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Molecular Microbiology Research 2024, Vol.14 http://microbescipublisher.com/index.php/mmr © 2024 MicroSci Publisher, an online publishing platform of Sophia Publishing Group. All Rights Reserved. Sophia Publishing Group (SPG), founded in British Columbia of Canada, is a multilingual publisher. Publisher MicroSci Publisher Editedby Editorial Team of Molecular Microbiology Research Email: edit@mmr.microbescipublisher.com Website: http://microbescipublisher.com/index.php/mmr Address: 11388 Stevenston Hwy, PO Box 96016, Richmond, V7A 5J5, British Columbia Canada Molecular Microbiology Research (ISSN 1927-5595) is an open access, peer reviewed journal published online by MicroSci Publisher. The journal publishes all the latest and outstanding research articles, letters and reviews in all areas of molecular microbiology, including original articles, reviews and brief reports in microbiology, bacteriology, mycology, molecular and cellular biology and virology at the level of gene expression and regulation, genetic transfer, cell biology and subcellular organization, pathogenicity and virulence, physiology and metabolism, cell-cell communication and signalling pathways as well as the interactions between the various cell systems of microorganisms including the interrelationship of DNA, RNA and protein biosynthesis. All the articles published in Molecular Pathogens are Open Access, and are distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. MicroSci Publisher uses CrossCheck service to identify academic plagiarism through the world’s leading plagiarism prevention tool, iParadigms, and to protect the original authors’ copyrights. MicroSci Publisher is an international Open Access publisher specializing in microbiology, bacteriology, mycology, molecular and cellular biology and virology registered at the publishing platform that is operated by Sophia Publishing Group (SPG), founded in British Columbia of Canada.
Molecular Microbiology Research (online), 2024, Vol. 14 ISSN 1927-5595 http://microbescipublisher.com/index.php/mmr © 2024 MicroSci Publisher, an online publishing platform of Sophia Publishing Group. All Rights Reserved. Sophia Publishing Group (SPG), founded in British Columbia of Canada, is a multilingual publisher. Latest Content 2024, Vol.14, No.4 【Review Article】 Fungal and Bacterial Diseases in Rye: Historical Contexts and Modern Solutions 162-170 Qiuxia Sun, Guoliang Wang DOI: 10.5376/mmr.2024.14.0018 【Research Perspective】 Microbial Symbionts: Molecular Codes and Ecological Significance of Tree-Rhizosphere Microbe Interactions 171-180 Shusheng Liu, Fumin Gao DOI: 10.5376/mmr.2024.14.0019 Alternaria Leaf Spot in Cotton: Identification and Control 181-187 Jiefu Lin, Yuexin Zhu DOI: 10.5376/mmr.2024.14.0020 【Research Insight】 A Systematic Analysis of Legume-Rhizobium Symbiosis: From Soil Microbiology to Agricultural Implications 188-197 Tianxia Guo, Jing Fu DOI: 10.5376/mmr.2024.14.0021 【Feature Review】 Roles of Marine Microorganisms in the Carbon, Nitrogen, and Sulfur Cycles 198-207 Bing Wang, Hongwei Liu DOI: 10.5376/mmr.2024.14.0022
Molecular Microbiology Research 2024, Vol.14, No.4, 162-170 http://microbescipublisher.com/index.php/mmr 162 Review Article Open Access Fungal and Bacterial Diseases in Rye: Historical Contexts and Modern Solutions Qiuxia Sun , Guoliang Wang Modern Agricultural Research Center of Cuixi Academy of Biotechology, Zhuji, 311800, Zhejiang, China Corresponding author: qiuxia.sun@cuixi.org Molecular Microbiology Research, 2024, Vol.14, No.4 doi: 10.5376/mmr.2024.14.0018 Received: 08 May, 2024 Accepted: 24 Jun., 2024 Published: 10 Jul., 2024 Copyright © 2024 Sun and Wang, This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Preferred citation for this article: Sun Q.X., and Wang G.L., 2024, Fungal and bacterial diseases in rye: historical contexts and modern solutions, Molecular Microbiology Research, 14(4): 162-170 (doi: 10.5376/mmr.2024.14.0018) Abstract Rye (Secale cereale L.), as an important cereal crop, has historically suffered from severe fungal and bacterial diseases. This study explores the historical context, modern management methods, and future directions for controlling these diseases. By examining major fungal diseases such as ergot, rusts, and smuts, as well as bacterial diseases like bacterial blight and black chaff, it reviews the impact of disease outbreaks on rye production and the evolution of disease resistance. Modern disease management strategies include the use of fungicides and antibiotics, the introduction of biological control agents, breeding for disease resistance, and integrated disease management practices. With the challenges posed by climate change, the control of rye diseases has become increasingly complex. This study integrates historical successes and modern technologies, emphasizing the importance of crop rotation, cultural practices, and biotechnology in future disease management to enhance rye’s disease resistance, ensure food security, and promote the sustainable development of agricultural ecosystems. Keywords Rye cultivation; Fungal diseases; Bacterial diseases; Disease resistance; Integrated disease management 1 Introduction Rye (Secale cereale L.) is a versatile cereal crop known for its resilience to harsh environmental conditions and its ability to thrive in poor soils where other cereals might fail. It is widely cultivated in temperate regions and is used for a variety of purposes, including food production, animal feed, and as a cover crop to improve soil health and prevent erosion (Frost et al., 2019). Despite its hardiness, rye is susceptible to several fungal and bacterial diseases that can significantly impact yield and quality. Historically, fungal diseases have posed a significant threat to rye cultivation. One of the most notorious diseases is ergot, caused by Claviceps purpurea, which has been a problem since the early Middle Ages in Europe. Ergot contamination not only reduces yield but also produces toxic alkaloids that can cause severe health issues in humans and animals (Miedaner and Geiger, 2015; Pitt and Miller, 2017). Another major disease is snow mold, caused by Microdochium nivale, which thrives under snow cover and can devastate winter rye crops (Gorshkov et al., 2020; Ponomareva et al., 2022). The historical context of these diseases highlights the ongoing challenge of managing fungal pathogens in rye cultivation. This study will provide a comprehensive overview of the fungal and bacterial diseases that affect rye, with a focus on their historical impact and the modern solutions being developed, including studying the biology and genetics of major pathogens, the effectiveness of current disease management strategies, and the potential for cultivating disease resistant rye varieties. It will explore the challenges and solutions currently available to address their impacts, with the aim of providing insights for future rye cultivation and conservation strategies. 2 Historical Context of Fungal and Bacterial Diseases in Rye 2.1 Major outbreaks and their consequences Rye (Secale cereale L.) has historically been susceptible to a variety of fungal and bacterial diseases, which have had significant impacts on crop yields and food security. One of the most notable fungal pathogens affecting rye is Microdochium nivale, which causes severe damage and has been poorly characterized at the molecular level until
Molecular Microbiology Research 2024, Vol.14, No.4, 162-170 http://microbescipublisher.com/index.php/mmr 163 recent studies (Tsers et al., 2021). The susceptibility of rye to this pathogen has led to substantial crop losses, highlighting the need for improved disease resistance. Another significant fungal disease in rye is powdery mildew, caused by Blumeria graminis f. sp. tritici. The introgression of resistance genes from rye into wheat, such as the Pm17 gene, has been a common strategy to combat this disease. However, the effectiveness of these resistance genes can be limited by the ancient variation of the corresponding fungal effector genes, which predate the introgression and can lead to rapid resistance breakdown. The historical context of rye diseases also includes the impact of climate change, which has been shown to exacerbate the emergence and spread of fungal pathogens. Environmental pressures resulting from climate change can lead to the adaptation of fungi to new conditions, increasing their pathogenicity and geographic range (Nnadi and Carter, 2021). This has been observed with various fungal species, which have become more problematic in recent decades due to changing climate conditions. 2.2 Evolution of disease resistance in rye The evolution of disease resistance in rye has been a critical area of research, particularly in the context of breeding programs aimed at enhancing phytoimmunity. Studies have identified several rye genotypes with non-specific resistance to multiple fungal diseases. For instance, research conducted on winter rye genotypes has revealed varieties with slow rusting traits and high resistance to septoria and other fungal infections (Shchekleina and Sheshegova, 2023). These resistant varieties, such as 'Rossiyanka 2', have been crucial in breeding programs to develop new rye cultivars with improved disease resistance. The identification and characterization of resistance genes have also played a significant role in the evolution of disease resistance in rye. The Pm17 and Pm8 resistance genes, originally introgressed from rye into wheat, demonstrate the ancient diversity and evolutionary divergence of resistance genes in cereal crops (Singh et al., 2018). These genes have been isolated and functionally validated, providing valuable insights into the genetic basis of disease resistance and guiding future breeding efforts. The development of novel translocation lines, such as the wheat-rye 1RS·1BL translocation lines, has contributed to the enhancement of disease resistance in rye. These lines exhibit high resistance to stripe rust and other fungal pathogens, offering new genetic resources for wheat and rye improvement programs (Ren et al., 2022). 3 Fungal Diseases Affecting Rye 3.1 Ergot disease Ergot disease, caused by fungi in the genus Claviceps, is a significant concern for rye cultivation. The most notable species, Claviceps purpurea, infects the ovaries of rye flowers, replacing seeds with toxic sclerotia. This disease has been documented in Europe since the early Middle Ages and poses severe health risks due to the alkaloids produced by the fungus, which can affect both humans and animals. In Canada, ergot is a grain-grading factor, impacting grain quality and safety due to the presence of ergot alkaloids (Walkowiak et al., 2022). Breeding efforts have identified several winter rye cultivars with moderate resistance to ergot, which can be utilized to develop more resistant varieties. 3.2 Rusts and smuts Rusts and smuts are other significant fungal diseases affecting rye. Rust diseases, such as stripe rust caused by Puccinia striiformis, have historically been a major threat to cereal crops. Although primarily a concern for wheat, rust fungi can also affect rye. The management of rust diseases often involves the use of fungicides and the development of resistant cultivars (Cook et al., 2021). Smut diseases, caused by fungi like Ustilago species, can also impact rye, leading to significant yield losses. 3.3 Modern fungal disease management 3.3.1 Fungicide application strategies Fungicide application remains a critical component of managing fungal diseases in rye. However, the efficacy of fungicides can be limited and weather-dependent, particularly for diseases like ergot (Miedaner and Geiger, 2015).
Molecular Microbiology Research 2024, Vol.14, No.4, 162-170 http://microbescipublisher.com/index.php/mmr 164 Soil-applied fungicides have shown promise in reducing sclerotia germination and disrupting the ergot disease cycle in perennial ryegrass, suggesting potential applications for rye as well (Dung et al., 2018). The emergence of fungicide-resistant strains of rust pathogens highlights the need for careful management and monitoring of fungicide use. 3.3.2 Breeding for fungal resistance Breeding for resistance is a sustainable approach to managing fungal diseases in rye. Research has identified several rye cultivars with moderate resistance to ergot, which can be used in breeding programs to develop more resistant varieties. Advances in molecular breeding techniques, such as the use of transcriptomics to understand the genetic basis of resistance, are paving the way for the development of rye cultivars with enhanced resistance to ergot and other fungal diseases (Mahmood et al., 2020). The identification of specific resistance genes, such as those conferring stripe rust resistance, further supports these efforts (Ashraf et al., 2022). 3.3.3 Integrated disease management Integrated Disease Management (IDM) combines multiple strategies to control fungal diseases in rye. This approach includes the use of resistant cultivars, timely fungicide applications, and cultural practices that reduce disease pressure. For example, the use of gametocides to induce male sterility in rye can enhance the effectiveness of ergot management by preventing pollen contamination and increasing the susceptibility of unfertilized ovaries to fungal infection (Hanosová et al., 2015). IDM practices are essential for sustainable disease management and reducing the reliance on chemical controls alone (Carmona et al., 2020). 4 Bacterial Diseases in Rye 4.1 Bacterial blight Bacterial blight in rye is primarily caused by the pathogen Xanthomonas campestris pv. translucens. This disease manifests as water-soaked lesions on leaves, which eventually turn necrotic, leading to significant yield losses. The pathogen is known for its rapid spread under favorable conditions, such as high humidity and warm temperatures. Similar to rice, where bacterial blight caused by Xanthomonas oryzae pv. oryzae is a major concern, extensive genetic and genomic studies have been conducted to understand the molecular mechanisms of plant-pathogen interactions and to develop resistant varieties (Jiang et al., 2020). 4.2 Black chaff Black chaff, caused by Xanthomonas translucens pv. undulosa, is another significant bacterial disease affecting rye. This disease is characterized by dark streaks on the glumes and leaves, often accompanied by a bacterial ooze. The symptoms can be confused with those of fungal diseases, making accurate diagnosis crucial for effective management. The disease can lead to reduced grain quality and yield. Research on similar bacterial diseases in other cereals, such as rice and wheat, has provided insights into potential control strategies, including the use of resistant varieties and biological control agents (Rojas et al., 2020; Byrne et al., 2022). 4.3 Advances in bacterial disease control 4.3.1 Use of antibiotics and biological control agents The use of antibiotics, such as streptomycin, has been a traditional method for controlling bacterial diseases in crops. However, the emergence of antibiotic-resistant strains and the environmental impact of antibiotics have led to a shift towards more sustainable solutions. Biological control agents, such as endophytic bacteria and fungi, have shown promise in managing bacterial diseases. For instance, Bacillus oryzicola, an endophytic bacterium isolated from rice roots, has demonstrated antimicrobial and systemic resistance-inducing activities, effectively suppressing bacterial blight in rice (Chung et al., 2015). Similarly, the application of beneficial microorganisms could be explored for controlling bacterial diseases in rye. 4.3.2 Development of resistant varieties Breeding for disease-resistant varieties is a cornerstone of integrated pest management. Advances in molecular biology and genomics have facilitated the identification and incorporation of resistance genes into crop varieties.
Molecular Microbiology Research 2024, Vol.14, No.4, 162-170 http://microbescipublisher.com/index.php/mmr 165 In rice, extensive research has led to the characterization of resistance (R) genes and their interactions with bacterial blight pathogens, enabling the development of varieties with durable and broad-spectrum resistance (Figure 1) (Jiang et al., 2020). During the infection process of bacterial blight, effector proteins secreted by the pathogen, such as RaxX, bind to the XA21 receptor located on the plasma membrane of rice cells, activating downstream defense responses. This process involves several regulatory proteins, such as OsSERK2, XB24, XB15, and XB21, which play key roles in maintaining XA21 function and regulating its phosphorylation state. This complex protein network effectively enhances rice’s defense against pathogens. Similar approaches can be applied to rye, leveraging genomic tools to identify and introduce resistance genes against bacterial blight and black chaff. The development of resistant varieties not only reduces the reliance on chemical controls but also ensures sustainable crop production. Figure 1 Xa21-mediated immune signaling pathways triggered byXanthomonas oryzae (Adopted from Jiang et al., 2020) 5 Integrated Disease Management Strategies 5.1 Crop rotation and cultural practices Crop rotation and cultural practices are fundamental components of integrated disease management (IDM) strategies. These practices help in breaking the life cycles of pathogens and reducing the inoculum levels in the soil. For instance, cover cropping with species like sunn hemp has been shown to suppress soilborne nematodes and fungal pathogens, such as Meloidogyne incognita, Rhizoctonia solani, and Sclerotinia sclerotiorum, especially when combined with deep tillage practices (Marquez and Hajihassani, 2023). However, the use of winter cereal cover crops, such as rye, can sometimes host pathogens that affect subsequent crops like corn, necessitating careful management to mitigate these risks (Bakker et al., 2016). The adoption of perennial grain crops, while beneficial for sustainable agriculture, introduces new disease management challenges that require innovative solutions (Fulcher et al., 2022). 5.2 Use of resistant varieties and biotechnology The development and use of disease-resistant crop varieties are crucial for managing both fungal and bacterial diseases in rye. Research has identified several winter rye varieties with non-specific resistance to multiple fungal diseases, which can be used in breeding programs to enhance phytoimmunity (Shchekleina and Sheshegova, 2023). For example, varieties like 'Rossiyanka 2' have shown high resistance to septoriose and slow rusting traits, making them valuable for breeding efforts. Furthermore, advances in biotechnology, such as genome modification,
Molecular Microbiology Research 2024, Vol.14, No.4, 162-170 http://microbescipublisher.com/index.php/mmr 166 offer promising avenues for developing crops with enhanced disease resistance. This approach is considered one of the most effective strategies against bacterial diseases, although more research is needed to develop novel management tactics (Sharma et al., 2022). 5.3 Future directions in disease management Future directions in disease management will likely focus on sustainable and environmentally friendly solutions. The increasing concern over the impact of fungicides and bactericides on human health and the environment underscores the need for alternative strategies. For instance, the use of antibiofilm compounds at sub-lethal concentrations offers a potential eco-sustainable strategy to counteract fungal pathogens, reducing the severity of diseases and the selection of resistant forms (Villa et al., 2017). Integrated pest management (IPM) techniques, such as forecasting disease pressure and optimizing fungicide use based on disease resistance and environmental conditions, can help minimize the reliance on chemical treatments while maintaining crop yields (Stetkiewicz et al., 2019). Research must continue to address the challenges posed by emerging pathogens and develop durable, accessible, and sustainable disease management practices (Fones et al., 2020). 6 Challenges in Managing Rye Diseases 6.1 Climate change and disease dynamics Climate change significantly impacts the dynamics of fungal and bacterial diseases in rye. The increasing global temperatures and changing precipitation patterns create favorable conditions for the emergence and spread of new pathogens. For instance, climate change can extend the geographic range of pathogenic species or their vectors, leading to the emergence of diseases in areas where they were previously unknown (Nnadi and Carter, 2021). Environmental disruptions such as floods and storms can disperse fungal spores, increasing the incidence of infections. Emerging fungal pathogens pose a significant risk to global food security, as they can infect staple crops and economically important commodities. The current agricultural systems, which emphasize intensive monoculture practices, further exacerbate the spread of these pathogens (Fones et al., 2020). The adaptation of fungi to higher temperatures due to climate change could lead to an increase in thermotolerant species capable of infecting rye and other crops. Therefore, understanding the role of climate change in disease dynamics is crucial for developing effective management strategies. 6.2 Resistance development and breakdown The development and breakdown of resistance in rye is a complex challenge in disease management. Resistance genes, such as those introgressed from rye to wheat, can be rapidly overcome by pathogens due to the presence of ancient variants of effector proteins in the pathogen gene pool (Müller et al., 2022). This rapid breakdown of resistance highlights the need for continuous monitoring and the development of new resistance genes. Breeding for resistance to specific diseases, such as snow mold, has shown promise. However, the limited use of resistance sources in contemporary breeding programs has resulted in a scarcity of varieties with moderate to high resistance (Figure 2) (Ponomareva et al., 2022). Identifying and utilizing diverse genetic sources of resistance is essential for enhancing the durability of resistance in rye. The evolutionary divergence of resistance genes, such as Pm17 and Pm8, demonstrates the complexity of resistance mechanisms. These genes, originally introgressed from rye to wheat, show significant diversity, suggesting that orthologous resistance genes can evolve differently in various cereal species (Singh et al., 2018). This diversity can be leveraged to develop novel resistance genes for rye breeding programs. The experiment in the image is a systematic evaluation of the resistance to snow mold in different rye varieties, aimed at identifying the optimal genetic sources of resistance. By incorporating these high-quality disease-resistant genes into new breeding programs, the resistance of rye to snow mold can be significantly
Molecular Microbiology Research 2024, Vol.14, No.4, 162-170 http://microbescipublisher.com/index.php/mmr 167 improved. This strategy of enhancing crop disease resistance through genetic diversity is expected to provide more disease-resistant crop varieties for future agriculture, reduce the reliance on chemical pesticides, and simultaneously increase crop yields and food safety. Figure 2 Rye plots in the nurseries with a natural infection background (NIB) (A) and with an artificially-enriched infection background (AIB) (B) (Photo credit : Ponomareva et al., 2022) 7 Case Studies of Successful Disease Management 7.1 Historical successes in disease control Historically, the management of fungal and bacterial diseases in rye and other crops has seen significant advancements. One notable success is the development and application of fungicide treatments. For instance, the use of fungicides such as metalaxyl, pyraclostrobin, fludioxonil, ipconazole, and sedaxane has been instrumental in controlling diseases caused by Pythium, Fusarium, and Rhizoctonia solani. These treatments have been shown to improve seed germination and seedling growth under controlled conditions, highlighting their effectiveness in disease management (Acharya et al., 2018). Another historical success is the understanding and management of central nervous system infections caused by bacterial and fungal pathogens. The progression of diseases such as cryptococcal meningitis and candidiasis has been well-documented, leading to improved diagnostic and treatment protocols. This historical perspective has provided a foundation for modern disease management strategies (Shih and Koeller, 2015). 7.2 Modern case studies from different regions In recent years, modern approaches to disease management in rye have continued to evolve, incorporating both traditional methods and innovative solutions. For example, the use of fungicide seed treatments in corn, which is often rotated with rye, has shown promising results. Studies have demonstrated that treatments targeting Pythium spp. significantly reduce disease incidence and improve seedling health, even in challenging environmental conditions (Acharya et al., 2018). Global initiatives such as the Leading International Fungal Education (LIFE) portal have facilitated the estimation and management of fungal infection burdens across different regions. This initiative has highlighted the varying prevalence of fungal diseases and the need for region-specific management strategies. By providing accurate data on the burden of serious fungal infections, the LIFE portal has enabled targeted interventions and improved disease outcomes (Bongomin et al., 2017). These modern case studies underscore the importance of both historical knowledge and contemporary research in effectively managing fungal and bacterial diseases in rye and other crops. By combining these approaches, researchers and farmers can develop robust strategies to mitigate the impact of these diseases on agricultural productivity.
Molecular Microbiology Research 2024, Vol.14, No.4, 162-170 http://microbescipublisher.com/index.php/mmr 168 8 Concluding Remarks Historically, fungal and bacterial diseases in rye have posed significant challenges to agriculture, with ergot (Claviceps spp.) being one of the most notorious. Ergot has been a known issue since the early Middle Ages, causing severe health problems due to the toxic alkaloids produced by the fungus. Traditional methods to combat these diseases included crop rotation, selection of resistant varieties, and manual removal of infected plants. However, these methods were often labor-intensive and not entirely effective. In modern times, the approach to managing rye diseases has evolved significantly. Advances in genetic research have led to the identification of resistant genotypes and the development of hybrid varieties with improved resistance to diseases like ergot and rust. Molecular breeding techniques, such as the introgression of effective restorer genes, have shown promise in reducing ergot infection levels. Additionally, fungicide treatments, although limited in efficacy and dependent on weather conditions, have been employed to manage fungal infections. The use of genome-wide association studies (GWAS) has furthered our understanding of the genetic basis of disease resistance. For instance, research on Fusarium culmorum has identified key SNPs associated with aggressiveness and mycotoxin production, providing valuable insights for resistance breeding. Moreover, the discovery of natural products with antimicrobial properties has opened new avenues for developing biocontrol agents. The future of rye disease management lies in the integration of advanced genetic tools and sustainable agricultural practices. Continued research into the genetic diversity of rye and its pathogens will be crucial. For example, the identification of novel resistance genes, such as Pm17 and Pm8, and their evolutionary divergence offers potential for developing new resistant varieties. Additionally, the use of resistant germplasm and the selection of distinct donors for breeding programs will enhance the genetic variability and durability of disease resistance in rye. Biotechnological advancements, such as CRISPR/Cas9, could be leveraged to introduce specific resistance traits into rye cultivars more efficiently. Furthermore, the development of environmentally friendly fungicides and biocontrol agents will play a significant role in sustainable disease management. The integration of these modern approaches with traditional practices, such as crop rotation and proper field management, will provide a holistic strategy to combat fungal and bacterial diseases in rye. Acknowledgments We express our sincere gratitude to two reviewers for their suggestions. Conflict of Interest Disclosure The authors affirm that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest. References Acharya J., Bakker M., Moorman T., Kaspar T., Lenssen A., and Robertson A., 2018, Effects of fungicide seed treatments and a winter cereal rye cover crop in no till on the seedling disease complex in corn, Canadian Journal of Plant Pathology, 40: 481-497. https://doi.org/10.1080/07060661.2018.1506503 Ashraf R., Johansson E., Vallenback P., Steffenson B., Bajgain P., and Rahmatov M., 2022, Identification of a small translocation from 6R possessing stripe rust resistance to wheat, Plant Disease, 107(3): 720-729. https://doi.org/10.1094/PDIS-07-22-1666-RE Bakker M., Acharya J., Moorman T., Robertson A., and Kaspar T., 2016, The potential for cereal rye cover crops to host corn seedling pathogens, Phytopathology, 106(6): 591-601. https://doi.org/10.1094/PHYTO-09-15-0214-R Bongomin F., Gago S., Oladele R., and Denning D., 2017, Global and multi-national prevalence of fungal diseases—estimate precision, Journal of Fungi, 3(4): 57. https://doi.org/10.3390/jof3040057 Byrne M., Thapa G., Doohan F., and Burke J., 2022, Lactic acid bacteria as potential biocontrol agents for fusarium head blight disease of spring barley, Frontiers in Microbiology, 13: 912632. https://doi.org/10.3389/fmicb.2022.912632
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Molecular Microbiology Research 2024, Vol.14, No.4, 171-180 http://microbescipublisher.com/index.php/mmr 171 Research Perspective Open Access Microbial Symbionts: Molecular Codes and Ecological Significance of Tree-Rhizosphere Microbe Interactions Shusheng Liu, Fumin Gao Tropical Microbial Resources Research Center, Hainan Institute of Tropical Agricultural Resources, Sanya, 572025, Hainan, China Corresponding author: fumin.gao@hitar.org Molecular Microbiology Research, 2024, Vol.14, No.4 doi: 10.5376/mmr.2024.14.0019 Received: 20 May, 2024 Accepted: 05 Jul., 2024 Published: 22 Jul., 2024 Copyright © 2024 Liu and Gao, This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Preferred citation for this article: Liu S.S., and Gao F.M., 2024, Microbial symbionts: molecular codes and ecological significance of tree-rhizosphere microbe interactions, Molecular Microbiology Research, 14(4): 171-180 (doi: 10.5376/mmr.2024.14.0019) Abstract The rhizosphere is a critical interface between plant roots and soil, where symbiotic relationships between trees and microbes thrive. This study explores the diversity of microbial symbionts in the rhizosphere, including mycorrhizal fungi, nitrogen-fixing bacteria, and plant growth-promoting rhizobacteria (PGPR), and their interactions with trees. It provides an in-depth analysis of the molecular mechanisms underlying these interactions, with a focus on signal exchange, symbiosis formation pathways, and the genetic basis of symbiotic compatibility. These symbionts play crucial roles in ecosystems, from nutrient acquisition and recycling to enhancing tree resilience to environmental stress and promoting soil health. Case studies highlight the importance of these relationships in forest ecosystems, agroforestry, and extreme environments. This study underscores the importance of integrating multidisciplinary approaches in future research to fully harness the potential of symbiotic microbes for sustainable ecosystem management. Keywords Rhizosphere; Symbiotic microbes; Mycorrhizal fungi; Nutrient acquisition; Molecular mechanisms 1 Introduction The rhizosphere, the narrow region of soil influenced by root secretions and associated soil microorganisms, is a hotspot for microbial activity and interactions. This zone is critical for plant growth and productivity due to the complex microbial communities it harbors, including bacteria, fungi, and archaea. These microorganisms form symbiotic relationships with plant roots, which can be mutualistic, commensal, or pathogenic. For instance, arbuscular mycorrhizal (AM) fungi and rhizobia bacteria are well-known symbionts that enhance nutrient uptake and nitrogen fixation, respectively (Tsiknia et al., 2020; Wang et al., 2020). The dynamic interactions within the rhizosphere are influenced by root exudates, which can shape the microbial community composition and function (Zhalnina et al., 2018). Understanding these interactions is essential for comprehending the ecological and evolutionary processes that govern plant health and soil fertility. Tree-microbe interactions in the rhizosphere are particularly significant due to their long-term impact on forest ecosystems and their role in carbon sequestration, nutrient cycling, and soil structure maintenance (Bulgarelli et al., 2015; Shi et al., 2016). Trees, with their extensive root systems, interact with a diverse array of microorganisms that can influence their growth, health, and resilience to environmental stresses. For example, the symbiotic relationships between trees and mycorrhizal fungi are crucial for nutrient acquisition and stress tolerance. The microbial communities associated with tree roots can act as a barrier against pathogens, enhancing the tree's immune responses (Li et al., 2021). By studying these interactions, researchers can develop strategies to improve forest management, enhance tree productivity, and mitigate the effects of climate change. This study will provide a comprehensive overview of the molecular mechanisms and ecological significance of tree-microbiome interactions, analyzing the diversity and functions of microbial communities in the tree rhizosphere. It will explore the molecular codes and signaling pathways involved in tree-microbiome symbiosis and discuss the ecological impacts of these interactions on forest ecosystems, as well as their potential
Molecular Microbiology Research 2024, Vol.14, No.4, 171-180 http://microbescipublisher.com/index.php/mmr 172 applications in sustainable forestry and agriculture. The study will also highlight recent advances in research methodologies, including omics technologies and bioinformatics tools, which have enhanced our understanding of these complex interactions. 2 Types of Microbial Symbionts in the Rhizosphere 2.1 Mycorrhizal fungi Mycorrhizal fungi form a symbiotic relationship with plant roots, facilitating nutrient exchange and enhancing plant growth. Arbuscular mycorrhizal (AM) fungi are particularly significant as they help in the uptake of phosphorus and other essential nutrients. These fungi penetrate the root cortical cells, forming arbuscules that increase the surface area for nutrient exchange. The symbiosis between AM fungi and plants is crucial for the assembly of root-associated microbial communities, which in turn promotes the accumulation of beneficial bacteria such as rhizobia in the rhizosphere. This interaction is vital for the overall health and productivity of plants, especially in nutrient-poor soils (Wang et al., 2020). 2.2 Nitrogen-fixing bacteria Nitrogen-fixing bacteria, such as rhizobia, play a critical role in converting atmospheric nitrogen into a form that plants can utilize. These bacteria form nodules on the roots of leguminous plants, where they fix nitrogen through a symbiotic relationship. The presence of AM fungi can enhance the colonization and effectiveness of rhizobia, leading to improved nitrogen fixation and plant growth. This tripartite interaction between plants, AM fungi, and nitrogen-fixing bacteria is essential for sustainable agriculture and ecological balance (Kour et al., 2019; Hakim et al., 2021). 2.3 Plant growth-promoting rhizobacteria (PGPR) Plant Growth-Promoting Rhizobacteria (PGPR) are a diverse group of bacteria that colonize the rhizosphere and enhance plant growth through various mechanisms (Kumar et al., 2022). PGPR can be classified into extracellular and intracellular types based on their location relative to the plant roots. They promote plant growth by producing phytohormones, solubilizing phosphorus, and producing siderophores that chelate iron. PGPR can induce systemic resistance in plants, making them more resilient to biotic and abiotic stresses. The use of PGPR in agriculture offers an eco-friendly alternative to chemical fertilizers and pesticides, contributing to sustainable agricultural practices. 3 Molecular Interactions Between Trees and Symbionts 3.1 Signal exchange and recognition 3.1.1 Root exudates as chemical signals Root exudates play a crucial role in the initial stages of tree-microbe interactions by acting as chemical signals that mediate communication between plant roots and soil microorganisms. These exudates, which include a variety of organic acids, sugars, amino acids, and secondary metabolites, are secreted by plant roots into the rhizosphere. They serve multiple functions, such as altering soil properties, inhibiting the growth of competing plants, and regulating microbial communities (Zhalnina et al., 2018; Handakumbura et al., 2021; Korenblum et al., 2022). For instance, plants like Avena barbata release specific aromatic organic acids that are preferentially consumed by rhizosphere bacteria, thereby shaping the microbial community composition. Root exudates can be modulated by biotic stress, leading to changes in the rhizospheric microbial community that enhance plant stress tolerance (Sharma et al., 2023). 3.1.2 Microbial receptor mechanisms Microorganisms in the rhizosphere possess specialized receptor mechanisms to detect and respond to the chemical signals emitted by plant roots. These receptors enable microbes to recognize specific compounds in root exudates, facilitating the establishment of symbiotic relationships. For example, rhizobia and arbuscular mycorrhizal (AM) fungi have evolved receptor systems that detect flavonoids and strigolactones, respectively, which are key signals
Molecular Microbiology Research 2024, Vol.14, No.4, 171-180 http://microbescipublisher.com/index.php/mmr 173 for initiating symbiosis (Rasmann and Turlings, 2016). The ability of microbes to sense and respond to these signals is critical for their colonization and interaction with plant roots, ultimately influencing plant growth and health. 3.1.3 Mutual recognition and binding processes The mutual recognition and binding processes between trees and their microbial symbionts involve a series of molecular interactions that ensure compatibility and successful symbiosis. These processes often begin with the recognition of root exudates by microbial receptors, followed by the activation of signaling pathways that lead to the expression of symbiosis-related genes. For instance, the establishment of AM symbiosis involves the activation of an ancestral signaling pathway in plants, which is also utilized for legume-rhizobia symbiosis (Figure 1) (Wang et al., 2020). This pathway facilitates the formation of specialized structures, such as arbuscules and nodules, where nutrient exchange occurs. The mutual recognition and binding are essential for the formation of a stable and functional symbiotic relationship. The study by Wang et al. (2020) demonstrated how arbuscular mycorrhizal (AM) symbiosis promotes the legume-rhizobium symbiosis by regulating the rhizosphere microbial community, and revealed the regulatory role of plant genotype in this symbiotic relationship. This process provides nutrients to the plants and enhances their growth and ecological functions. 3.2 Molecular pathways of symbiosis formation The formation of symbiotic relationships between trees and microbes involves complex molecular pathways that regulate the development and maintenance of these interactions. These pathways include the perception of microbial signals by plant receptors, the activation of downstream signaling cascades, and the expression of genes involved in symbiosis. For example, the establishment of AM symbiosis requires the activation of a common symbiosis signaling pathway, which involves the perception of fungal signals by plant receptors and the subsequent activation of calcium signaling and transcriptional responses. Similarly, the formation of legume-rhizobia symbiosis involves the recognition of rhizobial Nod factors by plant receptors, leading to the activation of signaling pathways that promote nodule formation and nitrogen fixation (Tsiknia et al., 2020; Wang et al., 2020). 3.3 Genetic basis of symbiotic compatibility The genetic basis of symbiotic compatibility between trees and their microbial symbionts is determined by the presence of specific genes that regulate the recognition, signaling, and development of symbiotic structures. These genes are often conserved across different plant species and are essential for the establishment of symbiosis. For instance, genes involved in the common symbiosis signaling pathway, such as those encoding receptor-like kinases and calcium-dependent protein kinases, are required for both AM and legume-rhizobia symbioses. Additionally, genetic variation in both plants and microbes can influence the efficiency and stability of symbiotic interactions, highlighting the importance of genetic compatibility for successful symbiosis (Lagunas et al., 2015). Understanding the genetic basis of symbiotic compatibility can inform strategies for improving plant-microbe interactions in agricultural and ecological contexts. 4 Ecological Functions of Symbiotic Microbes 4.1 Nutrient acquisition and recycling Symbiotic microbes play a crucial role in nutrient acquisition and recycling within the rhizosphere. Mycorrhizal fungi and nitrogen-fixing bacteria are particularly significant in this context. These microbes enhance plant mineral nutrition by converting unavailable nutrients into forms that plants can absorb. For instance, plant growth-promoting rhizobacteria (PGPR) convert essential nutrients like nitrogen, phosphorus, and zinc into available forms, thereby improving soil fertility and plant growth (Jacoby et al., 2017; Huang, 2024). The interaction between soil microbes and plants significantly affects soil microbial structure and function, which in
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