Editorial: Tobacco disease and biological control

Editorial on the Research Topic
Tobacco disease and biological control

Tobacco-inhabiting microorganisms play a crucial role in determining the quality and yield of tobacco products. Over the past decade, significant advancements have been made in understanding the microbial dynamics of smokeless tobacco. These microbiomes have also been linked to the development of several oral diseases, including oral squamous cell carcinoma (Saxena et al., 2022; Srivastava et al., 2022). Additionally, because of its economic importance, preventing and controlling tobacco-related diseases has been a major concern to improve both yield and quality. Microorganisms play a crucial role in fermentation by enhancing aroma and sensory attributes. Next-Generation Sequencing (NGS) has become vital for uncovering hidden information about uncultivable microorganisms. When combined with meta-transcriptomics, meta-proteomics, and metabolomics, NGS allows for comprehensive analysis of both pathogenic and non-pathogenic microbes. This Research Topic emphasizes the health of economically important tobacco crops. It covers 14 research articles on various facets of microorganisms affecting the health factors, aroma, diseases, and yield of smokeless tobacco.

Physical parameters significantly influence the fermentation process. Zhang et al. observed temperature-dependent improvements to the sensory qualities of cigar tobacco leaves. Furthermore, bacterial diversity in tobacco also showed high levels of Oceanobacillus and Bacillus, along with Staphylococcus and Corynebacterium, during increasing temperatures (35 ± 2 °C to 45 ± 2 °C). Bacillus spp. play a major role in the tobacco bacterial microbiome (Han et al., 2016; Sajid et al., 2021; Vishwakarma and Verma, 2024). Whole genome sequencing analysis by Wei et al. revealed that Bacillus halotolerans NS36 and Bacillus mycoides NS75 positively impact the sensory qualities of tobacco. Several reports highlight moisture's vital role in tobacco leaf fermentation. Gao et al. performed NGS-based analysis of cigar tobacco leaves and found that varying water content significantly alters the structure and abundance of bacterial communities. Furthermore, Li et al. conducted an NGS study on cigar tobacco leaves and observed a significant microbial shift due to air curing. Here, Pseudomonas and Sphingomonas populations were shifted to Pantoea from the pre- to post-air-curing stages. This transition resulted in increased pathways related to carbohydrate and amino acid metabolism, leading to the formation of flavor compounds in the middle leaves of tobacco. Wang et al. also performed multi-omics to understand the phyllosphere microbial community. The study concluded that the mid-stage is the most active metabolic phase, so this should be explored to develop biomarkers to assess the fermentation quality.

Fu et al. reported a correlation between fungal diversity and leaf health of tobacco. Healthy and moldy tobacco leaves exhibited significant differences in fungal communities. During analysis, Aspergillus was observed as the most harmful mold and notably reduced overall tobacco quality. Moldy tobacco also showed a notable decrease in pH, alkaloids, and flavor compounds, while fatty acid esters increased due to the abundance of Aspergillus. Fungi and yeasts influence various plant attributes. Ma et al. observed a significant shift in the rhizosphere bacterial diversity of tobacco due to the oomycete pathogen Phytophthora nicotianae. Further analysis revealed the buildup of beneficial microbes in the inter-root zone that form biofilms and activate the plant's immune system against pathogens. Jiang et al. studied the interactions in fungal-bacterial communities that combat Root-Knot Nematode (RKN) caused by Meloidogyne incognita. During RKN infection, an abundance of Microbacterium spp. and fungi was observed. Such symbiotic bacterial-fungal interactions could be developed as biocontrol agents for other nematodes. Sang et al. found that organic and fatty acids were more prevalent in RKN-infected soil compared to healthy soil, showing positive correlations with Basidiomycota, Agaricales, and Ralstonia. Whereas, Yang et al. observed that the diversity and count of pathogenic fungi significantly increased in Fusarium-infected tobacco roots as compared to the healthy plant. Shotgun-based metagenomic analysis showed a notable decrease in carbon metabolism in diseased tobacco. Mai et al. studied the yeast Phaffia rhodozyma for its potential to enhance tobacco aroma via fermentation; this yeast produces the valuable carotenoid astaxanthin, which stimulates sensory molecules in tobacco.

Intercropping has proven to be a fruitful traditional method for improving soil health. This was also reflected in microbial diversity during tobacco-maize relay intercropping. Yang et al. observed higher levels of beneficial microorganisms in intercropped systems compared to monoculture, which assisted in increasing the availability of phosphorus, nitrogen, and potassium in the soil.

The impact of viruses on the overall health of smokeless tobacco plants remains less studied. In a study, Sun et al. expressed the3′ UTR of Tobacco Vein Mottling Virus (TVMV) near Green Fluorescent Protein (GFP) in a tobacco plant. Transcriptome analysis showed that this3′ UTR could activate multiple plant resistance genes, indicating that viral non-coding regions play a pivotal role in plant antiviral defense mechanisms. The study of Wang et al. concludes that copper-zinc superoxide dismutases (Cu/Zn-SOD) play a significant role in the antiviral response in tobacco.

Overall, the Research Topic concludes that microorganisms significantly influence the health of tobacco. Microbes assist fermentation and incorporate flavor-enhancing alkaloids and flavonoids. A healthy microbiome can help to control diseases by stimulating plant defense mechanisms. With advancements in omics technologies, much progress has been made in understanding tobacco microbiology. However, there are lots of basic and applied research on the way, for instance, metabolomics studies are needed to better understand how microbes influence tobacco quality and disease resistance. Additionally, specific active microorganisms must be screened for their functions in tobacco products. Microorganism-pathogen-plant interactions must be verified to support the development of products with more practical and feasible applications.

Author contributions

DV: Conceptualization, Methodology, Validation, Writing – original draft, Writing – review & editing. ZZ: Conceptualization, Investigation, Methodology, Validation, Writing – original draft, Writing – review & editing. JL: Conceptualization, Investigation, Methodology, Validation, Writing – original draft, Writing – review & editing.

Acknowledgments

DV is grateful to ANRF, New Delhi, under grant number (CRG/2023/000676) for supporting smokeless tobacco research.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

The author(s) declared that they were an editorial board member of Frontiers at the time of submission. This had no impact on the peer review process and the final decision.

Generative AI statement

The author(s) declare that no Gen AI was used in the creation of this manuscript.

Any alternative text (alt text) provided alongside figures in this article has been generated by Frontiers with the support of artificial intelligence and reasonable efforts have been made to ensure accuracy, including review by the authors wherever possible. If you identify any issues, please contact us.

Publisher's note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

References

Han, J., Sanad, Y. M., Deck, J., Sutherland, J. B., Li, Z., Walters, M. J., et al. (2016). Bacterial populations associated with smokeless tobacco products. Appl. Environ. Microbiol. 82, 6273–6283. doi: 10.1128/AEM.01612-16

PubMed Abstract | Crossref Full Text | Google Scholar

Sajid, M., Srivastava, S., Kumar, A., Kumar, A., Singh, H., and Bharadwaj, M. (2021). Bacteriome of moist smokeless tobacco products consumed in India with emphasis on the predictive functional potential. Front in Microbiol. 12:3908. doi: 10.3389/fmicb.2021.784841

PubMed Abstract | Crossref Full Text | Google Scholar

Saxena, R., Prasoodanan P K, V., Gupta, S. V., Gupta, S., Waiker, P., Samaiya, A., et al. (2022). Assessing the effect of smokeless tobacco consumption on oral microbiome in healthy and oral cancer patients. Front. Cell. Infect. Microbiol. 12:841465. doi: 10.3389/fcimb.2022.841465

PubMed Abstract | Crossref Full Text | Google Scholar

Srivastava, A., Mishra, S., Garg, P. K., Dubey, A. K., Deo, S. V. S., and Verma, D. (2022). Comparative and analytical characterization of the oral bacteriome of smokeless tobacco users with oral squamous cell carcinoma. Appl. Microbiol. Biotechnol. 106, 4115–4128. doi: 10.1007/s00253-022-11980-5

PubMed Abstract | Crossref Full Text | Google Scholar

Vishwakarma, A., and Verma, D. (2024). 16S rDNA-based amplicon analysis unveiled a correlation between the bacterial diversity and antibiotic resistance genes of the bacteriome of commercial smokeless tobacco products. Appl. Biochem. Biotechnol. 196, 6759–6781. doi: 10.1007/s12010-024-04857-y

PubMed Abstract | Crossref Full Text | Google Scholar