Effects of a co-bacterial agent on the growth, disease control, and quality of ginseng based on rhizosphere microbial diversity

Li et al. BMC Plant Biology (2024) 24:647 https://doi.org/10.1186/s12870-024-05347-3 BMC Plant Biology Open Access RESEARCH Effects of a co-bacterial agent on the growth, disease control, and quality of ginseng based on rhizosphere microbial diversity Xinyue Li1†, Qun Liu2†, Yugang Gao1*, Pu Zang1 and Tong Zheng1 Abstract Background The ginseng endophyte Paenibacillus polymyxa Pp-7250 (Pp-7250) has multifaceted roles such as preventing ginseng diseases, promoting growth, increasing ginsenoside accumulation, and degrading pesticide residues, however, these effects still have room for improvements. Composite fungicides are an effective means to improve the biocontrol effect of fungicides, but the effect of Pp-7250 in combination with its symbiotic bacteria on ginseng needs to be further investigated, and its mechanism of action has not been elucidated. In this study, a series of experiments was conducted to elucidate the effect of Paenibacillus polymyxa and Bacillus cereus co-bacterial agent on the yield and quality of understory ginseng, and to investigate their mechanism of action. Results The results indicated that P. polymyxa and B. cereus co-bacterial agent (PB) treatment improved ginseng yield, ginsenoside accumulation, disease prevention, and pesticide degradation. The mechanism is that PB treatment increased the abundance of beneficial microorganisms, including Rhodanobacter, Pseudolabrys, Gemmatimonas, Bacillus, Paenibacillus, Cortinarius, Russula, Paecilomyces, and Trechispora, and decreased the abundance of pathogenic microorganisms, including Ellin6067, Acidibacter, Fusarium, Tetracladium, Alternaria, and Ilyonectria in ginseng rhizosphere soil. PB co-bacterial agents enhanced the function of microbial metabolic pathways, biosynthesis of secondary metabolites, biosynthesis of antibiotics, biosynthesis of amino acids, carbon fixation pathways in prokaryotes, DNA replication, and terpenoid backbone biosynthesis, and decreased the function of microbial plant pathogens and animal pathogens. Conclusion The combination of P. polymyxa and B. cereus may be a potential biocontrol agent to promote the resistance of ginseng to disease and improve the yield, quality, and pesticide degradation. Keywords Co-bacterial agent, Ginseng yield, Ginsenoside, Biological control, Pesticide degradation, Microbial community † Xinyue Li and Qun Liu contribute equally this work. *Correspondence: Yugang Gao 1 College of Chinese Medicinal Materials and Laboratory of Medicinal Plant Cultivation and Breeding of National Administration of Traditional Chinese Medicine, Jilin Agricultural University, Changchun 130118, China 2 Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Jiangsu Key Laboratory for the Research and Utilization of Plant Resources, Nanjing 2100147, China © The Author(s) 2024. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Li et al. BMC Plant Biology (2024) 24:647 Introduction Ginseng (Panax ginseng C. A. Meyer), a perennial herb genus in the family Araliaceae, is a traditional Chinese herb with significant medicinal and economic value [1]. Its demand is huge and it has a large planting area. Ginseng cultivation methods can be classified as forest-cultivated ginseng, cutting down forest-cultivated ginseng, and farmland-cultivated ginseng [2]. The cultivation of P. ginseng in the forest is a kind of wild cultivation mode. With an increase in the growing years, there are problems such as severe disease, long growth cycles, slow ginsenosides accumulation, and high pesticide residues, which seriously affect the yield and quality of ginseng [3, 4], limiting its production and application of ginseng. Beneficial microorganisms play an important role in biological control, plant growth promotion, effective composition accumulation and pesticide residue degradation [5, 6]. The use of bioinoculants for the ecological cultivation of ginseng is of great relevance for high-quality and safe ginseng herbs [7]. Biological control is an environmentally friendly and low-cost ginseng disease control method attracting increasing attention. Bacillus amyloliquefaciens FG14 showed good control of ginseng root rot [8]; Bacillus subtilis HK-CSM-1 can be used as an effective and ecologically friendly biological control agent for anthracnose in P. ginseng [9]; and ginseng endophytic PgBE14 (Bacillus amyloliquefaciens), PgBE40 (B. megaterium), PgBE45 (Pseudomonas frederiksbergensis), and PgBE42 (Staphylococcus saprophyticus) are antagonistic to two pathogens Cylindrocarpon destructans and/or Botrytis cinerea [10]. However, the preventive effect of individual strains is unstable, the spectrum of bacterial inhibition is narrower, and the combined use of bacterial agents to control ginseng diseases is a more reasonable and safer method [11]. The application of corn straw biochar and actinomycetes Frankia F1 to prepare composite microbial inoculum results in a better biocontrol effect in ginseng [12]. The combination of bioinoculants is an effective way to control ginseng diseases; however, the combination of more effective microbial agents needs to be screened and the mechanism needs to be clarified. Microorganisms play an important role in promoting ginseng growth. For example, Arthrobacter nicotinicola strain JI39 effectively promotes the growth of ginseng and has the potential to be a good microbial fertiliser for ginseng [13]. Moreover, the endophytic B. cereus promotes the growth of ginseng by increasing the content of IAA [14]; The ginseng endophyte Pseudomonas fluorescens can also promote the growth of ginseng [15]. The combination of microbial agents has a better growth-promoting effect on ginseng, and the combination of Bacillus subtilis, Bacillus amyloliquefaciens, and Paenibacillus mucilaginosus significantly increases the dry weights of Page 2 of 20 ginseng roots [16]. The combination of biological agents is an effective way to promote the growth of ginseng, but t (...truncated)