving functional traits of the mycorrhizal community.

Abstract Image
Fig. 1
Open in figure viewerPowerPoint
Proposed research directives aimed at advancing arbuscular mycorrhizal fungi (AMF) biofertiliser development. Key areas of focus include researching the infectious potential of various AMF propagules (spores, root pieces, hyphae), the risks associated with biofertiliser application, the persistence of AMF in the field post-inoculation, the viability of propagules following storage, and the determination of application rates necessary to achieve effective root colonisation.

What might initially seem like trivial research tasks are complicated by the various environmental factors that significantly influence AMF behaviour. This means that research must be conducted across diverse AMF species and environmental or production systems to build a robust body of knowledge. This is similar to what has been done in other areas of AMF research, such as its impact on plant nutrition. Although debates remain regarding concepts like the previously termed ‘mutualism–parasitism continuum’ (Bennett & Groten, 2022), the research community has largely reached a consensus on the common modes of AMF action when it comes to plant nutrition. The aim should be to achieve a similar strong knowledge base for research areas more closely related to AMF biofertilisers. Although we advocate that academia is well-positioned to undertake this research, it does not need to do so alone. This shift towards applied research is also well-suited for industry collaboration or partnerships with regulatory agencies, where both parties can benefit from shared knowledge and resources to establish effective solutions.

We can look to the commercial rhizobia inoculant industry as an exemplar of how well bioinoculants can be researched and applied. Symbiotic nitrogen fixation in legume roots by rhizobia bacteria shares many of the same principles and promises for sustainable agriculture as do AMF. Yet, in contrast to the commercial AMF inoculant industry, the rhizobia inoculant industry is well regulated, and has thus benefited from rigorous quality control frameworks and science-based research and development programs to improve bacterial strains and methods for field-based application (Bullard et al., 2005). As a result, commercial rhizobia products reliably nodulate host crop roots and confer significant benefits to crop yield and nutrition, while also increasing soil mineral N which can reduce the need for N fertiliser application.

As researchers of AMF, there is currently a window of opportunity for us to capitalise on the momentum of the recent studies of Lutz et al. (2023), Koziol et al. (2024b), and others. With increasing pressure from research institutions on their researchers to collaborate with, and solicit funding from, industry partners, we are well poised to prioritise practical research that supports global, systematic improvements in the AMF inoculant industry, towards the ultimate goal of furthering sustainable agricultural practice. To do this successfully will involve establishing ethical and transparent collaborations with the bioinoculant industry, and the willingness of the industry to work towards the common goal of releasing reliable AMF inoculum products. The potential environmental and societal impacts of leading the AMF inoculant industry in the right direction will be substantial and will benefit researchers, industry and growers alike.

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New Phytologist
New Phytologist 生物-植物科学
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期刊介绍: New Phytologist is an international electronic journal published 24 times a year. It is owned by the New Phytologist Foundation, a non-profit-making charitable organization dedicated to promoting plant science. The journal publishes excellent, novel, rigorous, and timely research and scholarship in plant science and its applications. The articles cover topics in five sections: Physiology & Development, Environment, Interaction, Evolution, and Transformative Plant Biotechnology. These sections encompass intracellular processes, global environmental change, and encourage cross-disciplinary approaches. The journal recognizes the use of techniques from molecular and cell biology, functional genomics, modeling, and system-based approaches in plant science. Abstracting and Indexing Information for New Phytologist includes Academic Search, AgBiotech News & Information, Agroforestry Abstracts, Biochemistry & Biophysics Citation Index, Botanical Pesticides, CAB Abstracts®, Environment Index, Global Health, and Plant Breeding Abstracts, and others.
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