Molecular Soil Biology 2024, Vol.15 http://bioscipublisher.com/index.php/msb © 2024 BioSciPublisher, 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. BioSciPublisher, operated by Sophia Publishing Group (SPG), is an international Open Access publishing platform that publishes scientific journals in the field of life science. Sophia Publishing Group (SPG), founded in British Columbia of Canada, is a multilingual publisher. Publisher Sophia Publishing Group Editedby Editorial Team of Molecular Soil Biology Email: edit@msb.bioscipublisher.com Website: http://bioscipublisher.com/index.php/msb Address: 11388 Stevenston Hwy, PO Box 96016, Richmond, V7A 5J5, British Columbia Canada Molecular Soil Biology (ISSN 1925-2005) is an open access, peer reviewed journal published online by BioSciPublisher. The journal publishes in describing and explaining biological processes in soil in terms of soil micro-structure, soil micro-ecosystems, soil microbiology and molecular interactions among soil, microbes and plants, environmental stress resistances, effects of introduced genetically modified organisms, chemical contamination and soil bioremediation, modeling of soil biological and biochemical processes, application and outcomes on the soil biotechnology, etc. At each level, different disciplinary approaches are welcome: molecular biology, genetics, ecophysiology and soil physiochemical properties. All the articles published in Molecular Soil Biology 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. BioSciPublisher uses CrossCheck service to identify academic plagiarism through the world’s leading plagiarism prevention tool, iParadigms, and to protect the original authors’ copyrights.
Molecular Soil Biology (online), 2024, Vol. 15 ISSN 1925-2005 https://bioscipublisher.com/index.php/msb © 2024 BioSci 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 Progress of Biotin Research in Plants Delong Fan, Shenkui Liu, Yuanyuan Bu Molecular Soil Biology, 2024, Vol. 15, No. 1 Harnessing the Power of PGPR: Unraveling the Molecular Interactions Between Beneficial Bacteria and Crop Roots LizhenHan Molecular Soil Biology, 2024, Vol. 15, No. 2 Innovative Strategies for Soil Health Restoration in Saline-Alkali Environments: Leveraging Engineered Synthetic Microbial Communities (SynComs) Yuanyuan Bu, Siyuan Gao, Shenkui Liu, Ruisheng Song Molecular Soil Biology, 2024, Vol. 15, No. 3 Advancements in Symbiotic Nitrogen Fixation: Enhancing Sugarcane Production Wenzhong Huang Molecular Soil Biology, 2024, Vol. 15, No. 4 Dung Decomposers: Impact on Soil Fertility and Plant Growth Kaiwen Liang Molecular Soil Biology, 2024, Vol. 15, No. 5
Molecular Soil Biology 2024, Vol.15, No.1, 1-7 http://bioscipublisher.com/index.php/msb 1 Review and Progress Open Access Progress of Biotin Research in Plants DelongFan1,2, Shenkui Liu 3, Yuanyuan Bu1,2 1 Key Laboratory of Saline-Alkali Vegetation Ecology Restoration (Northeast Forestry University), Ministry of Education, Harbin, 150040, China 2 College of Life Sciences, Northeast Forestry University, Harbin, 150040, China 3 State Key Laboratory of Subtropical Silviculture, Zhejiang A & F University, Lin’an, Hangzhou, 311300, China Corresponding author email: yuanyuanbu@nefu.edu.cn Molecular Soil Biology, 2024, Vol.15, No.1 doi: 10.5376/msb.2024.15.0001 Received: 08 Feb., 2024 Accepted: 29 Feb., 2024 Published: 08 Mar., 2024 Copyright © 2024 Fan et al., 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: Fan D.L., Liu S.K., and Bu Y.Y., 2024, Progress of biotin research in plants, Molecular Soil Biology, 15(1): 1-7 (doi: 10.5376/msb.2024.15.0001) Abstract Biotin is an essential component of living organisms and an important cofactor for enzymes involved in carboxylation, decarboxylation, and transcarboxylation reactions. Most of the current research on biotin has been focused on microorganisms and animals, and relatively few studies have been conducted in plants, whereas biotin may play an important role in responding to abiotic stresses in plants. Therefore, this paper reviews the development history of biotin and the research progress in plants, considering the research progress in China and abroad. It provides new ideas for further research on the functions of biotin in plants and lays a theoretical foundation for the in-depth interpretation of the molecular network mechanism of biotin in regulating the response to abiotic stresses. Keywords Biotin; Synthesis pathway; AtBIO2; Abiotic stress Introduction In the face of climate change, many plants may be forced to adapt to new and potentially challenging environmental conditions (Lu et al., 2014; Fang and Xiong, 2015; Ding et al., 2019). Plants that face abiotic stresses such as low temperatures, drought, and salinity during growth and development acquire mechanisms to survive, through which they sense the stress and regulate their physiology accordingly. During this process, there must be some changes of substances in the plant body, and biotin is one of them. Biotin is a water-soluble vitamin that is an important cofactor for several carboxylases, decarboxylases, and transcarboxylases in a variety of metabolic pathways in organisms (Knowles, 1989). Biotin is found in almost all living cells. Bacteria, plants, some fungi, and a few animals synthesize biotin, which is essential for growth and development (Prasad et al., 1998; Stolz et al., 1999). Previous studies have found that many vitamins are essential for plant growth and development. For example, thiamine (Vitamin B1) is an essential factor for several enzymes involved in central carbon metabolism (Settembre et al., 2003; Nosaka, 2006). Pyridoxol (Vitamin B6) is a potent antioxidant, especially effective in removing mono-linear oxygen and superoxide anions (Danon et al., 2005). Vitamin C can reduce stress-induced damage by eliminating reactive oxygen species (Chen and Gallie, 2006; Paciolla et al., 2019). In addition, it has been reported that adding biotin to the fermentation medium enhances the antioxidant activity of Pichia guilliermondii (Qi et al., 2015). Reactive oxygen species (ROS) are products of aerobic metabolism in plants, and environmental stresses can lead to the accumulation of large amounts of ROS in plant cells. The presence of a small amount of reactive oxygen species can be used as a signaling molecule in the plant to induce the expression of key genes in the face of adversity, thus enhancing the plant's ability to resist stress. However, when a large amount of ROS is generated in the plant under stress conditions, many normal metabolic processes will be impeded and even lead to plant death. Therefore, an effective reactive oxygen species scavenging mechanism will help plants maintain an appropriate concentration of reactive oxygen species to enhance plant stress tolerance. Here, we review the history of biotin development and the biotin synthesis pathway in plants. The research progress of biotin in abiotic stresses in plants is described. A theoretical foundation is laid for further investigation of the function of biotin in plants against abiotic stresses.
Molecular Soil Biology 2024, Vol.15, No.1, 1-7 http://bioscipublisher.com/index.php/msb 2 1 Discovery and Naming of Biotin Biotin (Vitamin B7 or Vitamin H) is a water-soluble vitamin essential for the normal metabolism of fats and proteins. In 1901, Wildiers first discovered a factor in yeast that is essential for its growth and named it "biotin". Bateman's team fed test animals an overdose of raw egg whites and found that this resulted in dermatitis and hair loss, which disappeared when the raw egg whites were heated (Bateman, 1916). Boas (1927) described an injury to the skin of rats caused by feeding them raw egg whites, and the appearance of a "protective factor X" in various foods which prevented and cured this injury. Allison's team discovered a respiratory auxin whose function was to promote the growth of rhizobial isolates and named it "auxin R" (Allison et al., 1933). At the same time, Kuhn also discovered this factor and called it Vitamin H. In 1936, Kogl and Tonnis isolated a substance in egg yolks that is essential for yeast growth and called it "biotin". In 1941, Du Vigneagud's team identified coenzyme R and biotin as the same substance, formalized the molecular formula of biotin, and isolated it from the liver (Du Vigneaud et al., 1940; György et al., 1940). The following year, Du Vigneaud's team formalized the structure of biotin (Du Vigneaud, 1942). 2 Synthesis of Biotin Bacteria and plants can synthesize the required biotin by themselves (Prasad et al., 1998; Stolz et al., 1999). The first relevant explorations of biotin synthesis were done in bacteria. Initially, the biotin synthesis pathway starting from primeloyl CoA and alanine was elucidated in bacteria. And biotin biosynthesis in bacteria involves a four-step reaction with the products being 7-keto-8-aminopelargonic acid (KAPA), 7,8-diaminopelargonic acid (DAPA), desulfotransfer biotin (DTB), and finally biotin. In Escherichia coli, these enzymes (bioF, bioA, bioD, bioB) are encoded by four genes clustered into a single manipulator whose structure and function have been elucidated in detail (Marquet et al., 2001). Research on biotin synthesis in plants began with the model plant Arabidopsis thaliana. The biotin synthesis pathway in plants is similar to that in bacteria, and the process is carried out by enzymes encoded by the BIO4, BIO1-BIO3, BIO1-BIO3, and BIO2 genes, which are homologs of the bacterial bioF, bioA, bioD, and bioB genes, respectively. The first step is catalyzed by KAPA synthase (BIO4) in the cytosol to produce KAPA. The enzyme that catalyzes the second and third steps is composed of DAPA synthase (BIO1) and DTB synthase (BIO3), a combined enzyme gene named BIO1-BIO3 (Muralla et al., 2008) that catalyzes KAPA to produce DTB in mitochondria. The final step is catalyzed by biotin synthase (BIO2) to produce biotin in mitochondria. The BIO2-catalysed step is considered to be the rate-limiting step in the biotin synthesis pathway. Unlike the biotin synthesis pathway in bacteria, biotin in plants is synthesized at two different sites. The initial synthesis product, KAPA, is synthesized in the cytosol while the final conversion of desulfated biotin to biotin occurs in the mitochondria (Weaver et al., 1996; Picciocchi et al., 2003; Arnal et al., 2006). Metabolic enzymes that require biotin as a cofactor are usually located in four different sites: chloroplasts, mitochondria, proteasomes, and cytoplasm (Che et al., 2003). In recent years, it has been shown that peroxisomes exhibit involvement in biotin biosynthesis in plants and fungi. In fungi, peroxisome protein-deficient mutants exhibit biotin deficiency (Tanabe et al., 2011). 3 Advances in Plant Biotin Synthesis Genes Since the discovery of the biotin synthesis pathway in Arabidopsis thaliana, many efforts have been devoted to the study of biotin synthesis genes. AtBIO4 encodes a KAPA synthase, and the bio4-1 mutant accumulates hydrogen peroxide in large quantities and increases the expression of several genes involved in defense against reactive oxygen species signaling. genes involved in defense against reactive oxygen species signal transduction. Studies on bio4 mutants have revealed that biotin deficiency leads to light-dependent spontaneous cell death and regulates the expression of defensive genes (Li et al., 2012). In 1998, another biotin nutrient-deficient mutant, bio2, was identified and it was experimentally demonstrated that the addition of biotin resulted in normal growth of the bio2 mutant, but the addition of desulfurized biotin did not affect the mutant, thus identifying AtBIO2 as being involved in the final step of biotin synthesis. Later studies revealed that this catalytic reaction occurs in plant mitochondria and confirmed that AtBIO2 requires
Molecular Soil Biology 2024, Vol.15, No.1, 1-7 http://bioscipublisher.com/index.php/msb 3 mitochondria-targeted activity to fulfill its role in biotin synthesis (Patton et al., 1998). AtBIO3 was earlier thought to encode the gene encoding desulfurised biotin synthase in the biotin synthesis pathway and the bio3 mutant has a phenotype similar to that of and nutrient-deficient phenotype. However, in-depth studies have revealed that BIO3 and BIO1 produce chimeric BIO3-BIO1 transcripts, and this study confirms that BIO3-BIO1 has a bifunctional site that catalyzes two sequential reactions in the same metabolic pathway (Muralla et al., 2008). In all studies of mutants of biotin synthesis genes, it was confirmed that biotin is an essential vitamin for plant growth and that plants cannot grow in the absence of biotin synthesis and without exogenous biotin additions. In 2000, a yeast mutant lacking the vht1 gene (dvht1) was used to identify possible plant biotin transport proteins, and after complementation of an Arabidopsis cDNA library was screened for a single clone capable of growth in a medium containing low concentrations of biotin. This screen identified sequences with high similarity to sucrose transporters (e.g, AtSUC1, AtSUC2). Functional analysis of the proteins showed that a member of the Arabidopsis family of sucrose transporter proteins (named SUC5; At1g71890) was radiolabelled also confirming that SUC5 can transport biotin (Ludwig et al., 2000). In biotin biosynthesis-deficient (bio1 and bio2) embryos, SUC5 is an essential carrier for the delivery of biotin. 4 Progress in the Study of Plant Biotinases Many enzymes in plants catalyze carboxylation, decarboxylation, and transcarboxylation reactions with biotin as an essential cofactor (Nikolau et al., 2003). Carboxylases typically use bicarbonate ions as the carboxyl donor and organic molecules as the acceptor; decarboxylases typically use organic molecules as the donor and water as the carboxyl acceptor; and transcarboxylases typically use organic molecules as the carboxyl donor and organic molecules as the carboxyl acceptor (Knowles, 1989). Four carboxylases with biotin as a cofactor have been identified, and these carboxylases catalyse the following two-step reaction, with A representing the carboxylated receptor substrate: HCO3− + ATP + Enzyme-biotin → Enzyme-biotin-CO2− +ADP +Pi Enzyme-biotin-CO2− +A → Enzyme-biotin + A-CO2− Acetyl coenzyme A carboxylase (ACCase) first received attention as an important component of the fatty acid biosynthesis pathway, catalyzing the first rate-limiting step of fatty acid synthesis in the presence of ATP and bicarbonate with biotin as a cofactor (Salie and Thelen, 2016). In prokaryotes, green algae, and most plants, this enzyme is a heterologous complex, and its activity is dependent on four distinct subunits, biotin carboxylase (BC), biotin carboxyl carrier protein (BCCP), and α- and β-carboxyltransferases (CT) (Elborough et al., 1996). Embryo-specific overexpression of biotin carboxyl carrier protein 2 (BCCP2) in mature Arabidopsis thaliana seeds inhibits ACCase activity in plastids, thereby altering oil, protein, and carbohydrate composition (Chen et al., 2009). A novel family of proteins in Arabidopsis thaliana, named biotin/lipoic acid-binding structural domain-containing protein family (BADC), was identified in in vivo immunoprecipitation using subunit-specific antibodies. Immunoprecipitation methods demonstrated that this newly identified protein interacts with acetyl coenzyme A carboxylase. Meanwhile, the yeast two-hybrid technique demonstrated that the three protein isoforms of BADC interact with each of the two protein isoforms of BCCP, and this interaction is not biotin-dependent (Salie et al., 2016). Another carboxylase identified with biotin as a cofactor is 3-methylcrotonamide acetyl coenzyme A (MCCase) (Nikolau et al., 2003). MCCase is a complex consisting of the biotin subunit MCCA and the non-biotin subunit MCCB. It catalyzes the ATP-dependent process from 3-methylcrotonamide acetyl coenzyme A (MC-CoA) to 3-methyl glutamyl acetyl coenzyme A (MG-CoA) (McKean et al., 2000). When Arabidopsis was used as the study material, it was found that the catabolism of leucine in the mitochondria was inhibited in the mutant material of MCCA and MCCB, resulting in a significant increase in leucine accumulation in the plant. In addition, the mutant materials of MCCA and MCCB exhibited abnormal flower and cilia development and a significant decrease in mutant seed germination, phenotypes that were attributed to the blocked leucine metabolism (Ding et al., 2012). In the study of Arabidopsis MCCase, it was also found that MCCase is inhibited by exogenous carbohydrates, especially sucrose, a phenomenon that may predict that one of the major physiological roles of MCCase is the maintenance of carbon homeostasis in plants (Che et al., 2002).
Molecular Soil Biology 2024, Vol.15, No.1, 1-7 http://bioscipublisher.com/index.php/msb 4 5 Advances in the Study of Biotin in Abiotic Stresses in Plants Because plants grow solidly, they cannot move to escape from adversity, so abiotic stress (such as extreme temperature, salt stress, drought or light stress, etc.) will accompany the entire development process of plants, severely stressing their distribution, growth, quality and yield, and even survival. Plants can only adapt to the environment by changing their own morphology and structure as well as physiological and biochemical reactions, or by releasing chemicals to influence the growth and development of other plants in the neighbourhood, in order to change the microenvironment and make the environment more suitable for their own growth. Biotin is a cofactor in the first reaction step of the fatty acid biosynthesis pathway and also a rate-limiting step in the fatty acid biosynthesis pathway. Previously, biotin was also found to be involved in plant response to abiotic stresses. In 1996, Patton reported that the expression of the plant BIO2 was regulated by cellular biotin concentration (Patton et al., 1996). They also showed that BIO2 expression changes during the light/dark cycle and that this trend is reproducible, consistent with the regulation of light or circadian rhythms (Patton et al., 1996). In 2016, Shin Kamiyama found that different cultivation conditions have an effect on biotin content in green vegetables, especially in pea sprouts (Pisum sativum). The biotin content was reduced under low temperature or short light conditions. The expression of BIO2 gene also changed similarly to biotin content (Kamiyama et al., 2016). In 2020, Wang Yao found that the gene encoding biotin synthase, AtBIO2, was significantly up-regulated under carbonate stress, and AtBIO2 overexpression plants had significantly higher biotin content than wild-type Arabidopsis thaliana and were more resistant to carbonate stress. This demonstrates that the exogenous addition of biotin can enhance the ability of Arabidopsis thaliana to resist carbonate stress (Wang et al., 2020). 6 Future Prospects Previous studies on plant biotin have mainly examined fatty acid biosynthesis and accumulation (Chen et al., 2009; Jang et al., 2015). Earlier studies on biotin biosynthesis genes were related to potential bioherbicides (Hwang et al., 2010; Hahn et al., 2015). Currently, relatively few studies have been conducted on biotin's ability to protect plants from specific abiotic stresses. Therefore, in the future, it is necessary to further validate the relationship between biotin and plant resistance to abiotic stresses, and to explore the mechanism of biotin's action under specific abiotic stress conditions. In addition, the factors that regulate biotin synthesis in plants are unknown. Biotin synthesis requires energy inputs from ATP, SAM and other reducing equivalents (e.g. nicotinamide adenine dinucleotide phosphate). To date, the source of sulfhydryl coenzyme a, the precursor of biotin synthesis, remains unclear. Plants may utilize aminobutyric acid as a carbon source for biotin, but genes associated with aminobutyric acid coenzyme a synthase have not yet been identified in plants. In bacteria, the genes involved in biotin synthesis form a cluster of genes whose transcription is regulated by a biotin manipulator that is sensitive to both intracellular biotin concentration and the level of homologous proteins that require biotin (Chakravartty and Cronan, 2012). In Arabidopsis, genomic loci for genes involved in biotin synthesis are dispersed, although the bio1 and bio3 genes have a bifunctional locus and produce a fusion protein that catalyzes two sequential reactions in the biotin synthesis pathway (Muralla et al., 2008). However, the details of elucidating how genes involved in biotin synthesis are regulated in plants have not yet been reported, so in the future, we further explored the regulatory mechanisms of biotin synthesis and metabolism under abiotic stress conditions. Authors’ Contributions FDL drafted the manuscript and compiled the literatures. BYY was the director of the project and revised the manuscript. LSK supervised and critically revised the manuscript. All authors read and approved the final manuscript. Acknowledgments This work was supported by the Program for Changjiang Scholars and Innovative Research Team at the University (grant number: No. IRT17R99), the Fundamental Research Funds for the Central Universities (No. 2572022DX11), and Heilongjiang Province Government Postdoctoral Science Foundation (grant number: LBH-Q18008).
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Molecular Soil Biology 2024, Vol.15, No.1, 8-16 http://bioscipublisher.com/index.php/msb 8 Research Report Open Access Harnessing the Power of PGPR: Unraveling the Molecular Interactions Between Beneficial Bacteria and Crop Roots LizhenHan College of Life Science, Guizhou University, Guiyang, 550025, China Corresponding author email: lzhan1@gzu.edu.cn Molecular Soil Biology, 2024, Vol.15, No.1 doi: 10.5376/msb.2024.15.0002 Received: 20 Nov., 2023 Accepted: 25 Dec., 2023 Published: 15 Jan., 2024 Copyright © 2024 Han, 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: Han L.Z., 2024, Harnessing the power of PGPR: unraveling the molecular interactions between beneficial bacteria and crop roots, Molecular Soil Biology, 15(1): 8-16 (doi: 10.5376/msb.2024.15.0002) Abstract Plant growth-promoting rhizobacteria (PGPR) have emerged as a promising eco-friendly alternative to chemical fertilizers and pesticides, offering significant benefits for sustainable agriculture. This systematic review delves into the intricate molecular interactions between PGPR and crop roots, highlighting their potential to enhance plant growth and health. PGPR, such as fluorescent Pseudomonas spp., Bacillus cereus, and multispecies inoculants, have been shown to improve crop yields by various mechanisms, including nitrogen fixation, phosphate solubilization, siderophore production, and the synthesis of phytohormones These bacteria also play a crucial role in disease suppression by competing with pathogens for nutrients, producing antimicrobial compounds, and inducing systemic resistance in plants. The review further explores the role of root exudates and bacterial secretions in modulating these interactions, emphasizing the importance of specific genes and metabolites in the process. Recent advancements in metatranscriptomics and gene expression profiling have provided deeper insights into the molecular mechanisms underlying these beneficial interactions, paving the way for more effective application of PGPR in agriculture. By understanding these complex interactions, we can develop innovative strategies to harness the full potential of PGPR, ultimately contributing to sustainable crop production and environmental conservation. Keywords Plant growth-promoting rhizobacteria (PGPR); Crop roots; Molecular interactions; Sustainable agriculture; Nitrogen fixation; Phosphate solubilization; Disease suppression; Root exudates; Metatranscriptomics Plant Growth-Promoting Rhizobacteria (PGPR) are a diverse group of bacteria that colonize plant roots and enhance plant growth through various mechanisms. These mechanisms include nutrient solubilization, phytohormone production, and biological nitrogen fixation, among others (Lugtenberg and Kamilova, 2009; Bhattacharyya and Jha, 2011; Nagargade et al., 2018). The significance of PGPR lies in their potential to replace chemical fertilizers and pesticides, thereby promoting sustainable agricultural practices (Bhattacharyya and Jha, 2011; Pérez-Montaño et al., 2014; Sinha et al., 2021). Understanding the molecular interactions between PGPR and crop roots is crucial for optimizing their application and maximizing their benefits in agriculture (Benizri et al., 2001; Oleńska et al., 2020). PGPR are beneficial bacteria found in the rhizosphere, the region of soil surrounding plant roots. They promote plant growth directly by enhancing nutrient availability and indirectly by protecting plants from pathogens (Lugtenberg and Kamilova, 2009; Singh et al., 2013; Nagargade et al., 2018). The ability of PGPR to improve plant health and yield makes them a valuable tool in sustainable agriculture (Bhattacharyya and Jha, 2011; Pérez-Montaño et al., 2014; Sinha et al., 2021). The molecular interactions between PGPR and crop roots are complex and involve various signaling pathways and biochemical processes. These interactions are essential for the successful colonization of plant roots by PGPR and the subsequent promotion of plant growth (Benizri et al., 2001; Lugtenberg and Kamilova, 2009). A deeper understanding of these molecular mechanisms can lead to the development of more effective PGPR-based biofertilizers and biocontrol agents (Nagargade et al., 2018; Oleńska et al., 2020). The purpose of this review is to highlight the importance of PGPR in sustainable agriculture, identify key molecular mechanisms involved in PGPR-crop root interactions, and discuss potential applications and future
Molecular Soil Biology 2024, Vol.15, No.1, 8-16 http://bioscipublisher.com/index.php/msb 9 directions. By systematically reviewing the current knowledge on PGPR and their interactions with crop roots, this paper aims to provide a comprehensive understanding of their role in sustainable agriculture and identify areas for future research and development. 1 Molecular Mechanisms of PGPR-Root Interactions 1.1 Signal molecules and receptors Root exudates play a crucial role in attracting plant growth-promoting rhizobacteria (PGPR) to the rhizosphere. These exudates consist of a variety of organic compounds, including sugars, amino acids, and secondary metabolites, which serve as chemical signals to beneficial microbes. For instance, the study by (Yi et al., 2018) highlights the importance of root exudates in modulating the transcriptomic response of Bacillus mycoides to potato root exudates, indicating that these exudates are pivotal in establishing beneficial plant-microbe interactions. Similarly (Palma et al., 2020), discusses how root exudates influence the expression of bacterial genes involved in microbe-plant interactions, further emphasizing their role in attracting and selecting specific microbial populations. Specific signal molecules such as flavonoids and strigolactones are key players in the communication between plants and PGPR. Flavonoids, for example, have been shown to be involved in the biosynthetic pathways that regulate plant-microbe interactions (Thomas et al., 2019). These molecules not only attract beneficial bacteria but also modulate their behavior to enhance colonization and symbiosis. Strigolactones, another class of signal molecules, are known to play a role in the establishment of symbiotic relationships with mycorrhizal fungi and potentially with PGPR as well (Baysal and Silme, 2019). PGPR possess specific receptors that recognize and respond to plant-derived signals. These receptors enable the bacteria to detect and move towards the root exudates, facilitating colonization. The study by (Wheatley and Poole, 2018) reviews the molecular mechanisms governing bacterial attachment to roots, highlighting the role of specific receptors in recognizing plant signals. Additionally (Mark et al., 2005), identifies genes in Pseudomonas aeruginosa that are regulated in response to root exudates, suggesting the presence of specialized receptors that mediate these interactions. 1.2 Colonization and biofilm formation The initial attachment of PGPR to root surfaces is a critical step in the colonization process. This attachment is often mediated by bacterial surface structures such as pili and flagella, which facilitate close contact with the root epidermis (Wheatley and Poole, 2018). The biphasic mechanism of root attachment, as described in (Wheatley and Poole, 2018), involves an initial reversible phase followed by a more stable, irreversible attachment, ensuring effective colonization. Biofilm formation is a significant aspect of PGPR colonization, providing a protective environment for the bacteria and enhancing their ability to persist in the rhizosphere. Biofilms facilitate nutrient exchange and protect the bacteria from environmental stresses and antimicrobial compounds. The study by (Yi et al., 2018) underscores the importance of biofilm formation in the context of plant-microbe interactions, as it allows for sustained colonization and interaction with the host plant. Several factors influence the effectiveness of PGPR colonization, including the composition of root exudates, soil conditions, and the presence of other microbial communities. For instance (Somenahally, 2017), discusses how soil conditions such as moisture stress and pH can impact root-microbe interactions, thereby affecting colonization efficiency. Additionally, the presence of deleterious microorganisms in the rhizosphere can compete with PGPR for resources, influencing their colonization success (Schippers et al., 1987). 1.3 Modulation of root architecture PGPR can significantly influence root development and architecture, promoting root growth and branching. This modulation is often mediated by the production of plant hormones and other growth-promoting substances. For example (Thomas et al., 2019), identifies differentially expressed genes in rice roots during interactions with
Molecular Soil Biology 2024, Vol.15, No.1, 8-16 http://bioscipublisher.com/index.php/msb 10 Azospirillum brasilense, many of which are involved in hormone signaling pathways that regulate root development. PGPR influence root architecture through the production and modulation of plant hormones such as auxins, cytokinins, and gibberellins. Auxins, in particular, play a crucial role in root elongation and branching. The study by (Thomas et al., 2019) highlights the involvement of hormone signaling pathways in the interaction between rice roots and Azospirillum brasilense, indicating that PGPR can alter the hormonal balance within the plant to promote root growth. PGPR also interact with plant stress hormones such as ethylene and abscisic acid (ABA) to enhance plant stress tolerance. For instance (Pineda et al., 2010), reviews the role of beneficial soil-borne microbes in helping plants cope with biotic and abiotic stresses, including the modulation of stress hormone levels. By influencing the levels of ethylene and ABA, PGPR can help plants better manage stress conditions, thereby improving overall plant health and productivity. 2 Functional Benefits of PGPR in Crop Growth 2.1 Nutrient acquisition Plant Growth-Promoting Rhizobacteria (PGPR) play a crucial role in enhancing nutrient availability to crops through various mechanisms such as nitrogen fixation, phosphate solubilization, and potassium solubilization. For instance, PGPR like Azospirillum, Azotobacter, and Klebsiella are known for their nitrogen-fixing capabilities, which convert atmospheric nitrogen into a form that plants can readily absorb and utilize (Hayat et al., 2012; Kuan et al., 2016; Mohanty et al., 2021). Additionally, phosphate-solubilizing bacteria such as Bacillus megaterium and Pseudomonas species release organic acids that convert insoluble phosphates into soluble forms, making phosphorus more accessible to plants (Wu et al., 2012; Tang et al., 2020; Mohanty et al., 2021). PGPR facilitate nutrient uptake by altering plant hormone levels, which enhances root surface area and morphology, thereby increasing nutrient absorption. For example, the production of indole acetic acid (IAA) by PGPR stimulates root elongation and branching, leading to a larger root surface area for nutrient uptake (Bhattacharyya and Jha, 2011; Ankati and Podile, 2019; Mohanty et al., 2021). Furthermore, PGPR can produce siderophores that chelate iron from the soil, making it more available to plants (Bhattacharyya and Jha, 2011; Hayat et al., 2012). The synergistic interaction between earthworms and PGPR has also been shown to significantly increase the availability of nitrogen, phosphorus, and potassium in the soil, further enhancing nutrient uptake (Wu et al., 2012). 2.2 Stress tolerance PGPR contribute to plant tolerance against various abiotic stresses such as drought, salinity, and heavy metals. For instance, PGPR like Bacillus and Pseudomonas species produce exopolysaccharides that help in soil aggregation and water retention, thereby aiding plants in drought conditions (Hayat et al., 2012; Mohanty et al., 2021). Additionally, PGPR can produce ACC deaminase, which lowers ethylene levels in plants under stress, thus promoting root growth and stress tolerance (Bhattacharyya and Jha, 2011; Hayat et al., 2012). The molecular pathways involved in PGPR-mediated stress mitigation include the production of antioxidants, osmolytes, and stress-related proteins. For example, PGPR can induce the production of osmoprotectants like proline and trehalose in plants, which help in maintaining cellular osmotic balance under stress conditions (Hayat et al., 2012; Vejan et al., 2019). Moreover, PGPR can activate plant defense pathways by inducing the expression of stress-responsive genes, thereby enhancing the plant's ability to withstand adverse environmental conditions (Bhattacharyya and Jha, 2011; Hayat et al., 2012). 2.3 Disease suppression PGPR exhibit biocontrol mechanisms that suppress phytopathogens through the production of antimicrobial compounds, competition for nutrients and niches, and induction of systemic resistance in plants. For instance,
Molecular Soil Biology 2024, Vol.15, No.1, 8-16 http://bioscipublisher.com/index.php/msb 11 PGPR like Pseudomonas and Bacillus species produce antibiotics, siderophores, and lytic enzymes that inhibit the growth of pathogenic microbes (Bhattacharyya and Jha, 2011; Hayat et al., 2012; Mohanty et al., 2021). PGPR produce a variety of antimicrobial compounds such as hydrogen cyanide, phenazines, and pyrrolnitrin, which directly inhibit the growth of phytopathogens (Bhattacharyya and Jha, 2011; Hayat et al., 2012; Mohanty et al., 2021). These compounds disrupt the cell membranes of pathogens, interfere with their metabolic processes, and ultimately lead to their death. PGPR can induce systemic resistance in plants, making them more resilient to pathogen attacks. This is achieved through the activation of plant defense mechanisms, including the production of pathogenesis-related proteins and secondary metabolites (Bhattacharyya and Jha, 2011; Hayat et al., 2012). For example, the production of volatile organic compounds (VOCs) by PGPR can trigger systemic resistance in plants, enhancing their overall immunity against a wide range of pathogens (Bhattacharyya and Jha, 2011; Hayat et al., 2012). In summary, PGPR offer multifaceted benefits in crop growth by enhancing nutrient acquisition, improving stress tolerance, and suppressing diseases through various biochemical and molecular mechanisms. These attributes make PGPR a valuable tool in sustainable agriculture, reducing the reliance on chemical fertilizers and pesticides while promoting healthier and more resilient crops. 3 Genomic and Proteomic Insights 3.1 Genomic studies Recent advancements in sequencing technologies have significantly enhanced our understanding of the genomic landscape of Plant Growth-Promoting Rhizobacteria (PGPR). High-throughput sequencing methods, such as next-generation sequencing (NGS), have enabled comprehensive genomic analyses, facilitating the identification of key genes and regulatory networks involved in PGPR-plant interactions. These technologies have allowed researchers to sequence entire genomes of various PGPR strains, providing insights into their genetic makeup and potential functional capabilities (Verma et al., 2018). Genomic studies have identified several key genes that play crucial roles in the interaction between PGPR and plants. These genes are involved in various processes such as nitrogen fixation, production of phytohormones, and synthesis of antimicrobial compounds. For instance, genes responsible for the production of indole-3-acetic acid (IAA), a plant hormone that promotes root elongation, have been identified in multiple PGPR strains (Ambrosini and Passaglia, 2017). Additionally, genes encoding for enzymes involved in phosphate solubilization and siderophore production, which enhance nutrient availability to plants, have also been characterized (Verma et al., 2018). The expression of these genes is often regulated in response to plant signals, highlighting the dynamic nature of PGPR-plant interactions. 3.2 Proteomic studies Proteomic analyses have revealed a diverse array of proteins and enzymes secreted by PGPR that contribute to plant growth promotion and stress resistance. For example, the proteomic study of Paenibacillus polymyxa E681 interacting with Arabidopsis thaliana identified 41 differentially expressed proteins, including those involved in amino acid metabolism, antioxidant activity, and defense responses (Kwon et al., 2016). These proteins play vital roles in enhancing plant growth and providing resistance against environmental stresses. The functional roles of PGPR proteins in promoting plant growth are multifaceted. Proteins involved in nitrogen fixation, such as nitrogenase, facilitate the conversion of atmospheric nitrogen into a form that plants can readily assimilate (Ambrosini and Passaglia, 2017). Enzymes like ACC deaminase lower plant ethylene levels, which can otherwise inhibit root growth under stress conditions (Ambrosini and Passaglia, 2017). Additionally, proteins involved in the synthesis of antimicrobial compounds help in suppressing plant pathogens, thereby protecting the plants and promoting healthier growth (Verma et al., 2018). The upregulation of defense-related proteins in plants treated with PGPR, as observed in proteomic studies, further underscores the role of these proteins in enhancing plant resilience against biotic and abiotic stresses (Kwon et al., 2016; Dhawi, 2020).
Molecular Soil Biology 2024, Vol.15, No.1, 8-16 http://bioscipublisher.com/index.php/msb 12 In summary, genomic and proteomic studies have provided valuable insights into the molecular mechanisms underlying PGPR-plant interactions. The identification of key genes and proteins involved in these interactions paves the way for the development of more effective PGPR-based biofertilizers and biocontrol agents, contributing to sustainable agricultural practices. 4 Applications and Future Directions 4.1 Agricultural practices The integration of Plant Growth-Promoting Rhizobacteria (PGPR) into crop management practices has shown significant promise in enhancing crop productivity and sustainability. PGPR can be applied through various methods such as seed inoculation, soil application, and fertigation. These methods have been demonstrated to improve nutrient availability, enhance root growth, and increase crop yields (Lopes et al., 2021; Mohanty et al., 2021; Stoll et al., 2021). For instance, the use of Bacillus velezensis strain BBC047 in nurseries and post-transplantation stages has significantly improved the growth and productivity of horticultural crops like basil, cabbage, tomato, and bell pepper (Stoll et al., 2021). Additionally, the combination of biochar with PGPR inoculants has been shown to enhance soil fertility and crop yield, particularly in acidic sandy soils (Kari et al., 2021). The formulation and application methods for PGPR inoculants are critical for their effectiveness. Successful PGPR formulations should possess high rhizosphere competence, extensive competitive saprophytic ability, and ease of mass production (Mohanty et al., 2021). Seed coating, soil application, and root inoculation are common methods used to apply PGPR. However, challenges such as inconsistent results due to varying soil conditions and environmental factors need to be addressed (Lopes et al., 2021). Innovative approaches like immobilizing PGPR on biochar surfaces have shown promise in enhancing the effectiveness of PGPR inoculants (Kari et al., 2021). Moreover, the timing of PGPR application is crucial, with early-stage applications in nurseries being more effective than late-stage applications (Stoll et al., 2021). 4.2 Biotechnological advances Genetic engineering of PGPR offers the potential to enhance their efficacy in promoting plant growth and stress tolerance. Advances in molecular biology and genetic engineering have enabled the development of PGPR strains with improved traits such as enhanced nutrient solubilization, hormone production, and stress tolerance (Oleńska et al., 2020; Mellidou and Karamanoli, 2022). For example, genetically engineered PGPR strains can produce higher levels of phytohormones like indole acetic acid (IAA) and ethylene, which are crucial for plant growth and stress response (Oleńska et al., 2020; Mohanty et al., 2021). Additionally, the identification and manipulation of genes associated with induced systemic resistance (ISR) can further enhance the biocontrol capabilities of PGPR (Meena et al., 2020). The development of synthetic microbial consortia involves combining multiple PGPR strains to create a synergistic effect that enhances plant growth and health. These consortia can be tailored to specific crops and environmental conditions, providing a more robust and effective solution compared to single-strain inoculants (Li et al., 2020). For instance, a consortium of Providencia rettgeri, Advenella incenata, Acinetobacter calcoaceticus, and Serratia plymuthica has been shown to improve the growth and soil properties of various crops (Li et al., 2020). The use of synthetic microbial consortia can also help in overcoming the limitations of individual PGPR strains by providing a broader spectrum of beneficial traits (Li et al., 2020; Kong and Liu, 2022). 4.3 Challenges and future research Despite the promising potential of PGPR, several challenges hinder their widespread application. Inconsistent results due to varying soil conditions, environmental factors, and the complex interactions within the rhizosphere are major obstacles (Lopes et al., 2021). Additionally, the survival and persistence of PGPR in the soil environment are critical factors that influence their effectiveness (Kong and Liu, 2022). Technical issues related to the formulation and application methods, such as seed coating, also need to be addressed to ensure the successful integration of PGPR into conventional agricultural practices (Stoll et al., 2021).
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