Volatile compounds mediated effects of Stenotrophomonas maltophilia strain UN1512 in plant growth promotion and its potential for the biocontrol of Colletotrichum nymphaeae

https://doi.org/10.1016/j.pmpp.2020.101555Get rights and content

Highlights

  • Strain UN1512 was isolated from healthy strawberry leaves and was identified as Stenotrophomonas maltophilia.

  • Strain UN1512 inhibited growth of Colletotrichum nymphaeae under in vitro, in vivo and greenhouse conditions.

  • Strain UN1512 produced VOCs with plant growth promotion properties.

  • VOCs produced by strain UN1512 was identified by GC-MS.

Abstract

A novel endophytic bacterium, designated strain UN1512, was isolated from strawberry leaves, and its antifungal activity against Colletotrichum nymphaeae was estimated under in vitro, in vivo, and greenhouse conditions. The bacterial isolate was identified as Stenotrophomonas maltophilia via morphological, biochemical, and molecular traits. The strain UN1512 decreased the mycelial growth of C. nymphaeae (54.92%) in dual culture. The volatile and non-volatile compounds produced by strain UN1512 reduced mycelial growth of fungal pathogen by 17.85% and 30.06%, respectively. Also, the strain was able to secrete of protease, chitinase, pectinase, siderophore, IAA, and gibberellin. In addition, disease severity of strawberry anthracnose was inhibited via inoculating the bacterial suspension in phylloplane, rhizosphere, and healthy fruits. Also, the effect of volatile compounds (VOCs) produced by strain UN1512 on growth promotion of tomato plants was investigated under in vitro and growth chamber experiments. The results showed that, these compounds significantly enhance the fresh weight and length of roots and shoots. The VOCs produced by strain UN1512 were analyzed by GC-MS and 31 identified VOCs, that Benzothiazole (18.271%), 1,3,5,7-Cyclooctatetraene-1-carboxaldehyde (9.308%), Carbonic acid, octadecyl phenyl ester (5.203%), Benzaldehyde, 2,5-bis[(trimethylsilyl)oxy]- (4.086%), Estragole (3.557%), Benzaldehyde (3.506%) were the major components. Our studies report that strain UN1512 was capable to inhibit the causal agent strawberry anthracnose, and the VOCs produced by this strain increased the tomato seedlings growth.

Introduction

Nowadays, a various chemical fungicides used in disease management of phytopathogens. A lot of researches are being done to find an environmentally friendly alternative method [1]. According to this trend, bacteria could have demonstrated as an alternative method to apply in crop protection via the production of phytohormones, lytic enzymes, siderophore, and secretion of antifungal metabolites [2]. Many studies have been performed with endophytic bacteria as potential biological control agents (BCAs) of some fungal disease [[3], [4], [5], [6]]. Plant growth promoting rhizobacteria (PGPR) produces volatile organic compounds (VOCs) that are capable to control phytopathogens, increase plant growth, and induce systemic resistance. Some of the bacterial species, including Bacillus, Pseudomonas, Serratia, Arthrobacter, and Stenotrophomonas, produce VOCs that promote plant growth [7]. Zou et al. [8] illustrated that Bacillus megaterium strain XTBG34 emits 2-pentylfuran which increases the growth of Arabidopsis thaliana. Also, it has been reported that Acetoin and 2,3-butanediol produced by Bacillus spp. improves plant growth in Arabidopsis [9]. Furthermore, the growth of Nicotiana tabacum was promoted by 13-tetradecadien-1-ol, 2-butanone, and 2-methyl-n-1-tridecene, from Pseudomonas fluorescens strain SS101 [10]. These bacteria stimulate plant growth by modulating plant hormones (auxins, gibberellins, ethylene and cytokinins) and enhancing the availability of N, P, and Fe. The VOCs that produced by bacteria increase plant growth through interacting with plant hormones [7]. Stenotrophomonas maltophilia is an aerobic and Gram -negative bacterium common in the environment. This species frequently isolated from the rhizosphere of wheat, oat, cucumber, maize, and potato. S. maltophilia indicates plant growth promoting properties and biocontrol activity against phytopathogens [11]. It has been reported that S. maltophilia strain W81 inhibited the growth of the Pythium ultimum [12]. Zhang and Yuen [13] indicated that S. maltophilia strain C3 decreased growth of Bipolaris sorokiniana in turfgrass, and it has been also demonstrated, that S. maltophilia significantly suppressed Ralstonia solanacearum [14].

In the present study according to the importance of controlling Colletotrichum nymphaeae causal agent of strawberry anthracnose, we isolated the antagonistic endophytic bacterium S. maltophilia strain UN1512 (GenBank accession no. MT448956) from healthy strawberry plants and its antagonistic activity against C. nymphaeae was investigated under in vitro, in vivo, and greenhouse conditions. Then, we investigated the effect of VOCs from this bacterium on plant growth promotion and identified these compounds by GC-MS. To the best of our knowledge, this is the first document on the efficacy of S. maltophilia against strawberry anthracnose disease.

Section snippets

Selection and characterization of bacterial strain

The endophytic bacterial strain was isolated from the healthy strawberry leaf in Kamyaran, Kurdistan province. Leaves of collected plants were surface sterilized and macerated in sterile distilled water, then 50 μl was cultured on nutrient agar (NA) medium. The water from the last rinse of samples was used to evaluate of sterilization. The initial characterization of strain UN1512 was performed according to morphological, physiological and biochemical tests [15,16]. For identification of the

Identification of bacterial strain UN1512

Biochemical traits displayed that strain UN1512 was positive for catalase, lipase, and negative for oxidase, and HCN production. Also, this strain able to nitrogen fixation, phosphate solubilization, and produce lytic enzymes such as protease, chitinase, pectinase and secret siderophore, IAA (5065 μg/L) and GA (12991.4 μg/L). The hypersensitive response test demonstrated that the endophytic bacterial strain did not cause symptoms in the tobacco leaf and strawberry fruit (Table 1). Based on

Discussion

For the first time, a novel strain of S. maltophilia was showed that suppressed C. nymphaeae growth under in vitro, in vivo and in greenhouse experiments. The strain was able to produce chitinase, protease, pectinase, and siderophore. The results of dual culture, VOCs and non-VOCs tests revealed that this strain inhibits the growth of the C. nymphaeae. These findings demonstrate a possible secretion of lytic enzymes, siderophore, volatile and non-volatile metabolites responsible for such

Conclusions

In conclusion, this study shows that the strain UN1512 produced lytic enzymes, including chitinase, pectinase, and protease and also produced siderophore, IAA and GA. The growth of mycelium, conidial germination, and disease severity of strawberry anthracnose were suppressed by this strain. The potential of the strain UN1512 could be due to several mechanisms such as presence of lytic enzymes, siderophore and antifungal metabolites. This investigate represented the relationship between VOCs

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgment

This research was supported by the Department of Plant Protection, University of Kurdistan, Iran (Grant No: 96/19/30039).

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