3.1 Effects of strain WSW007 inoculation and VOCs on growth of plant
In the growth tests (Table 1), the growth of tobacco seedlings was significantly inhibited. At low concentration (10 CFU/mL), inoculation of strain WSW007 in 24-well plate showed no difference in the growth of tobacco compared with the control. As the concentration increased, the growth of tobacco was gradually inhibited from 1.0×103 CFU/mL and the inhibitory effect was strongest at 1.0×107 CFU/mL and 1.0×109 CFU/mL, and there was no significant difference between them. Compared with the control, the tobacco leaves were yellowish, the plants were short and the root growth length was shorter. These results showed that suspension of WSW007 had no effect on tobacco growth at low concentrations, but inhibited tobacco growth at high concentration. In I-plates, with the increase of VOCs concentration of strain WSW007, the growth promotion effect on tobacco was increased, the total fresh weight of tobacco seedlings co-incubated with strain WSW007 using two sterile filter paper (40 ml inoculant) plates remained stable after reaching the highest level, significantly increasing to 143% (Fig. 1).
Table 1. Growth promoting of tobacco by WSW007 inoculation different concentration
Treatment
|
Inoculation with WSW007 at concentration of (CFU/mL)*
|
0 (CK)
|
10
|
1.0×103
|
1.0×105
|
1.0×107
|
1.0×109
|
Total fresh weight (g)
|
0.082±
0.0027a
|
0.076±
0.0006a
|
0.056±
0.0012b
|
0.05±
0.0009b
|
0.04±
0.0037b
|
0.035±
0.0012b
|
Decrease
|
-
|
7.3%
|
31.7%
|
39%
|
51.2%
|
57.3%
|
*. Each plant was inoculated on roots with 20 ml of B. velezensis suspension. The same letter followed the values in the same column means no significant difference based on the least significant difference (LSD) test (p < 0.05).
3.2 PGP traits of Bacillus velezensis WSW007
Strain WSW007 produced 14.86 mg/ml IAA in the culture and grew slowly and weakly on PKO medium. After 2-7 days of incubation on PKO medium, the colonies gradually expanded, and the phosphate solubilizing ring gradually appeared, but not obvious and it remained unchanged after 7 days. On organophosphorus medium, strain WSW007 presented a more obvious dissolving effect. After 7 days of incubation, the solubilization ring was very obvious (SI = 1.25), and it continuously expanded until the entire plate became almost transparent. On CAS medium, colonies of strain WSW007 began to grow after 5 days of incubation, with the appearance of yellow circles, evidencing the production of siderophore. After 14 days of incubation, the solubilization ring was very obvious (SI = 2.2). Detailed results for PGP traits of B. velezensis WSW007 are available in (Fig. 2).
3.3 Transcriptomal analysis of tobacco plants responding to VOCs
In transcriptomal analysis, 38011 genes were detected in the plants co-cultured with strain WSW007 and 37636 genes were detected in the control plants. Analysis of RNAseq data revealed 3065 differentially expressed transcripts (DEGs) induced by VOCs of strain WSW007, including 1975 up-regulated and 1090 down-regulated transcripts (Fig. 3). The most important (Log2 Fold Change>5.5 or <-4.5) up-regulated (50) and down-regulated (25) transcripts are listed in Table 2. Among them, UDP-glycosyltransferase, RING/U-box protein with C6HC-type zinc finger, Glutamate receptor, Transmembrane amino acid transporter family protein, Tetratricopeptide repeat (TPR)-like superfamily protein and Aspartic proteinase A1 were the highest up-regulated DEGs in the VOCs–treated tobacco seedlings. Bifunctional inhibitor, Cytochrome P450 superfamily protein, and Aluminum-activated malate transporter 2 were significantly repressed by the VOCs treatment.
In the functional annotation, DEGs with the largest increases in expression were those related to sequence-specific DNA binding, DNA-binding transcription factor activity and transcription regulator activity based upon the GO enrichment analyses (Fig. 4, Table 2). Based on the KEGG pathway, the most significant up-regulated transcripts by VOCs were categorised into glutathione metabolism, taurine and hypotaurine metabolism and alpha-Linolenic acid metabolism pathways (Fig. 4). The expression profile of TF genes displays the upcoming transcription actions regulated by these genes. The largest TF families detected in our study were basic helix-loop-helix (bHLH) DNA-binding superfamily protein, WRKY, NAC domain-containing protein (NAC), ethylene responsive factor (ERF), and zinc finger protein genes (C2H2), respectively (Fig. 5).
Table 2. Most important differentially expressed genes in tobacco plants inoculated with WSW007
Gene ID
|
Log2 Fold Change
|
Gene Description
|
Upregulated genes
|
|
|
Niben101Scf00661g00002
|
10.060430640
|
UDP-glycosyltransferase 74 F1 Length=449
|
Niben101Scf06249g05020
|
8.655379403
|
RING/U-box protein with C6HC-type zinc finger Length=384
|
Niben101Scf08670g00020
|
7.530560396
|
Glutamate receptor 2.9
|
Niben101Scf03020g00009
|
7.215864727
|
Transmembrane amino acid transporter family protein Length=519
|
Niben101Scf12266g09001
|
7.051653856
|
Tetratricopeptide repeat (TPR)-like superfamily protein Length=305
|
Niben101Scf06301g01003
|
7.049458081
|
Aspartic proteinase A1
|
Niben101Scf09547g02001
|
6.978790124
|
Vicilin
|
Niben101Scf10205g00006
|
6.961113014
|
Glutathione S-transferase U7
|
Niben101Scf00571g08006
|
6.872915147
|
calmodulin-binding family protein Length=605
|
Niben101Scf00892g00003
|
6.856268380
|
VQ motif protein [Medicago truncatula]
|
Niben101Scf11071g04005
|
6.765291308
|
Calmodulin binding protein-like Length=451
|
Niben101Scf07058g04002
|
6.748638631
|
P-loop containing nucleoside triphosphate hydrolases superfamily protein Length=500
|
Niben101Scf02188g00002
|
6.641885511
|
WRKY transcription factor 1
|
Niben101Scf10086g00004
|
6.628733410
|
Pyridoxal phosphate (PLP)-dependent transferases superfamily protein LENGTH=482
|
Niben101Scf01400g00014
|
6.593433989
|
Thaumatin-like protein
|
Niben101Scf05099g01002
|
6.582500241
|
Mitochondrial import inner membrane translocase subunit Tim17/Tim22/Tim23 family protein Length=178
|
Niben101Scf10316g03004
|
6.566745729
|
Glutathione S-transferase U8
|
Niben101Scf02406g00002
|
6.560683046
|
GDSL esterase/lipase
|
Niben101Scf08351g01002
|
6.553346888
|
Tumor susceptibility gene 101 protein
|
Niben101Scf07599g00019
|
6.498548300
|
Bifunctional inhibitor/lipid-transfer protein/seed storage 2S albumin superfamily protein Length=149
|
Niben101Scf03191g04002
|
6.485170225
|
Eukaryotic aspartyl protease family protein Length=433
|
Niben101Scf11609g03002
|
6.476297273
|
Vicilin
|
Niben101Scf15467g02029
|
6.452546071
|
Patatin-like protein 2
|
Niben101Scf07123g01015
|
6.378502254
|
Leucine-rich repeat receptor-like protein kinase family protein Length=1045
|
Niben101Scf06603g03002
|
6.337344255
|
WRKY transcription factor 55
|
Niben101Scf13429g04019
|
6.305358141
|
L-lactate dehydrogenase A-like 6B
|
Niben101Scf02041g00002
|
6.288632348
|
Chitinase 8
|
Niben101Scf12017g01005
|
6.276659260
|
transmembrane protein, putative [Medicago truncatula]
|
Niben101Scf04124g05022
|
6.209441727
|
SPX domain-containing protein 3
|
Niben101Scf02411g00015
|
6.202117169
|
receptor kinase 3 Length=850
|
Niben101Scf04547g02001
|
6.193216865
|
LL-diaminopimelate aminotransferase
|
Niben101Scf02411g01007
|
6.166484534
|
Calcium-binding EF-hand family protein Length=130
|
Niben101Scf02907g06004
|
6.158855386
|
Alcohol dehydrogenase
|
Niben101Scf03006g10013
|
6.151587732
|
Transcription factor 15
|
Niben101Scf06916g01011
|
6.145218827
|
NAC domain-containing protein 2
|
Niben101Scf02373g05009
|
5.984339124
|
Pumilio homolog 11
|
Niben101Scf01701g03007
|
5.968736001
|
Ethylene-responsive transcription factor 1
|
Niben101Scf00332g06012
|
5.910002559
|
Pyrophosphate-energized vacuolar membrane proton pump
|
Niben101Scf00096g00004
|
5.906978650
|
Myb family transcription factor APL
|
Niben101Scf12102g01006
|
5.849476341
|
VQ motif protein [Medicago truncatula]
|
Niben101Scf02115g04004
|
5.807380053
|
Eukaryotic aspartyl protease family protein Length=474
|
Niben101Scf04894g00006
|
5.799178811
|
UDP-glucose 4-epimerase
|
Niben101Scf02869g03007
|
5.748520484
|
Potassium transporter 6
|
Niben101Scf04343g01005
|
5.743969810
|
Bidirectional sugar transporter N3
|
Niben101Scf00526g00018
|
5.724743243
|
NAC domain-containing protein 86
|
Niben101Scf01517g06010
|
5.717129463
|
Glutathione S-transferase 3
|
Niben101Scf02305g01016
|
5.680442984
|
receptor kinase 3 Length=850
|
Niben101Scf09445g04018
|
5.678406391
|
ankyrin repeat family protein Length=548
|
Niben101Scf03147g10010
|
5.641454430
|
Glutathione S-transferase U8
|
Niben101Scf02264g06032
|
5.621964655
|
receptor kinase 2 Length=847
|
Downregulated genes
|
|
|
Niben101Scf02807g00003
|
-7.365966006
|
Bifunctional inhibitor/lipid-transfer protein/seed storage 2S albumin superfamily protein Length=275
|
Niben101Scf01826g00001
|
-6.517665466
|
Cytochrome P450 superfamily protein Length=488
|
Niben101Scf39499g00005
|
-6.391959580
|
Aluminum-activated malate transporter 2
|
Niben101Scf00298g00001
|
-6.308027899
|
Ethylene-responsive transcription factor 1
|
Niben101Scf02838g00003
|
-6.231295351
|
equilibrative nucleoside transporter 7 Length=417
|
Niben101Scf11694g01005
|
-6.007749087
|
Ethylene-responsive transcription factor 4
|
Niben101Scf02375g06001
|
-5.828865641
|
Homeobox protein knotted-1-like 2
|
Niben101Scf28036g00001
|
-5.742318039
|
jasmonate-zim-domain protein 8 Length=131
|
Niben101Scf07775g01006
|
-5.649346051
|
Terpenoid synthase 6
|
Niben101Scf14022g01008
|
-5.349178022
|
Growth-regulating factor 5
|
Niben101Scf00180g07005
|
-5.256451151
|
Serine carboxypeptidase-like 31
|
Niben101Scf09248g03013
|
-5.207860959
|
Peroxidase 4
|
Niben101Scf09317g01012
|
-5.193418084
|
alpha/beta-Hydrolases superfamily protein Length=517
|
Niben101Scf02393g02025
|
-5.185958414
|
Cupredoxin superfamily protein Length=257
|
Niben101Scf01198g00002
|
-5.148755969
|
Domain of Uncharacterized protein function, putative isoform 1 [Theobroma cacao] gb|EOX92163.1| Domain of Uncharacterized protein function, putative isoform 1 [Theobroma cacao]
|
Niben101Scf06890g00001
|
-5.074875710
|
Subtilisin-like protease
|
Niben101Scf16773g02010
|
-4.979752442
|
GRF1-interacting factor 1
|
Niben101Scf01971g01006
|
-4.967651870
|
Kunitz-type inhibitor C [Solanum tuberosum]
|
Niben101Scf10219g00026
|
-4.892743863
|
Cathepsin B-like cysteine proteinase
|
Niben101Scf09368g02010
|
-4.852826600
|
Transcription factor bHLH96
|
Niben101Scf07105g04004
|
-4.820323982
|
1-aminocyclopropane-1-carboxylate oxidase homolog 4
|
Niben101Scf03660g02003
|
-4.792373513
|
Membrane transporter D1
|
Niben101Scf00478g05003
|
-4.783667557
|
BnaC01g07190D [Brassica napus]
|
Niben101Scf05459g00001
|
-4.623767607
|
Ethylene-responsive transcription factor 10
|
Niben101Scf01188g10003
|
-4.552564262
|
cysteine-rich extensin-like protein-2 [Nicotiana tabacum]
|
3.4 Identification of VOCs produced by Bacillus velezensis WSW007
In GC-MS analysis, 38 compounds were detected, in which 13 (accounting 34.21% of the total VOCs) were reported as PGP effective VOCs, and 11 (accounting 28.95% of the total VOCs) had potential to increase the resistance of plant to phytopathogens (Table 3). According to their relative abundances, four compounds could be identified as the main components, each occupying more than 5% of the total, including the pathogen inhibiting compounds Carbon dioxide (28.6%) and 2,4-bis(1,1-dimethylethyl)- Phenol (14.1%), and the growth promoting compounds Acetoin (5.9%) and 2,3-Butanediol (5.97%). Among these compounds, 2,4-Di-tert-butylphenol [o 2,4-bis(1,1-dimethylethyl)- phenol] and Carbon dioxide were the most abundant VOCs of strain WSW007 (Fig. 6).
Table 3. VOCs detected from the metabolites of Bacillus velezensis WSW007
R.T.
|
VOCs
|
Effect
|
Description of effects
|
Relative abundance
|
Reference
|
(min)
|
0.953
|
Carbon dioxide
|
Disease resistance
|
Production of volatile metabolites from Streptomyces albidoflavus cultivated on gypsum board and tryptone glucose extract agar-influence of temperature, oxygen and carbon dioxide levels.
|
28.60%
|
(Sunesson et al., 1997)
|
1.347
|
Acetic acid
|
Unknown
|
|
12.96%
|
|
1.633
|
Isovaleraldehyde
|
Disease resistance
|
Soil bacterial diffusible and volatile organic compounds inhibit Phytophthora capsici and promote plant growth
|
0.71%
|
(Syed-Ab-Rahman et al., 2019)
|
1.824
|
Silanediol, dimethyl-
|
Unknown
|
|
2.03%
|
|
2.015
|
Acetoin
|
PGPR
|
Volatiles produced by Bacillus mojavensis RRC101 act as plant growth modulators and are strongly culture-dependent
|
5.90%
|
(Rath et al., 2018)
|
2.836
|
2,3-Butanediol
|
PGPR
|
Bacterial volatiles promote growth in Arabidopsis
|
5.97%
|
(Ryu et al., 2003)
|
3.835
|
1-Propanamine, N,2-dimethyl-
|
Unknown
|
|
1.00%
|
|
4.038
|
Propanoic acid
|
PGPR
|
Enhancement in plant growth and zinc biofortification of chickpea (Cicer arietinum L.) by Bacillus altitudinis
|
1.03%
|
(Kushwaha et al., 2021)
|
4.967
|
2-Heptanone
|
PGPR
|
Volatile organic compounds emitted by Bacillus sp. JC03 promote plant growth through the action of auxin and strigolactone
|
1.52%
|
(Jiang et al., 2019)
|
5.47
|
Pyrazine, 2,5-dimethyl-
|
Disease resistance
|
Identification of endophytic Bacillus velezensis ZSY-1 strain and antifungal activity of its volatile compounds against Alternaria solani and Botrytis cinerea
|
0.55%
|
(Gao et al., 2017)
|
6.608
|
6-Methyl-2 -Heptanone
|
Disease resistance
|
mechanism of a volatile organic compound (6-methyl-2-heptanone) emitted from Bacillus subtilis ZD01 against Alternaria solani in Potato
|
0.46%
|
(Zhang et al., 2022)
|
6.717
|
Benzaldehyde
|
PGPR
|
Benzaldehyde as a new class plant growth regulator on Brassica campestris
|
1.10%
|
(Choi et al., 2016)
|
9.058
|
Benzene -acetaldehyde
|
Unknown
|
|
1.66%
|
|
10.19
|
2-Ethylacridine
|
Unknown
|
|
0.34%
|
|
10.343
|
Pyrazine, tetramethyl-
|
Disease resistance
|
Antibacterial property of tetramethyl-pyrazine from the stem of Jatropha podagrica
|
0.95%
|
(Odebiyi, 1980)
|
10.502
|
2-Nonanone
|
PGPR
|
Physiological response of Lactuca sativa exposed to 2-nonanone emitted by Bacillus sp. BCT9
|
1.21%
|
(Fincheira and Quiroz, 2019)
|
10.756
|
2-Heptadecanol
|
PGPR
|
Soil bacterial diffusible and volatile organic compounds inhibit Phytophthora capsici and promote plant growth
|
0.58%
|
(Syed-Ab-Rahman et al., 2019)
|
10.852
|
2-Hepten-1-ol, (E)-
|
Unknown
|
|
0.78%
|
|
11.043
|
2-Hydroxy -octanoic acid
|
Unknown
|
|
0.43%
|
|
13.626
|
Oxalic acid, isobutyl pentyl ester
|
Unknown
|
|
0.34%
|
|
15.197
|
Phenol, 2,3,5-trimethyl-
|
Unknown
|
|
0.42%
|
|
16.202
|
2-Undecanone
|
Disease resistance
|
The bacillary postbiotics, including 2-undecanone, suppress the virulence of pathogenic microorganisms
|
1.08%
|
(Rajasekharan and Shemesh, 2022)
|
16.399
|
2-Hexadecanol
|
Disease resistance
|
Production of volatile organic compounds by an antagonistic strain Paenibacillus polymyxa WR-2 in the presence of root exudates and organic fertilizer and their antifungal activity against Fusarium oxysporum f. sp. niveum
|
1.40%
|
(Raza et al., 2015)
|
17.506
|
Naphthalene, decahydro-4a -methyl-,
|
Disease resistance
|
Biopesticidal potentials of plants extracts against Cochliobolus lunatus RR Nelson & FA Haasis. Anamorph: Curvularia lunatus (Wakker) Boedgin.
|
0.33%
|
(Ilondu, 2020)
|
17.914
|
2-Hexanone, 4-methyl-
|
Unknown
|
|
0.38%
|
|
19.008
|
Tetradecane
|
PGPR
|
Strain-specific variation in plant growth promoting volatile organic compounds production by five different Pseudomonas spp. as confirmed by response of Vigna radiata seedlings
|
0.96%
|
(Jishma et al., 2017)
|
19.288
|
Androst-5-ene-3,7-dione,4,4-dimethyl-17-trimethylsily -loxy-
|
Unknown
|
|
0.34%
|
|
21.394
|
2-Tridecanone
|
PGPR
|
Volatile organic compounds stimulate plant growing and seed germination of Lactuca sativa
|
1.43%
|
(Fincheira et al., 2017)
|
21.788
|
Phenol, 2,4-bis(1,1 -dimethylethyl)-
|
Disease resistance
|
Effect of volatile substances of Streptomyces platensis F-1 on controlof plant fungal diseases
|
14.10%
|
(Wan et al., 2008)
|
22.921
|
2-Tetradecanone
|
Unknown
|
|
0.91%
|
|
23.086
|
2-Dodecanone
|
PGPR
|
Biocontrol of Colletotrichum falcatum with volatile metabolites produced by endophytic bacteria and profiling VOCs by headspace SPME coupled with GC–MS
|
1.57%
|
(Jayakumar et al., 2021)
|
23.239
|
2-Tetradecanol
|
Unknown
|
|
0.56%
|
|
23.849
|
Nonadecane
|
PGPR
|
Strain-specific variation in plant growth promoting volatile organic compounds production by five different Pseudomonas spp. as confirmed by response of Vigna radiata seedlings
|
0.74%
|
(Jishma et al., 2017)
|
26.082
|
Heptadecane
|
Disease resistance
|
Identification of rhizospheric actinomycete Streptomyces lavendulae SPS-33 and the inhibitory effect of its volatile organic compounds against Ceratocystis fimbriata in postharvest sweet potato (Ipomoea batatas)
|
3.68%
|
(Li et al., 2020)
|
28.704
|
Octyl-.beta.-D-glu -copyranoside
|
Unknown
|
|
0.52%
|
|
28.907
|
17-Pentatriacontene
|
Disease resistance
|
Phytochemical screening and antibacterial activity of Eucalyptus camaldulensis's leaves and bark extracts
|
1.23%
|
(Alghamdi and Ababutain, 2019)
|
29.244
|
2-Pentadecanone, 6,10,14-trimethyl-
|
PGPR
|
Seedling growth-promoting composition, a kit, a method for applying the former, and use of the volatile organic compounds comprising the composition
|
1.06%
|
(Fincheira et al., 2017)
|
32.603
|
n-Hexadecanoic acid
|
PGPR
|
Plant growth promotion and biocontrol potential of fungal endophytes in the inflorescence of Aloe vera L.
|
1.17%
|
(Chowdhary and Sharma, 2020)
|
Alghamdi, A.I., Ababutain, I.M., 2019. Research article phytochemical screening and antibacterial activity of Eucalyptus camaldulensis’s leaves and bark extracts. Asian Journal of Scientific Research 12, 202-210.
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Chowdhary, K., Sharma, S., 2020. Plant Growth Promotion and Biocontrol Potential of Fungal Endophytes in the Inflorescence of Aloe vera L. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences 90, 1045-1055.
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