Inhibition and biocontrol potential of Ochrobactrum pseudogrignonense NC1 against four Phytophthora species

doi:10.21203/rs.3.rs-2980205/v1

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Inhibition and biocontrol potential of Ochrobactrum pseudogrignonense NC1 against four Phytophthora species

https://doi.org/10.21203/rs.3.rs-2980205/v1

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Phytophthora species are highly destructive soilborne oomycetes pathogens that spread through infested soil and water. Ochrobactrum pseudogrignonense NC1 has been shown to inhibit plant parasitic nematodes via volatile organic compounds (VOCs). In this study, we investigated the inhibitory effect of O. pseudogrignonense NC1 against four Phytophthora species on agar plates and in vivo bioassay. We found that NC1 significantly inhibited the mycelial growth and zoospore production of all four species of Phytophthora in a dose-dependent manner. The half maximal inhibitory concentration (IC₅₀) values for inhibition of mycelial growth (or zoospore production) were 26.0% (14.8%), 18.9% (14.2%), 20.3% (8.3%) and 46.9% (4%) for Phytophthora capsici Leonian, Phytophthora infestans, Phytophthora parasitica var. nicotiana and Phytophthora sojae, respectively. The biocontrol efficiency of NC1 was 46.3% in pepper seedlings against P. capsici, almost 100% in potato tubers against P. infestans, 60% in tomato leave against P. parasitica and 100% in soybean leave against P. sojae, respectively. Our findings suggest that O. pseudogrignonense NC1 has great potential as a biocontrol agent for managing Phytophthora diseases.

Phytophthora

biological control

Ochrobactrum pseudogrignonense

crop diseases

Soil-borne diseases are a crucial type of agricultural production disease that leads to significant crop yield losses, negatively impacting global food safety and the economy (Derevnina et al., 2016; Savary et al., 2019; Khadka et al., 2020; Wang et al., 2020). Phytophthora, a genus containing around 140 species, is among the most destructive soil-borne plant pathogens worldwide, posing a significant threat to crop security. A number of diseases such as chestnut ink disease, potato late blight, tobacco black shank and soybean stem rot that are caused by Phytophthora cinnamomi, P. infestans, Phytophthora nicotiana, P. sojae, respectively, are resulted in substantial economic losses (Choupina et al., 2014; Kamoun et al., 2015).

Extensive researches to control the diseases caused by Phytophthora have conducted around the world and chemical control measures are widely used for their high and quick efficiency. However, persistent resistance of host plants is difficult to maintain, and the lack of effective fungicides for Phytophthora makes disease control challenging. Biological control, which involves the use of organisms or their metabolites to control or reduce the degree of harm to plants or animals, is an efficient and sustainable method to control crop diseases. Screening for new biocontrol microbes, including fungi, actinomycetes, bacteria and viruses, is provital in the biocontrol of plant diseases (Naing et al., 2014).

Several studies have shown the effectiveness of biological control agents in controlling plant diseases caused by Phytophthora. Pseudomonas strains that produce biosurfactants have been shown to enhance biological control of Phytophthora blight in pepper (Kim et al., 2000; Nielsen et al., 2006; Ümit & Kemal, 2013). A Trichoderma atroviride strain isolated from the strawberry tree has also been found to be effective against P. cinnamomi, reducing its growth by about 80% (Martins et al., 2022). Additionally, Bacillus species are used in controlling various Phytophthora spp. (de Andrade Lourenco et al., 2022).

Bacterial volatiles are considered a promising source for developing natural compounds that can protect plants from disease or promote plant growth (Kai et al., 2009). Agrobacterium, Alcaligenes, Bacillus, Pseudomonas, Serratia, Streptomyces and Xanthomonas, are some of the more frequent biological VOC producers. Bacillus species are of particular interest because they inhibit fungal growth (Chaurasia et al., 2005; Yuan et al., 2012; Baysal et al., 2013) and contribute to the biocontrol of plant diseases via VOCs (Chaurasia et al., 2005). Soil bacteria have been reported to produce VOCs that antagonize phytopathogenic fungi belonging to various genera, such as Alternaria, Aspergillus, Botrytis, Colletotrichum, Fusarium, Pythium, Rhizoctonia, Sclerotini, and Verticillium (Chaurasia et al., 2005; Kai et al., 2007; Ren et al., 2010; Zheng et al., 2013).

Ochrobactrum pseudogrignonense NC1 was isolated from the rhizosphere soil of a healthy tomato and has been well documented to kill nematodes via VOCs of dimethyl disulfide (DMDS) and benzaldehyde (Yang et al., 2022). DMDS is a widely used sulfur organic compound which is effectiveness in controlling root-knot nematodes and soil pathogens (Gomez-Tenorio et al., 2015). Benzaldehyde, on the other hand, is a potent bactericide (Ullah et al., 2015). Therefore, we hypothesized that this strain may also have good activity in inhibiting other crop pathogens, especially Phytophthora spp. Therefore, we investigated inhibition of mycelium growth and zoospore production of four Phytophthora species and biocontrol potential in vivo by NC1.

Cultures of Ochrobactrum pseudogrignonense and Phytophthora species

O. pseudogrignonense NC1 used in this experiment was isolated from the rhizosphere of healthy tomatoes and deposited at the China General Microbiological Culture Collection Center (CGMCC No.12154). The liquid culture and fermentation filtrate of NC1 were prepared following Xiang et al. (2019). Phytophthora infestans (Pi) and Phytophthora sojae (Ps) were provided by the Plant Protection Institute, Hebei Academy of Agricultural Sciences and cultured on Rye Sucrose Agar (RSA) and Carrot Agar (CA) plates respectively. Phytophthora capsici Leonian (Pc, ACCC 37300) and Phytophthora parasitica var. nicotiana (Pp, ACCC 38065) were obtained from the Agricultural Culture Collection of China and cultured on Potato Dextrose Agar (PDA) plates.

Inhibition of mycelium growth and zoospore production of Phytophthora by NC1

The growth inhibition assay was carried out using the two-sealed-base-plates method described by Méndez-Bravo et al. (2018). In brief, NC1 was streaked onto Nutrient Agar (NA) medium in the bottom of a petri dish, and after 2 days, a 5 mm mycelial plug of each Phytophthora species was placed in the center of the bottom of another petri dish containing PDA, RSA or CA. These two petri dishes were sealed with parafilm. Control was setup as same as those treatment except without NC1 inoculation. Four replicates per treatment were cultured in the incubator at 25℃ (18℃ for Pi). After 10 days of incubation, colony diameter was measured and inhibition rate was calculated. The zoospore concentration was determined with a hemocytometer and inhibition rate of zoospore production was calculated.

Determination of IC₅₀ value

Agar plates were prepared to containing NC1 fermented filtrate at 0%, 2%, 10%, and 20% (0%, 5%, 10%, 20%, 30% for Pc), respectively. A 5 mm colony plug of Phytophthora culture was inoculated into the center of agar plate. Four replicates were setup for each treatment. After 10 days of incubation, colony diameter was measured. Zoospore suspension was prepared using the method described by Zheng (1997) and zoospore concentrations were determined with a hemocytometer. IC₅₀ values and regression equations were calculated for inhibition of mycelial growth and zoospore production.

Biocontrol efficiency of four Phytophthora species by NC1

Seeds of the "Xiangyan 15" cultivar of chilli pepper (Capsicum annuum L.) were surface sterilized and germinated in sterile vermiculite before being transplanted into pots containing field soil. Three weeks after transplanting one plant to each pot, five 5 mm mycelial plugs of Pc were inoculated into the stem base of each plant and 1 mL of NC1 fermentation liquid (NC1-Pc) or sterile water (CK-Pc) were injected at the same time for each pot. The plants were monitored for disease symptoms after inoculation of 21 days, and disease index was calculated based on the classification standard of the Ministry of Agriculture of China. Plant biomass was measured at the end of the experiment. For potato late blight, commercially available potatoes were purchased from grocery store and surface disinfected with 2% sodium hypochlorite for 2 mins, then rinsed with sterile distilled water and air-dried (Elsherbiny et al., 2020). 5 mm colony plug of Pi was inoculated onto the potato where 1 cm² square was wounded by a sterilized scalpel (CK-Pi) and total of 1 mL NC1 suspension was pipetted onto wounded area in five separate times (200 µL each time) (NC1-Pi). Five inoculation area for each potato and seven replicates for each treatment were applied. The potatoes were observed for rust brown lesions after 14 days of inoculation. This experiment was conducted at room temperature 25℃.

Seeds of soybean "Sturdy" cultivar and tomato “Hezuo 913” cultivar were surface sterilized with 3% sodium hypochlorite for 3 mins and washed thrice with sterilized water. Then seeds were placed into sterile vermiculite and germinated at room temperature for 5 days. After three weeks of transplanting, healthy leaves of soybean or tomato at the same age were selected and a 5 mm colony plug of Ps or Pp were inoculated onto the leave respectively. 1 mL of NC1 fermentation liquid (NC1-Ps/NC1-Pp) or 1 mL sterile water (CK-Ps/CK-Pp) were sprayed onto the leave surface and kept at 25℃. The disease area of soybean leaves was measured at 7, 10, and 14 days with six replicates. Disease incidence of tomato leaves was determined at 14 days with ten replicates. We also explore the growth-promoting effect of the NC1 on soybean and tomato seedlings after 14 days of transplanting with 16 replicates.

Statistics analysis

Statistical analysis of Phytophthora mycelial growth and zoospore production were conducted using R software (Version 4.1.1). Wilcox test or t-test was used to assess the difference between the “Exposed to VOCs” and “Control”. IC₅₀ value and regression equations were analyzed with Excel (2016). The diameter and zoospore concentration of four Phytophthora species under different concentrations of NC1 fermentation liquid filtrate were analyzed using one-way ANOVA in GraphPad Prism 8.3. T-test was performed for the in vivo assay. Statistical analysis was considered significance at P < 0.05. (Data are available in supplementary materials)

VOCs produced by NC1 inhibit the radial mycelial growth, and decrease zoospore concentration

VOCs produced by NC1 effectively inhibit the radial mycelial growth of P. capsici, P. infestans, P. sojae and the aerial hyphae growth of P. parasitica (Fig. 1a, b), with growth inhibition of 36.75%, 100%, 41.79% and 18.42%, respectively (Table 1), while having no significant effect on basal hyphae growth of P. parasitica. Additionally, the zoospore concentration of the four Phytophthora species was significantly lower than that of the control, indicating that VOCs have a negative impact on zoospore production (Fig. 1c). P. infestans as the most sensitive to VOCs, with zoospores being more susceptible than hyphae of all four Phytophthora species (Table 1). The inhibition of zoospore production by VOCs was 97.75% (Pc), 100% (Pi), 95.26% (Pp), 75.50% (Ps), respectively (Table 1). Furthermore, our findings show that NC1 inhibits hyphae growth and zoospore production in a dosage-dependent manner, with significant inhibition observed at different concentrations of the NC1 fermentation liquid filtrate (Fig. 3, Fig. 4).

Table 1

The inhibitory rate of NCl VOCs on mycelial growth and zoospore production of four Phytophthora species
	Mycelial growth inhibition rate (± SE) (%)	Zoospore production inhibition rate (± SE) (%)
P. infestans	100	100
P. sojae	41.79 ± 3.61	75.50 ± 4.63
P. parasitica var. nicotianae	18.42 ± 8.74	95.26 ± 0.87
P. capsici Leonian	36.75 ± 9.14	97.75 ± 0.85

IC₅₀ value of NC1 on Phytophthora mycelial growth and zoospore production

The IC₅₀ values, indicating the concentration at which 50% inhibition of mycelial growth occurred, were found to be 26.0% (Pc), 18.9% (Pi), 20.3% (Pp) and 46.9% (Ps), respectively (Table 2). For inhibition of zoospore production, the IC₅₀ values were found to be 14.8% (Pc), 14.2% (Pi), 8.3% (Pp), and 4.0% (Ps), respectively (Table 3). The radial mycelial growth was observed to decrease with increasing concentrations of NC1 fermentation liquid filtrate (Fig. 2). The diameter of P. sojae was significantly reduced compared to the control at 2% concentration (Fig. 3d), while P. infestans and P. capsici showed inhibition at 10% concentration (Fig. 3a, b). All tested Phytophthora species were significantly inhibited at 20% concentration (Fig. 3a, b, c, d). The zoospore concentrations of P. sojae and P. perasitica were significantly reduced compared to the control at 2% concentration (Fig. 4c, d), all tested Phytophthora species were significantly inhibited at 20% concentration (Fig. 4a, b, c, d).

Table 2

Regression equation and IC50 value of colony diameter
	Regression equation	Correlation coefficient (R²)	IC₅₀ value
^*P. infestans	y = 19.907x-8.5539	0.9975	18.9%
^*P. sojae	y = 9.9365x + 11.755	0.9995	46.9%
P. perasitica var. nicotiana	y = 1.8852x + 11.674	0.9999	20.3%
P. capsici Leonian	y = 2.2024x − 7.2917	0.9269	26.0%
^* Indicate that x in the regression equation is logarithmically transformed

Table 3

Regression equation and IC50 value of zoospore production
	Regression equation	Correlation coefficient (R²)	IC₅₀ value
P. infestans	y = 2.5232x + 14.25	0.9234	14.2%
^*P. sojae	y = 20.8x + 21.043	0.9996	4.0%
P. perasitica var. nicotiana	y = 2.6203x + 28.253	0.9653	8.3%
P. capsici Leonian	y = 4.9672x − 23.394	0.9857	14.8%
^* Indicate that x in the regression equation is logarithmically transformed

Crop disease resistance experiment: evaluating the disease control efficiency of NC1 against Phytophthora

Inoculation with NC1 fermentation liquid significantly decreased the disease severity of chilli pepper seedlings compared to the control group (sterile water) (Fig. 5a, b), and the most serious disease index occurred in the control group, in which after 21 days of infection, the disease index of chilli pepper seedlings was 76.3%, significantly higher than that of the NC1 group (30%). At each recording time (days 10, 14, and 21), the disease index for the control group was significantly higher than that for the NC1 group (Fig. 5b). Additionally, NC1 had an obvious effect on promoting plant growth, there was strongly positive responses of NC1 inoculation on parameters of plant growth (shoot biomass, root biomass, total biomass, and root/shoot ratio) compared to the control group (Fig. 5c, d, e, f). These results indicate that NC1 can significantly promote the growth and resistance of chilli pepper seedlings to Phytophthora disease.

In another experiment involving potato tuber infection, the late blight of potato tuber was significantly alleviated after inoculation with NC1 fermentation liquid (Fig. 6). After 14 days of infection with P. infestans, few rust brown lesions were observed under the epidermal layer of all the tubers that received NC1 treatment, while the disease incidence of the control group reached 100%.

A pot experiment was performed to evaluate the effectiveness of NC1 fermentation liquid on the growth of soybean seedlings. Plant height of soybean seedlings significantly increased with NC1 inoculation compared to sterile water treatment, although biomass did not change significantly (Fig. 7a, b, c). NC1 fermentation liquid significantly reduced phytophthora disease severity in soybean leaves. The disease index of the control group reached 87.8% on the 14th day, while leaves treated with NC1 fermentation liquid showed no obvious disease symptoms (Fig. 7d, e). Combining all results, we conclude that NC1 can effectively protect soybean leaves from infection by P. sojae while playing a role in promoting growth.

In the experiment to evaluate the effect of NC1 fermentation liquid on the growth of tomato seedlings, plant total biomass and height were effectively improved after inoculated with NC1 fermentation liquid compared with sterile water (Fig. 8a, c, d). It could also control P. parasitica disease on tomato leaves effectively. After 14 days of infection, the disease incidence of tomato leaves in the control group was 80%, four times as many as the NC1 group (20%) (Fig. 8b).

The study presented the potential of O. pseudogrignonense in inhibiting the growth of four Phytophthora species and controlling diseases caused by P. capsici, P. infestans, P. parasitica and P. sojae in pepper seedlings, potato tuber, tomato leaf and soybean leaf, respectively.

The study focused on the VOCs produced by O. pseudogrignonense NC1, which has been previously shown to inhibit plant parasitic nematodes. It is a naturally occurring environmental organism that exists in water and soil (Kettaneh et al., 2003). The study proved that the VOCs of NC1 significantly decreased the zoospore production and colony diameters of four Phytophthora species, showing its potential in inhibiting the growth of Phytophthora. Bacterial VOCs have been studied for their potential to suppress pathogens, and some of the most studied biocontrol bacteria are Pseudomonas spp. (Andrews, 1992) and Bacillus spp. (Saxena et al., 2020). NC1 was isolated from healthy tomato roots, which belongs to "plant microbiomes," perceived as potential sources of biological control against plant pathogens. The beneficial plant-associated bacteria can suppress harmful pathogens by producing secondary metabolites, and VOCs have been proven to display inhibitory effects on several plant pathogens. (Sheoran et al., 2015; Munjal et al., 2016; Wang et al., 2016; Toffano et al., 2017; Agisha et al., 2019; Patel et al., 2021).

Biocontrol of microorganisms is attributable to specific VOCs such as ammonia, cyanide, and sulfur-containing metabolites (DMDS, dimethyl trisulphide). This study showed that the two VOCs produced by the NC1, DMDS, and benzaldehyde, have potential anti-phytophthora properties. Although O. pseudogrignonense is known to cause diseases in humans (Ryan et al., 2020), the study is the first to demonstrate the anti-phytophthora properties of NC1 VOCs. Recently, bacterial VOCs-mediated suppression of pathogens was deemed a characteristic for the selection of new biocontrol agents. This study also demonstrated that the biocontrol efficiency of NC1 was 46.3% in pepper seedlings against P. capsici, almost 100% in potato tubers against P. infestans, 60% in tomato leave against P. parasitica and 100% in soybean leave against P. sojae, respectively, showing its potential as a new biological control agents.

Fungicides have been used to control Phytophthora crop diseases, but they cause ecological pollution, threaten human health, and destroy beneficial bacteria in the soil. Biocontrollers such as Bacillus, Pseudomonas, Streptomyces, Trichoderma and some yeasts species have been reported (Quispe-Quispe et al., 2022; Volynchikova & Kim, 2022). Bacillus vallismortis BS07 has been proven against Phytophthora blight effectively (Majid et al., 2016). Ezziyyani et al. (2007) use Trichoderma harzianum to reduce the necrosis of the chili plant successfully. Lee et al. (2003) proved that two strains of Pseudomonas corrugata: CCR04 and CCR80 resided in chili roots and effectively suppressed Phytophthora blight disease compared to Escherichia coli DH5α. Cheng et al. (2022) discovered that ferroptosis induced by the biocontrol agent Pythium oligandrum could enhance soybean resistance to P. sojae. The study adds to this list and demonstrates the potential of O. pseudogrignonense as a biological control agent against Phytophthora blight.

In the in vivo assay, for example, soybean disease caused by P. sojae, can occur during all development stages (Yu et al., 2022), and as the disease progresses, the leaves become yellow or brown, just as what our results have shown, and NC1 fermentation liquid promote soybean growth while playing the role of biocontrol. However, in vivo experiments are limited in their coverage of environmental factors. They may not even represent natural biological control effect. Still, some cases, a decrease or loss of biocontrol efficacy was usually caused by a lack of direct interaction between biocontrol bacteria and pathogen or low colonization activity in nature (Volynchikova & Kim, 2022). Therefore, in vivo biological control tests remain important. Morrison et al. (2017) assessed the biocontrol efficiency of the antibiotic phenzine-1-carboxylic acid-producing Pseudomonas fluorescens LBUM636 in tuber and growth chamber assays. Interestingly, strong consistency protection effect was observed.

Our research first proved O. pseudogrignonense NC1 was a new biocontrol bacterium that directly inhibited the growth of the four Phytophthora species and provided protection to pepper, potato, soybean and tomato against phytophthora diseases. Future studies should consider the efficacy of NC1 in field conditions, as well as the long-term effects on soil microbial communities, combined with various biological control microorganisms or stimulators, such as root exudates, and composts, which may enhance the biological control.

Acknowledgements

This research was jointly supported by the National Key R&D Program of China (2022YFD1400700), the National Natural Science Foundation of China (32201402), the Fundamental Research Funds for the Central Universities, Nankai University (63211053) and the start-up funding from Nankai University for Prof. Xingzhong Liu (030/C029215002).

Conflict of interest All authors declare no conflict of interest.

Informed consent All authors have reviewed the manuscript and approved its submission to the European Journal of Plant Pathology.

Ethics approval Not applicable

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Inhibition and biocontrol potential of Ochrobactrum pseudogrignonense NC1 against four Phytophthora species

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Abstract

Figures

Introduction

Materials and methods

Statistics analysis

Results

VOCs produced by NC1 inhibit the radial mycelial growth, and decrease zoospore concentration

IC₅₀ value of NC1 on Phytophthora mycelial growth and zoospore production

Crop disease resistance experiment: evaluating the disease control efficiency of NC1 against Phytophthora

Discussion

Conclusion

Declarations

References

Supplementary Files

Status:

Version 1

Inhibition and biocontrol potential of Ochrobactrum pseudogrignonense NC1 against four Phytophthora species

Status:

Version 1

Abstract

Figures

Introduction

Materials and methods

Statistics analysis

Results

VOCs produced by NC1 inhibit the radial mycelial growth, and decrease zoospore concentration

IC50 value of NC1 on Phytophthora mycelial growth and zoospore production

Crop disease resistance experiment: evaluating the disease control efficiency of NC1 against Phytophthora

Discussion

Conclusion

Declarations

References

Supplementary Files

Status:

Version 1

IC₅₀ value of NC1 on Phytophthora mycelial growth and zoospore production