Positive feedback effect of rhizosphere Bacillus on the growth and defense of Ageratina adenophora

Abstract

Background: The formation of symbiotic relationships between invasive plants and soil microorganisms in invaded regions, which enhances their adaptive capacity has been extensively studied. Bacillus, as a representative soil beneficial microorganism, can be recruited by invasive plants to their rhizosphere to promote growth. However, it remains unclear how dominant Bacillus species in the rhizosphere changes, and what feedback effects these changes may have, when invasive plants encounter biotic resistance in the invaded region, particularly from plant competition and insect herbivory.

Results: This study investigated the contents of Bacillus idriensis, B. mycoides, B. thuringiensis in the rhizosphere soil of Ageratina adenophora under different biotic resistance. It showed that B. idriensis exhibited the highest increase in the rhizosphere during plant competition, whereas B. thuringiensis showed the most significant increase under Aphis gossypii infestation. The effect of these Bacillus species on the competitive interactions between A. adenophora and native plant Rabdosia amethystoides were assessed. Inoculation with B. idriensis led to an 185.66% increase in biomass for monocultured A. adenophora and a 175.83% increase in mixed culture, thereby enhancing the positive effect of interspecific competition on the growth of A. adenophora. Additionally, the responses of A. adenophora to infestation by the generalist herbivorous A . gossypii following Bacillus inoculation were examined. B.thuringiensis inoculated significantly increased the levels of jasmonic acid, total phenols, flavonoids in A. adenophora infested by A. gossypii by 49.38%, 20.78%, 18.59%, while significantly reducing the survival rate and nymph density of A. gossypii, indicating enhanced resistance to the herbivore. B. idriensis improved the tolerance of A. adenophora to A. gossypii through growth promotion.

Conclusion: Our findings demonstrate that the abundance of distinct Bacillus species in the rhizosphere of A. adenophora varies in response to diverse biotic resistance encountered in the invaded region. These rhizobacterial interactions generate specific feedback effects that collectively enhance the invasiveness of the species.

Keywords: Ageratina adenophora; Bacillus; Biotic resistance; Defense-growth tradeoffs; Feedback.

Fig. 1

Variation of three Bacillus (a, B. idriensis, b, B. mycoides, c, B. thuringiensis) content in rhizosphere soil for A. adenophora in different biotic resistance sites. C, non-invaded soil; A, dominated by A. adenophora soil; AC, A. adenophora competition with native plants soil; AG, A. adenophora infested by A. gossypii soil. Different lowercase letters represent significant difference among different biotic resistance soil (LSD’s test, P < 0.05). Data are means ± SD (n = 5)

Fig. 2

Effect of competition and inoculum on the plant biomass of invasive plant A. adenophora (a) and native plant R. amethystoides (b) when grown in monoculture or in mixture. C, non-inoculation treatment; BI, inoculated with B. idriensis; BM, inoculated with B. mycoides; BT, inoculated with B. thuringiensis. Bars with different lowercase letters represent significant differences between the inoculation treatments by LSD test (P < 0.05). Bars with different uppercase letters represent significant differences between monoculture and mixture at P < 0.05. Data are means ± SD (n = 5)

Fig. 3

Effect of Bacillus on the corrected index of relative competition intensity (CRCI) of invasive plant A. adenophora (a) and native plant R. amethystoides (b). C, non-inoculation treatment; BI, inoculated with B. idriensis; BM, inoculated with B. mycoides; BT, inoculated with B. thuringiensis. Different lowercase letters indicate significant differences among the inoculation treatments at P < 0.05. Data are means ± SD (n = 5)

Fig. 4

Effect of competition and inoculum on C concentration, N concentration and P concentration of A. adenophora (a-c) and R. amethystoides (d-f) when grown in monoculture or in mixture. C, non-inoculation treatment; BI, inoculated with B. idriensis; BM, inoculated with B. mycoides; BT, inoculated with B. thuringiensis. Bars with different lowercase letters represent significant differences between the inoculation treatments by LSD test (P < 0.05). Bars with different uppercase letters represent significant differences between monoculture and mixture at P < 0.05. Data are means ± SD (n = 5)

Fig. 5

Effect of competition and inoculum on Bacillus density of A. adenophora (a) and R. amethystoides (d) when grown in monoculture or in mixture. C, non-inoculation treatment; BI, inoculated with B. idriensis; BM, inoculated with B. mycoides; BT, inoculated with B. thuringiensis. Bars with different lowercase letters represent significant differences between the inoculation treatments by LSD test (P < 0.05). Bars with different uppercase letters represent significant differences between monoculture and mixture at P < 0.05. Data are means ± SD (n = 5)

Fig. 6

Effect of inoculum and A. gossypii treatment on the biomass of A. adenophora. C, non-inoculation treatment; BI, inoculated with B. idriensis; BM, inoculated with B. mycoides; BT, inoculated with B. thuringiensis. Different letters in lowercase indicate significant differences between four treatments at P < 0.05. Different uppercase letters indicate significant different between treatments with or without A. gossypii infestation at P < 0.05. Data are means ± SD (n = 5)

Fig. 7

Effect of inoculum and A. gossypii treatment on the activity of PAL (a), PPO (b), POD (c) and SOD (d) of A. adenophora. C, non-inoculation treatment; BI, inoculated with B. idriensis; BM, inoculated with B. mycoides; BT, inoculated with B. thuringiensis. Bars with different lowercase letters represent significant differences between the inoculation treatments by LSD test (P < 0.05). Bars with different uppercase letters represent significant differences between treatments with or without A. gossypii infestation at P < 0.05. Data are means ± SD (n = 5)

Fig. 8

Effect of inoculum and A. gossypii treatment on the concentration of jamonic acid (a) and salicylic acid (b) of A. adenophora. C, non-inoculation treatment; BI, inoculated with B. idriensis; BM, inoculated with B. mycoides; BT, inoculated with B. thuringiensis. Different letters in lowercase indicate significant differences between four treatments at P < 0.05. Different uppercase letters indicate significant different between treatments with or without A. gossypii infestation at P < 0.05. Error bars represent ± 1SE of mean. Data are means ± SD (n = 5)

Fig. 9

Effect of inoculum and A. gossypii treatment on the concentration of secondary metabolite (a-c) of A. adenophora. C, non-inoculation treatment; BI, inoculated with B. idriensis; BM, inoculated with B. mycoides; BT, inoculated with B. thuringiensis. Bars with different lowercase letters represent significant differences between the inoculation treatments by LSD test (P < 0.05). Bars with different uppercase letters represent significant differences between treatments with or without A. gossypii infestation at P < 0.05. Data are means ± SD (n = 5)

Fig. 10

Effect of inoculum and A. gossypii treatment on the Bacillus density of A. adenophora. C, non-inoculation treatment; BI, inoculated with B. idriensis; BM, inoculated with B. mycoides; BT, inoculated with B. thuringiensis. Bars with different lowercase letters represent significant differences between the inoculation treatments by LSD test (P < 0.05). Bars with different uppercase letters represent significant differences between treatments with or without A. gossypii infestation at P < 0.05. Data are means ± SD (n = 5)

Fig. 11

Effect of inoculum on the A. gossypii survival and densities of nymphs. C, non-inoculation treatment; BI, inoculated with B. idriensis; BM, inoculated with B. mycoides; BT, inoculated with B. thuringiensis. Different letters in lowercase indicate significant differences between four treatments at P < 0.05. Data are means ± SD (n = 5)