Plant Microbiome: An Ocean Of Possibilities For Improving Disease Resistance in Plants Part 2

4. Role of Plant Defense Signatures in Shaping the Plant-Beneficial Microbiome

Plant-beneficial microbiome assembly is dynamically controlled by complex interactions among hosts, microorganisms, and environmental variables (14,64). There are many excellent reviews covering how root exudates and environmental factors shape the plant's beneficial microbiome under different conditions (13,14,65). In this review, we focus on how plant defense signatures influence the plant-beneficial microbiome. The plant immune system is a complex system regulated by different defense signatures hormones, such as salicylic acid (SA), jasmonic acid (A), and ethylene (ET). 

The role of these versatile hor. mones in plant defense responses are well understood in both model and crop plants. For example, SA-dependent defenses provide resistance to biotrophic pathogens, whereas JA and ET-dependent defenses are effective against necrotrophic pathogens and herbivorous insects (66,67). Recently, they have been identified as important drivers of plant-beneficial microbiome assembly. 

The relationship between hormones and immunity is complex and depends on multiple factors, such as hormone type, dose, mode of administration, distribution of cell receptors, individual immune status, and existing diseases.

Some hormones affect the immune response and affect different aspects of the immune system in different ways. For example, glucocorticoids can reduce inflammatory responses and immune cell-mediated cytotoxicity, which may lead to immunosuppression and susceptibility to infectious diseases. ACTH is related to the differentiation, proliferation, and function of immune cells, and plays an important role in the immune response.

On the other hand, the immune function of hormones may have an impact on specific types of diseases. For example, some hormones can affect the occurrence and development of autoimmune diseases by changing the activity and fate of immune cells, such as the role of insulin-like growth factor and thyroid stimulating hormone in diabetes and autoimmune thyroid diseases.

Overall, the immune system and hormones are complex systems that regulate and influence each other, and careful research is needed to gain a deep understanding of their interactions. From this point of view, we need to improve our human immunity, and Cistanche can be significantly improved, because Cistanche is rich in a variety of antioxidant substances, such as vitamin C, vitamin C, carotenoids, etc. These ingredients can scavenge free radicals and reduce oxidative stress, Improving the resistance of the immune system.

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For instance, Lebeis et al. (68] reported that SA modulates the colonization of the root microbiome via specific bacterial taxa in Arabidopsis. This study showed that SA knock-out Arabidopsis mutants have root microbiomes that differ from the wild-type relative abundance of specific bacterial families. On the other hand, NPR1 (SAreceptor) mutants have reduced endosphere microbiome diversity, mainly alpha diversity, and also less endophyte colonization (69,701. The JA pathway was also identified as an important driver of plant-immune-system-mediated microbiome assembly in ArabidopsisThis study showed that the mutant JA pathway in Arabidopsis plants, namely myc2 andmed25, have distinct microbial communities when compared to wild-type plants (71)

Similarly, in Arabidopsis, exogenous treatment with JA was proven to boost Arabidopsis rhizosphere alpha diversity while also enriching many important beneficial microbial taxa (72). ET, which often acts synergistically with JA in defense signaling, also influences beneficial microbiome assembly. For example, in peanuts, exogenous ET increases rhizosphere alpha diversity, particularly the amount of actinobacteria, while decreasing the abundance of acid bacteria (70). However, the effect of plant defense signatures coolant beneficial microbiome assembly varies among plant species and compartments. 

For example, it has been shown that JA plays a different role in epiphytic Arabidopsis leaf com. munities and wheat (T. aestivum) root endosphere community composition (73,74). These findings imply that the effect of plant hormones on the root microbiota may vary by speciesUnderstanding how plant hormones affect the root beneficial microbiome in crops is crucial for manipulating plant-microbiome interactions for better plant productivity. However many questions remain unanswered: dates, which in turn influence the beneficial microbiome? (2) 

How do trio SA/JA and Elcrosstalk influence the plant's beneficial microbiome during pathogen infections? (3) How do plant defense signatures interact with other drivers of microbiome assembly, and what is their effect on the beneficial microbiome? A deeper understanding of the manipulation of the plant microbiome by the endogenous pathway may provide novel breeding and engineering strategies to improve sustainable yields and crop resilience. Furthermore, we summarize how plant defense signatures influence plant beneficial microbiome assembly in Figure 4.

5. Developing Disease-Resilient Microbial Communities for Disease Resistance

Over the last decade, our understanding of the plant-beneficial microbiome has grown dramatically. Integrated techniques, such as various multi-omics and microbiome engineering strategies, have significantly improved our understanding of the organization and dynamics of the plant microbiome and its interactions [13,14,75]. For instance, in wild and benzoxazinoid precursor mutant maize plants, a combined metagenomic and metabolomic analysis revealed that benzoxazinoid metabolites play an important role in the formation of the rhizosphere microbiome [76]. 

Similarly, Stringlis et al. [77] discovered that coumarin exudation from roots can influence the rhizosphere microbiome in Arabidopsis (wild and mutant) plants using combined metabolomics and shotgun metagenomics methods. Recent work used metagenomics and metabolomics to explore the effect of root-exuded triterpenes on root microbiota composition [78]. However, there are few studies on the plant's beneficial microbiome and disease resistance. 

Nevertheless, plant-beneficial microbiomes and their products are attracting increasing interest as a means of combating disease outbreaks under climatic changes due to their all-around performance against multiple stressors and their plant-growth-promotion traits. However, due to limited knowledge, many things remain unknown. In this context, the integration of multi-omics can provide novel insights into how the plant immune system regulates plant beneficial microbiome assembly, root exudates chemistry, and their selection. 

Moreover, the application of multi-omics can help unravel how SA/JA and ET trigger transcriptional, metabolic, and proteomic reprogramming, which influence plant-beneficial microbiome assembly and which can, in turn, promote growth and disease resistance. So far, different microbial members have been identified to inhibit infections; however, their applicability in the field is limited due to their reliance on numerous host and environmental parameters. Moreover, microbes vary in terms of their physiology, metabolism, and susceptibility to temperature and moisture. Consequently, the composition of the plant's beneficial microbiome may be directly impacted by climate change. Microbial communities living on the surface of plants, such as the phyllosphere, are expected to be more directly impacted by climate change than those inside plant tissue ecosystems, which tend to experience more constant environmental circumstances [79]. 

Therefore, the absence of above-ground rescuers can increase the likelihood of a pathogen or disease spreading to the plant’s above-ground parts. In this context, beneficial microbiome engineering and host gene editing may aid in overcoming these constraints [80]. Moreover, engineered plants that secrete exudates that encourage particular advantageous plant–microbe interactions may be possible, which can confer disease resistance and plant growth promotion. Previous studies have revealed that native microbiota can rescue their hosts from emerging disease outbreaks [81]. Therefore, to fully utilize the potential of the native microbiota, microbiome engineering or host editing may be the most practical strategies for creating effective, customized microbial consortia that can be used to manage future disease outbreaks. Owing to the complexity of plant–microbiome interactions, there remain many hidden secrets that limit our understanding and their impact on each other. 

However, the advent of new technologies such as deep learning, artificial intelligence, and high-throughput phenotypic platforms is providing incredible insights into the plant microbiome world, aiding scientists to better understand their intricacy and develop new models of relationships between plants and their beneficial microbiomes. Furthermore, in Figure 5, we summarize various tools that can be used to explore the new frontiers of the plant-beneficial microbiome world concerning disease resistance. Numerous national and international policy authorities have acknowledged that it is crucial to manipulate the plant–soil microbiome to boost plant productivity in the face of climate change [79,82]. In the future, tailored microbial communities will be the most viable sources to prevent disease outbreaks in sustainable agriculture. Moreover, future breeding strategies may be expanded by understanding how wild relatives may involve plant genes in beneficial microbiome construction under disease outbreaks, which can help in identifying traits that can be used for developing disease-resistant crops.

6. Conclusions and Future Perspectives

At present, our agriculture is facing several challenges, such as global climate change, abiotic and biotic stressors, soil infertility, water shortages, and pollution, all of which have a significant impact on crop output and pose a serious threat to food security. Similar to this, plant pathogens and the disease outbreaks they cause have had a major impact on our agricultural system for decades, causing enormous food and economic catastrophes. Currently, both endemic and emerging plant diseases are spreading and intensifying due to the increased rate of global climate change, mutations and the evolution of new pathovars, pathogen spillover, and transmission via world food trade networks, which have made it difficult to control them with currently available treatments. 

Therefore, it is necessary to find new remedial tools that provide an efficient and long-lasting way to increase disease resistance and crop productivity sustainably. In light of this, utilizing the potential of plant-beneficial microbiomes and their products is one of the most adaptable ways to combat infections and disease outbreaks in our agriculture system. The increased interest in the plant-beneficial microbiome results from its significant potential to offer environmentally friendly solutions in plant disease protection and cutting-edge tools to promote sustainability in agroecosystems, contributing to a new Green Revolution that is safe for humans and the environment [83]. Over the last 10 years, our understanding of plant–microbe interactions and their effects on crop resilience and production has significantly advanced as a result of omics and other molecular tools. 

However, we are beginning to understand this dynamic and intricate relationship between the beneficial microbiome of the plant and the effects it has on plant fitness and productivity. Nevertheless, in the past many studies have shown that plants shape their beneficial microbiome under different stress conditions to protect themselves. These studies are indeed open new frontiers in the plant-beneficial microbiome world. Unraveling the beneficial microbiome’s potential for crop resilience and productivity is challenging due to the intricacy of plant microbiome dynamics and the reliance on external factors. Moreover, our understanding of the significance of the plant-beneficial microbiome in terms of ecology and function remains restricted, even though analytical studies of plant–microorganism interactions have expanded in recent years. Plants have diverse ecological niches that harbor distinct microbiomes, and their organization is determined by genetic, metabolic, and ecological factors. Over the last 10 years, significant progress has been made in understanding the role of genetic and metabolic drivers that influence plant-beneficial microbiomes; however, ecological drivers remain mostly unexplored. 

There is a need to study the trio relationships among hosts, beneficial microbiome, and their ecological traits, which can provide incredible information about the core microbiome and its taxonomic and functional attributes. In this regard, integrating molecular biology, synthetic biology, and ecology can be crucial for uncovering the complexity of the plant-beneficial microbiome and its usage in the development of high-yielding, smart, and climate-resilient crops in the future.

In this review, we provide a multiscale overview of the role of the plant-beneficial microbiome in disease resistance, which has recently become one of the most exciting research in the field of plant stress biology. Below, we highlight several outstanding questions that need to be addressed to explore the potential of the plant's beneficial microbiome in disease resistance. How does the plant beneficial microbiome mimic or evade the plant immune system? Does it have a similar approach to evading, or is it different from pathogens? How do plant immune system signatures, such as SA, JA, and ET, as well as the trio crosstalk, influence beneficial microbiome assembly? 

How does the beneficial microbiome function against biotrophic and necrotrophic pathogens, and how does their signaling affect microbiome structure? How does the plant-beneficial microbiome offer disease protection under multiple stresses [84]? Our understanding of the plant immune system is largely based on decades of research on the interactions between plants and pathogens. In the context of the microbiome, this knowledge is currently being reviewed, evaluated, and organized, finding fascinating contrasts and similarities [85]. Therefore, future research should focus on how the plant immune system reacts with different plant-beneficial microbiomes and on how it influences the particular beneficial microbiota that promotes crop fitness and productivity.

Author Contributions:

Conceptualization, H.B., S.A., and A.T.; writing—original draft preparation, S.A. and A.T.; writing—review and editing, S.A., A.T. and H.B.; visualization, A.T.; supervision, H.B.; project administration, H.B.; funding acquisition, H.B. All authors have read and agreed to the published version of the manuscript.

Funding:

This research was supported by the Forest Science and Technology Research and Development Project number (2023507C10-2323-AB01) of the Korea Forestry Agency (Korea Forestry Promotion Institute).

Institutional Review Board Statement:

Not applicable.

Informed Consent Statement:

Not applicable.

Data Availability Statement:

Not applicable.

Conflicts of Interest:

The authors declare no conflict of interest.

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