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Plant Growth Promoting Rhizobacteria (PGPR) Regulated Phyto and Microbial Beneficial Protein Interactions

  • Faten Dhawi EMAIL logo
Published/Copyright: February 28, 2020
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Open Life Sciences
From the journal Open Life Sciences Volume 15 Issue 1

Abstract

Plant Growth Promoting Rhizobacteria (PGPR) influence plants’ physiological characteristics, metabolites, pathways and proteins via alteration of corresponding gene expression. In the current study, a total of 42 upregulated uncharacterized sorghum bicolor root proteins influenced by PGPR were subjected to different analyses: phylogenetic tree, protein functional network, sequences similarity network (SSN), Genome Neighborhood Network (GNN) and motif analysis. The screen for homologous bacterial proteins to uncover associated protein families and similar proteins in non-PGPRs was identified. The sorghum roots’ uncharacterized protein sequences analysis indicated the existence of two protein categories, the first being related to phytobeneficial protein family associated with DNA regulation such as Sulfatase, FGGY_C, Phosphodiesterase or stress tolerance such as HSP70. The second is associated with bacterial transcriptional regulators such as FtsZ, MreB_Mbl and DNA-binding transcriptional regulators, as well as the AcrR family, which existed in PGPR and non PGPR. Therefore, Plant Growth-Promoting Rhizobacteria (PGPR) regulated phytobeneficial traits through reciprocal protein stimulation via microbe plant interactions, both during and post colonization.

Keywords: Plant Growth promoting rhizobacteria; Sorghum; phylogenetic analysis; protein family; microbe interactions

1 Introduction

The successful use of Plant-Growth-Promoting Rhizobacteria (PGPR) in agriculture is correlated with reciprocal gene regulation between bacteria and plants during plant colonization. This gene regulation exerts phytobeneficial results on biomass, nutrient uptake and metabolite upregulation [1, 2, 3, 4, 5] on proteins and biological pathways [6], as well as on gene expression [7]. In the current study, the PGPR—Pseudomonas sp. TLC 6-6.5-4—as previously used [1] was applied to two-day-old sorghum seedlings to check the function of upregulated, uncharacterized root proteins three months after PGPR colonization. The study’s main objective was to reveal the function of uncharacterized sorghum bicolor proteins in roots treated with PGPR. In order to identify the functions of these proteins, several steps were conducted. Sorghum root uncharacterized protein sequences were used in a Blast search for homologous protein sequences in bacteria, since they were unidentified in plant protein sequences. In total, 564 proteins were subjected to several analyses to determine their possible role in phytobeneficial traits. The analyses included the following: sequence similarity network (SSN), Genome Neighborhood Network (GNN), functional network and motif identification. The sorghum roots’ uncharacterized protein analysis revealed the existence of protein families belonging to plant, Plant-Growth-Promoting Rhizobacteria (PGPR) and Non-Plant-Growth-Promoting Rhizobacteria (non-PGPR), thus emphasizing the role of microbe plant interactions during and post colonization.

2 Material and methods

2.1 Plant growth conditions and treatments

Two-day-old germinated seedlings of sorghum bicolor were inoculated with PGPR Pseudomonas sp. TLC 6-6.5-4 [1] for two hours, after which they were planted in 600 g of pasteurized mixed soil consisting of coarse sand and loam (1:1). Pseudomonas sp. TLC 6-6.5-4 was grown on Luria-Bertani (LB) agar for 48 h, harvested, suspended and dissolved in 120 ml of 0.85% NaCl solution to reach 10-8 cfu/mL, which was used for the sorghum seedling inoculation and was sprayed on the soil surface. The growth conditions for sorghum in a greenhouse were 14 hours of light, at 30°C and 65% humidity. The experiment consisted of seven sorghum bicolor treated with PGPR Pseudomonas sp. TLC 6-6.5-4- and seven untreated sorghum bicolor as a control. Sorghum bicolor plants were harvested after 90 days for root protein analyses. Roots were washed with distilled water to remove soil then frozen in liquid nitrogen. Protein was extracted from frozen roots; three samples for each group followed the procedure described in Dhawi et al. [6] and modified from Fukao et al. [8].

Three protein samples for each group (treated and control) were digested with trypsin and then analyzed using LC-MS/MS on a Waters/Micromass AB QSTAR Elite (Waters nano ACQUITY ultra high-pressure liquid chromatograph UPLC) for peptide separation. The detected peptides were quantified and normalized to obtain the abundance of each sample according to Progenesis QI (http://www.nonlinear.com/progenesis/qi/v2.0/faq/hownormalisation-works.aspx). Protein levels of two folds and above in comparison to the control were considered significant change to be consider in further analysis.

2.2 Sorghum root uncharacterized protein processing

The sequences of the 42 uncharacterized sorghum root proteins (Table 1) were used to search for homologous bacterial proteins using PSI Blast (https://blast.ncbi.nlm.nih.gov/Blast.cgi?PAGE=Proteins), which resulted in 830 protein sequences. These sequences were filtered using Cluster Database at High Identity with Tolerance (CD-HIT) Suite: Biological Sequence Clustering and Comparison (http://weizhongli-lab.org/cdhit_suite/cgi-bin/index.cgi) with a 90% identity cut-off. The 90% cut-off step resulted in 564 protein sequences for inclusion in the multiple sequence alignment (MSA). MSA was created by using the MEGA7 (Molecular Evolutionary Genetics Analysis) software version 6 [9]. The phylogenetic tree was established in MEGA 6 and aligned via the Muscle program for 564 proteins, 42 of which were sorghum root uncharacterized upregulated proteins. Protein sequences were aligned using neighbor-joining [10] and UPGMA (Unweighted Pair Group Method), with a bootstrap method of 500 replications for a phylogeny test. The interactive tree of life (iTol) online web tool (http://itol.embl.deg) was then used to display and modify the tree colors [11].

Table 1

Uncharacterized sorghum proteins fold changes influenced by Pseudomonas sp. in comparison with control

Protein IDFold change
C5YZ775.5
C5XHS54.8
C5X5F04.7
C5XV254.1
C5XFI23.9
C5YUN23.7
C5XGS93.5
C5YPP63.2
C5XLV52.9
C5Y9B52.5
C5WXA42.3
C5YPX82.3
C5XC952.3
C5X4M52.3
C5WXN22.1
C5YBP81.9
C5Y9211.9
C5XYX01.9
C5YC511.8
C5YU581.8
C5YR141.7
C5Y6L41.7
C5XG111.7
C5YAG21.7
C5YYY81.7
C5YDJ21.7
C5XCI91.7
C5YIX71.7
C5YYX11.7
C5WT781.6
C5WXD71.6
C5XG441.6
C5YXQ91.6
C5YEW31.6
C5Z7E81.6
C5Z1X31.6
C5YI641.6
C5WRP71.5
C5XHR81.5
C5Y6511.5
C5XWM51.5
C5Z8A91.5

3 Protein functional network and family assignment

A combination of different approaches was used to assign homologous proteins to protein families (Pfam) with a putative function. In total, 564 protein sequences consisting of sorghum root uncharacterized protein and similar bacterial protein sequences were used to determine functions via the genomic, protein and gene interactions through the sequence similarity network (SSN) and Genome Neighborhood Network (GNN) approach, respectively. The GNN approach was performed using the Enzyme Similarity Tool–Enzyme Function Initiative (EFI-EST) https://efi.igb.illinois.edu/efi-est/[12]. In order to use EFI-EST, the 564 proteins were converted to UniProt Id, resulting in 554 identified proteins in the UniProt database and 10 unidentified bacterial proteins. The EFI-EST website was used to generate a sequence similarity network (SSN), and the resulting files were visualized in Cytoscape software [13]. Sorghum protein sequences were screened for motifs using the MEME (Multiple EM for Motif Elicitation) tool (http://meme-suite.org/tools/meme) [14], with a maximum number of eight motifs for the detection level and an E-value equal to or less than 0.05. Further analyses were performed for protein families using STRING Consortium 2019 (https://string-db.org/) [15].

4 Results

4.1 Phylogenetic tree analysis

The results showed 42 sorghum proteins according to UniProt (http://www.uniprot.org/), which were upregulated from 2–5-fold when compared to the control group. The 42 upregulated sorghum proteins have an unknown function; therefore, several analyses and different approaches were used to identify the function and check for similarity of these uncharacterized proteins with bacterial proteins via an NCBI search (https://blast.ncbi.nlm.nih.gov/Blast.cgi).

The phylogenetic tree of 564 protein sequences included 42 uncharacterized sorghum proteins and similar bacterial proteins aligned using Multiple Sequence alignments (MUSCLE) with a bootstrap of 500. The resulting unrooted phylogenetic tree consisted of 20 nodes, in which sorghum uncharacterized protein sequences were clustered in five of them (Figure 1). The motif analysis of these sorghum and bacterial protein sequences clustered in the same nodes identified eight similar protein family domains represented by motif logos in Figure 2, namely, Sulfatase, CARBOHYDRATE KINASES (FGGY _C), Phosphodiest, Cell division protein FtsA, GSDH, MreB_Mbl, StbA and HSP70.

Figure 1 The phylogenetic tree of uncharacterized sorghum proteins and similar bacterial proteins. The unrooted neighbor-joining phylogenetic tree constructed based on 564 multiple proteins sequence alignment using MUSCLE with 500 bootstrap replicates.
Figure 1

The phylogenetic tree of uncharacterized sorghum proteins and similar bacterial proteins. The unrooted neighbor-joining phylogenetic tree constructed based on 564 multiple proteins sequence alignment using MUSCLE with 500 bootstrap replicates.

Figure 2 The phylogenetic tree of uncharacterized sorghum proteins and similar bacterial proteins. The unrooted neighbor-joining phylogenetic tree constructed based on the sequence alignment of 564 multiple proteins using Multiple Sequence alignments (MUSCLE) with 500 bootstrap replicates.
Figure 2

The phylogenetic tree of uncharacterized sorghum proteins and similar bacterial proteins. The unrooted neighbor-joining phylogenetic tree constructed based on the sequence alignment of 564 multiple proteins using Multiple Sequence alignments (MUSCLE) with 500 bootstrap replicates.

4.2 Sequence similarity network (SSN)

The SSN used to analyze 554 sequences consisted of 42 uncharacterized sorghum protein sequences and 507 bacterial protein sequences. These sequences were obtained by PSI-BLAST at E values of 10–15; the sequences were clustered based on their similarities in seven clusters. The SSN clusters containing sorghum proteins were cluster 1 (61 protein sequences), cluster 3 (23 sequences), cluster 5 (17 protein sequences), cluster 14 (seven protein sequences), cluster 16 (five protein sequences), cluster 19 (four protein sequences) and cluster 24 (three protein families) (Figure 3). Some proteins were separated with no clusters due to a different E value score. These SSN results were used to establish a Genome Neighborhood Network (GNN).

Figure 3 a) Sequence similarity network of uncharacterized sorghum and similar bacterial proteins consisting of 564 sequences at an E value of 10-15. b) Sorghum uncharacterized proteins clustered in seven groups, with different protein nodes. Each node (circle) represents proteins with similar sequences; the lines indicate the pairwise relationship between sequences. Proteins that have no sorghum sequences appeared as separated and are not labelled.
Figure 3

a) Sequence similarity network of uncharacterized sorghum and similar bacterial proteins consisting of 564 sequences at an E value of 10-15. b) Sorghum uncharacterized proteins clustered in seven groups, with different protein nodes. Each node (circle) represents proteins with similar sequences; the lines indicate the pairwise relationship between sequences. Proteins that have no sorghum sequences appeared as separated and are not labelled.

4.3 Genome Neighborhood Networks (GNN), motif screening and functional partenrs

The SNN results were used to build GNNs. The output of the GNN in the Hub–Nodes format showed the number of Pfam gene neighbors that were found in each cluster of sequences. The SNN revealed that uncharacterized protein sequences of sorghum were clustered in seven nodes. The nodes included 1, 3, 5, 14, 16, 19 and 24 protein families, arranged based on their genomic context (Fig.4). Nodes shared 86 protein families (See appendix Table1). On the other hand, the motif scan analysis of sorghum root proteins identified four main protein families: HSP70, MreB_Mbl, StbA and FtsA (Figure 4). The functional protein association network analysis using STRING 2019 predicted nine functional partners. These functional partners were N-acetyltransferase, the GNAT superfamily (includes histone acetyltransferase HPA2), DNA-binding transcriptional regulator, AcrR family; MFS family permease, SAM-dependent methyltransferase, DNA-binding transcriptional regulator, ArsR family, cAMP-binding domain of CRP or a regulatory subunit of cAMP-dependent protein kinases, glycosyltransferase involved in cell wall biosynthesis, signal transduction histidine kinase, and sugar kinase of the NBD/HSP70 family containing an N-terminal HTH domain (Figure 5).

Figure 4 a) Genome Neighborhood Networks (GNNs) in the Hub–Nodes format for 564 protein sequences. b) The hexagon shapes (hubs) represent sequence similarity network (SSN) clusters, and the other shapes (nodes) represent the Pfam genome neighbors. Seven node clusters are indicated with 94 genes. The names of nodes are the short name of the protein family (Pfam).
Figure 4

a) Genome Neighborhood Networks (GNNs) in the Hub–Nodes format for 564 protein sequences. b) The hexagon shapes (hubs) represent sequence similarity network (SSN) clusters, and the other shapes (nodes) represent the Pfam genome neighbors. Seven node clusters are indicated with 94 genes. The names of nodes are the short name of the protein family (Pfam).

Figure 5 The functional protein association networks for 86 protein families resulting from GNN using the STRING Consortium 2019 functional protein association networks (https://string-db.org/) Szklarczyk et al., [15].
Figure 5

The functional protein association networks for 86 protein families resulting from GNN using the STRING Consortium 2019 functional protein association networks (https://string-db.org/) Szklarczyk et al., [15].

5 Discussion

The phylogenetic tree analysis of the 20 nodes identified that five nodes were sorghum proteins clustered with similar bacterial proteins. The motif analysis of these sorghum and bacterial protein sequences clustered in the same nodes revealed six protein family domains (Sulfatase, CARBOHYDRATE KINASES (FGGY _C), Phosphodiesterase, FtsZ, MreB_Mbl and HSP70). Some members of this protein family have no eukaryotic existence, but this might have remained in root cells following plant treatment and may play an intrinsic role. This resulted in phytobeneficial traits such as tolerance to salinity [16], heavy metal [1, 2], and drought [17], or increased plant biomass under normal environmental conditions [18]. Similarly, the results of SNN, GNN and STRING protein functional networks of sorghum root proteins identified the main protein families: HSP70, MreB_Mbl, StbA and FtsA. Therefore, protein analysis revealed the existence of protein families belonging to plant, Plant-Growth-Promoting Rhizobacteria (PGPR) and Non-Plant-Growth-Promoting Rhizobacteria (non-PGPR), thus emphasizing the reciprocal benefit synchronized between plant and bacteria during and post colonization.

5.1 Phytobeneficial proteins induced by PGPR

Plant-Growth-Promoting Rhizobacteria (PGPR) induced several phytobeneficial and desired traits such as an increase in production or tolerance during biotic or abiotic stress [19]. The beneficial effect is associated with an increase in gene expression and certain protein families such as sulfatase substrates, which are involved in hormone regulation, cellular degradation and the modulation of signaling pathways. The increase of element compositions post plant inoculation with PGPR might be explained by sulfatase’s ability to cycle environmental sulfur via degradation or cellular remodeling [20]. The increase of biomass in plants is associated with the increased sugars and carbohydrates represented in this study due to an increase in the Carbohydrate kinases (FGGY _C) protein family, which is involved in bacterial signaling molecules [21]. In addition, FGGY carbohydrate kinases contributed plant adenosine and thriphosphate (ATP)-dependent phosphorylation of nine distinct sugar enzymes. These enzymes include L-fucolokinase, gluconokinase, glycerol kinase, xylulokinase, D-ribulose kinase and L-xylulose kinase [22]. In the current study, we identified two distinct protein families, Phosphodiesterase and Heat S hock Protein 70 (Hsp70), that are known to contribute to high plant tolerance. Phosphodiesterase is involved in independent pathways of DNA–protein crosslink repair in plants [23]. However, Heat Shock Protein 70 (Hsp70) is an evolutionarily conserved family of proteins that is typically localized in the cytoplasm and distributed in the intermembrane space of chloroplasts. Hsp70 plays a crucial role in protein biogenesis, protection during stress, assistance in protein translocation [24], protection against several stress types, and the maintenance of cellular homeostasis [25]. The upregulation of several sorghum proteins associated with an increase in N-acetyltransferase, the GNAT superfamily (including histone acetyltransferase HPA2) was observed in the current study, and this is believed to be involved in the regulation of the transcription of many genes [26].

5.2 Rhizobacterial transcriptional regulators

Several protein families related to bacteria were found in sorghum roots post plant inoculation that work as functional gene regulators. Some of these proteins were identified in a previous study and are known to contribute to phytobeneficial traits related to PGPR [7]. Other proteins are known as bacterial proteins induced by plant root exudates and participate in the bacterial gene regulation of PGPR, such as Bacillus atrophaeus [27]. Some of the predicted functionally related bacterial protein families are known bacterial transcriptional regulators, such as FtsZ, MreB_Mbl, DNA-binding transcriptional regulator and the AcrR family, as shown by the results of the current study. These functionally related protein families are MFS family permease, SAM-dependent methyltransferase, S‐ adenosyl methionine (SAM), DNA-binding transcriptional regulator, ArsR family transcriptional regulator, the cAMP-binding domain of CRP or a regulatory subunit of cAMP-dependent protein kinases, DNA-binding and transcription regulation, glycosyltransferase, and histidine kinases (HKs).

The family of FtsZ is a bacterial membrane tubulin-related cell division protein [28]. MreB/Mbl is a gene-coding protein related to the bacterial protein FtsZ cell membrane protein [29]. Additionally, the analysis identified possible roles of the bacteria–DNA-binding transcriptional regulators known as the AcrR family [30] and the association of amino acid transfer proteins known as MFS family permease [31]. Thus, we emphasized the role of plant root exudates in enhancing bacterial growth activity via the activation of functional partner proteins such as SAM-dependent methyltransferase S‐adenosyl methionine (SAM), which is known to transfer the methyl group to DNA [32]. The DNA-binding transcriptional regulator and ArsR family transcriptional regulator are involved in lipid metabolism regulation [33], cAMP-dependent protein kinase DNA-binding and transcription regulation [34], while glycosyltransferase is involved in cell wall biosynthesis [35], and histidine kinases (HKs) are known to function in bacterial signal transduction [36].

6 Conclusion

Plant Growth Promoting Rhizobacteria (PGPR) regulated phytobeneficial traits by reciprocal protein stimulation via microbe–plant interactions during and post colonization. Furthermore, plant root exudates stimulated bacterial gene regulators associated with bacterial signaling, DNA-binding transcriptional regulators, and cell growth.

Acknowledgements

We express deep gratitude to Dhawi and Safia for their great help during the process of research development. This study was self-funded in fully supported by the author.

  1. Data Availability: Data that are supplementary to the manuscript will be available by request.

  2. Conflict of interest: Authors state no conflict of interest.

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Appendix

Table 2

The protein families (Pfam) and their description resulted from analysis on Genome Neighbourhood Networks GNN in Hub-Nodes format from 564 protein sequences resulted in seven node clusters indicated with 86 genes.

PfamPfam Description
Node 1
HrcAHrcA protein C terminal domain
GrpEFactor GrpE domain
Node 14
Ribonuc_L-PSPEndoribonuclease L-PSP
Amidohydro_1Amidohydrolase family
Abhydrolase_3alpha/beta hydrolase fold
YceIYceI-like domain
SnoaL_2SnoaL-like domain
DUF1643Protein of unknown function (DUF1643)
Flavodoxin_2Flavodoxin-like fold
Pyr_redox_3Pyridine nucleotide-disulphide oxidoreductase
Glyco_hydro_3-Glyco_hydro_3_CGlycosyl hydrolase family 3 N terminal domain-Glycosyl hydrolase family 3 C-terminal domain
PkinaseProtein kinase domain
Cupin_1Cupin
Response_reg-Trans_reg_CResponse regulator receiver domain-Transcriptional regulatory protein, C terminal
Chlorophyllase2Chlorophyllase enzyme
STAS_2STAS domain
DNA_ligase_A_M-DNA_ligase_A_CATP dependent DNA ligase domain-ATP dependent DNA ligase C terminal region
DNA_primase_SDNA primase small subunit
PQQ_2PQQ-like domain
SpoIIEStage II sporulation protein E (SpoIIE)
HisKA-HATPase_cHis Kinase A (phospho-acceptor) domain-Histidine kinase-, DNA gyrase B-, and HSP90-like ATPase
ABC_tranABC transporter
ABC2_membrane_2ABC-2 family transporter protein
Peptidase_A24-DiS_P_DiSType IV leader peptidase family-Bacterial Peptidase A24 N-terminal domain
HisKA-HATPase_c-PAS_4His Kinase A (phospho-acceptor) domain-Histidine kinase-, DNA gyrase B-, and HSP90-like ATPase-PAS fold
Cupin_2Cupin domain
Pkinase-PD40Protein kinase domain-WD40-like Beta Propeller Repeat
PBP-DUF1028Phosphatidylethanolamine-binding protein-Family of unknown function (DUF1028)
Mce4_CUP1Cholesterol uptake porter CUP1 of Mce4, putative
MlaDMlaD protein
MlaD-Mce4_CUP1MlaD protein-Cholesterol uptake porter CUP1 of Mce4, putative
RelERelE toxin of RelE / RelB toxin-antitoxin system
VirC1VirC1 protein
AAA_31AAA domain
T4SS-DNA_transfType IV secretory system Conjugative DNA transfer
PRiA4_ORF3Plasmid pRiA4b ORF-3-like protein
GntR-FCDBacterial regulatory proteins, gntR family-FCD domain
Transp_cyt_purPermease for cytosine/purines, uracil, thiamine, allantoin
ResolvaseResolvase, N terminal domain
DUF4158Domain of unknown function (DUF4158)
HTH_31Helix-turn-helix domain
DDE_Tnp_Tn3Tn3 transposase DDE domain
Flavin_ReductFlavin reductase like domain
Asp_Glu_raceAsp/Glu/Hydantoin racemase
Node 16
PTS-HPrPTS HPr component phosphorylation site
Glyco_hydro_32N-Glyco_hydro_32CGlycosyl hydrolases family 32 N-terminal domain-Glycosyl hydrolases family 32 C terminal
Hydrolase_3haloacid dehalogenase-like hydrolase
tRNA-synt_1-Anticodon_1tRNA synthetases class I (I, L, M and V)-Anticodon-binding domain of tRNA
Peptidase_C26Peptidase C26
23S_rRNA_IVP23S rRNA-intervening sequence protein
Trans_reg_CTranscriptional regulatory protein, C terminal
Phage_integrase-Arm-DNA-bind_4-Phage_ int_SAM_3Phage integrase family-Arm DNA-binding domain-Phage integrase, N-terminal SAM-like domain
PTS_EIIB-PTS_EIICphosphotransferase system, EIIB-Phosphotransferase system, EIIC
Vsr-DUF559DNA mismatch endonuclease Vsr-Protein of unknown function (DUF559)
LacI-Peripla_BP_3Bacterial regulatory proteins, lacI family-Periplasmic binding protein-like domain
ATP-cone-NRDDATP cone domain-Anaerobic ribonucleoside-triphosphate reductase
PDDEXK_9-AAA-ATPase_likePD-(D/E)XK nuclease superfamily-Predicted AAA-ATPase
BPD_transp_1Binding-protein-dependent transport system inner membrane component
Sulfate_transp-STASSulfate permease family-STAS domain
DEAD-Helicase_C-HRDC-RecQ_Zn_bindDEAD/DEAH box helicase-Helicase conserved C-terminal domain-HRDC domain-RecQ zinc-binding
ECF-ribofla_trSECF-type riboflavin transporter, S component
Node 19
Plug-CarbopepD_reg_2TonB-dependent Receptor Plug Domain-CarboxypepD_reg-like domain
HexapepBacterial transferase hexapeptide (six repeats)
GSHPxGlutathione peroxidase
MarRMarR family
Pyr_redox_2-Reductase_CPyridine nucleotide-disulphide oxidoreductase-Reductase C-terminal
OsmCOsmC-like protein
DEDD_Tnp_IS110-Transposase_20Transposase-Transposase IS116/IS110/IS902 family
Aldo_ket_redAldo/keto reductase family
Node 24
VCBSRepeat domain in Vibrio, Colwellia, Bradyrhizobium and Shewanella
Asn_synthase-GATase_7Asparagine synthase-Glutamine amidotransferase domain
UvrA_DNA-bind-UvrA_interUvrA DNA-binding domain-UvrA interaction domain
adh_short_C2Enoyl-(Acyl carrier protein) reductase
E1_dh-Transket_pyr-Transketolase_CDehydrogenase E1 component-Transketolase, pyrimidine binding domain-Transketolase, C-terminal domain
Lysine_decarboxPossible lysine decarboxylase
HEM4Uroporphyrinogen-III synthase HemD
ALADDelta-aminolevulinic acid dehydratase
ACP_syn_III_C-ACP_syn_III3-Oxoacyl-[acyl-carrier-protein (ACP)] synthase III C terminal -3-Oxoacyl-[acyl-carrier-protein (ACP)] synthase III
UnbV_ASPIC-VCBSASPIC and UnbV-Repeat domain in Vibrio, Colwellia, Bradyrhizobium and Shewanella
PseudoU_synth_2RNA pseudouridylate synthase
HisKA-HATPase_c-PAS_3-PAS_4His Kinase A (phospho-acceptor) domain-Histidine kinase-, DNA gyrase B-, and HSP90-like ATPase-PAS fold-PAS fold
Polysacc_deac_1Polysaccharide deacetylase
Glyco_hydro_11Glycosyl hydrolases family 11
Response_reg-Sigma54_activat-HTH_8Response regulator receiver domain-Sigma-54 interaction domain-Bacterial regulatory protein, Fis family
Aminotran_3Aminotransferase class-III
AMP-binding-PP-bindingAMP-binding enzyme-Phosphopantetheine attachment site
Received: 2019-11-08
Accepted: 2019-11-22
Published Online: 2020-02-28

© 2020 Faten Dhawi published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

Articles in the same Issue

  1. Plant Sciences
  2. Dependence of the heterosis effect on genetic distance, determined using various molecular markers
  3. Plant Growth Promoting Rhizobacteria (PGPR) Regulated Phyto and Microbial Beneficial Protein Interactions
  4. Role of strigolactones: Signalling and crosstalk with other phytohormones
  5. An efficient protocol for regenerating shoots from paper mulberry (Broussonetia papyrifera) leaf explants
  6. Functional divergence and adaptive selection of KNOX gene family in plants
  7. In silico identification of Capsicum type III polyketide synthase genes and expression patterns in Capsicum annuum
  8. In vitro induction and characterisation of tetraploid drumstick tree (Moringa oleifera Lam.)
  9. CRISPR/Cas9 or prime editing? – It depends on…
  10. Study on the optimal antagonistic effect of a bacterial complex against Monilinia fructicola in peach
  11. Natural variation in stress response induced by low CO2 in Arabidopsis thaliana
  12. The complete mitogenome sequence of the coral lily (Lilium pumilum) and the Lanzhou lily (Lilium davidii) in China
  13. Ecology and Environmental Sciences
  14. Use of phosphatase and dehydrogenase activities in the assessment of calcium peroxide and citric acid effects in soil contaminated with petrol
  15. Analysis of ethanol dehydration using membrane separation processes
  16. Activity of Vip3Aa1 against Periplaneta americana
  17. Thermostable cellulase biosynthesis from Paenibacillus alvei and its utilization in lactic acid production by simultaneous saccharification and fermentation
  18. Spatiotemporal dynamics of terrestrial invertebrate assemblages in the riparian zone of the Wewe river, Ashanti region, Ghana
  19. Antifungal activity of selected volatile essential oils against Penicillium sp.
  20. Toxic effect of three imidazole ionic liquids on two terrestrial plants
  21. Biosurfactant production by a Bacillus megaterium strain
  22. Distribution and density of Lutraria rhynchaena Jonas, 1844 relate to sediment while reproduction shows multiple peaks per year in Cat Ba-Ha Long Bay, Vietnam
  23. Biomedical Sciences
  24. Treatment of Epilepsy Associated with Common Chromosomal Developmental Diseases
  25. A Mouse Model for Studying Stem Cell Effects on Regeneration of Hair Follicle Outer Root Sheaths
  26. Morphine modulates hippocampal neurogenesis and contextual memory extinction via miR-34c/Notch1 pathway in male ICR mice
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  41. Hepatoprotective effects of chamazulene against alcohol-induced liver damage by alleviation of oxidative stress in rat models
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  62. Neuroanatomy of melanocortin-4 receptor pathway in the mouse brain
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  79. miR-339-3p regulated acute pancreatitis induced by caerulein through targeting TNF receptor-associated factor 3 in AR42J cells
  80. LncRNA RP1-85F18.6 affects osteoblast cells by regulating the cell cycle
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  82. MiR-30c-5p/ROCK2 axis regulates cell proliferation, apoptosis and EMT via the PI3K/AKT signaling pathway in HG-induced HK-2 cells
  83. CTRP9 protects against MIA-induced inflammation and knee cartilage damage by deactivating the MAPK/NF-κB pathway in rats with osteoarthritis
  84. Relationship between hemodynamic parameters and portal venous pressure in cirrhosis patients with portal hypertension
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  109. Special Issue On New Approach To Obtain Bioactive Compounds And New Metabolites From Agro-Industrial By-Products
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  114. The impedance analysis of small intestine fusion by pulse source
  115. Errata
  116. Erratum to “Diagnostic performance of serum CK-MB, TNF-α and hs-CRP in children with viral myocarditis”
  117. Erratum to “MYL6B drives the capabilities of proliferation, invasion, and migration in rectal adenocarcinoma through the EMT process”
  118. Erratum to “Thermostable cellulase biosynthesis from Paenibacillus alvei and its utilization in lactic acid production by simultaneous saccharification and fermentation”
https://doi.org/10.1515/biol-2020-0008
Keywords for this article
Plant Growth promoting rhizobacteria; Sorghum; phylogenetic analysis; protein family; microbe interactions
Creative Commons
BY 4.0

Articles in the same Issue

  1. Plant Sciences
  2. Dependence of the heterosis effect on genetic distance, determined using various molecular markers
  3. Plant Growth Promoting Rhizobacteria (PGPR) Regulated Phyto and Microbial Beneficial Protein Interactions
  4. Role of strigolactones: Signalling and crosstalk with other phytohormones
  5. An efficient protocol for regenerating shoots from paper mulberry (Broussonetia papyrifera) leaf explants
  6. Functional divergence and adaptive selection of KNOX gene family in plants
  7. In silico identification of Capsicum type III polyketide synthase genes and expression patterns in Capsicum annuum
  8. In vitro induction and characterisation of tetraploid drumstick tree (Moringa oleifera Lam.)
  9. CRISPR/Cas9 or prime editing? – It depends on…
  10. Study on the optimal antagonistic effect of a bacterial complex against Monilinia fructicola in peach
  11. Natural variation in stress response induced by low CO2 in Arabidopsis thaliana
  12. The complete mitogenome sequence of the coral lily (Lilium pumilum) and the Lanzhou lily (Lilium davidii) in China
  13. Ecology and Environmental Sciences
  14. Use of phosphatase and dehydrogenase activities in the assessment of calcium peroxide and citric acid effects in soil contaminated with petrol
  15. Analysis of ethanol dehydration using membrane separation processes
  16. Activity of Vip3Aa1 against Periplaneta americana
  17. Thermostable cellulase biosynthesis from Paenibacillus alvei and its utilization in lactic acid production by simultaneous saccharification and fermentation
  18. Spatiotemporal dynamics of terrestrial invertebrate assemblages in the riparian zone of the Wewe river, Ashanti region, Ghana
  19. Antifungal activity of selected volatile essential oils against Penicillium sp.
  20. Toxic effect of three imidazole ionic liquids on two terrestrial plants
  21. Biosurfactant production by a Bacillus megaterium strain
  22. Distribution and density of Lutraria rhynchaena Jonas, 1844 relate to sediment while reproduction shows multiple peaks per year in Cat Ba-Ha Long Bay, Vietnam
  23. Biomedical Sciences
  24. Treatment of Epilepsy Associated with Common Chromosomal Developmental Diseases
  25. A Mouse Model for Studying Stem Cell Effects on Regeneration of Hair Follicle Outer Root Sheaths
  26. Morphine modulates hippocampal neurogenesis and contextual memory extinction via miR-34c/Notch1 pathway in male ICR mice
  27. Composition, Anticholinesterase and Antipedicular Activities of Satureja capitata L. Volatile Oil
  28. Weight loss may be unrelated to dietary intake in the imiquimod-induced plaque psoriasis mice model
  29. Construction of recombinant lentiviral vector containing human stem cell leukemia gene and its expression in interstitial cells of cajal
  30. Knockdown of lncRNA KCNQ1OT1 inhibits glioma progression by regulating miR-338-3p/RRM2
  31. Protective effect of asiaticoside on radiation-induced proliferation inhibition and DNA damage of fibroblasts and mice death
  32. Prevalence of dyslipidemia in Tibetan monks from Gansu Province, Northwest China
  33. Sevoflurane inhibits proliferation, invasion, but enhances apoptosis of lung cancer cells by Wnt/β-catenin signaling via regulating lncRNA PCAT6/ miR-326 axis
  34. MiR-542-3p suppresses neuroblastoma cell proliferation and invasion by downregulation of KDM1A and ZNF346
  35. Calcium Phosphate Cement Causes Nucleus Pulposus Cell Degeneration Through the ERK Signaling Pathway
  36. Human Dental Pulp Stem Cells Exhibit Osteogenic Differentiation Potential
  37. MiR-489-3p inhibits cell proliferation, migration, and invasion, and induces apoptosis, by targeting the BDNF-mediated PI3K/AKT pathway in glioblastoma
  38. Long non-coding RNA TUG1 knockdown hinders the tumorigenesis of multiple myeloma by regulating the microRNA-34a-5p/NOTCH1 signaling pathway
  39. Large Brunner’s gland adenoma of the duodenum for almost 10 years
  40. Neurotrophin-3 accelerates reendothelialization through inducing EPC mobilization and homing
  41. Hepatoprotective effects of chamazulene against alcohol-induced liver damage by alleviation of oxidative stress in rat models
  42. FXYD6 overexpression in HBV-related hepatocellular carcinoma with cirrhosis
  43. Risk factors for elevated serum colorectal cancer markers in patients with type 2 diabetes mellitus
  44. Effect of hepatic sympathetic nerve removal on energy metabolism in an animal model of cognitive impairment and its relationship to Glut2 expression
  45. Progress in research on the role of fibrinogen in lung cancer
  46. Advanced glycation end product levels were correlated with inflammation and carotid atherosclerosis in type 2 diabetes patients
  47. MiR-223-3p regulates cell viability, migration, invasion, and apoptosis of non-small cell lung cancer cells by targeting RHOB
  48. Knockdown of DDX46 inhibits trophoblast cell proliferation and migration through the PI3K/Akt/mTOR signaling pathway in preeclampsia
  49. Buformin suppresses osteosarcoma via targeting AMPK signaling pathway
  50. Effect of FibroScan test in antiviral therapy for HBV-infected patients with ALT <2 upper limit of normal
  51. LncRNA SNHG15 regulates osteosarcoma progression in vitro and in vivo via sponging miR-346 and regulating TRAF4 expression
  52. LINC00202 promotes retinoblastoma progression by regulating cell proliferation, apoptosis, and aerobic glycolysis through miR-204-5p/HMGCR axis
  53. Coexisting flavonoids and administration route effect on pharmacokinetics of Puerarin in MCAO rats
  54. GeneXpert Technology for the diagnosis of HIV-associated tuberculosis: Is scale-up worth it?
  55. Circ_001569 regulates FLOT2 expression to promote the proliferation, migration, invasion and EMT of osteosarcoma cells through sponging miR-185-5p
  56. Lnc-PICSAR contributes to cisplatin resistance by miR-485-5p/REV3L axis in cutaneous squamous cell carcinoma
  57. BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells
  58. MYL6B drives the capabilities of proliferation, invasion, and migration in rectal adenocarcinoma through the EMT process
  59. Inhibition of lncRNA LINC00461/miR-216a/aquaporin 4 pathway suppresses cell proliferation, migration, invasion, and chemoresistance in glioma
  60. Upregulation of miR-150-5p alleviates LPS-induced inflammatory response and apoptosis of RAW264.7 macrophages by targeting Notch1
  61. Long non-coding RNA LINC00704 promotes cell proliferation, migration, and invasion in papillary thyroid carcinoma via miR-204-5p/HMGB1 axis
  62. Neuroanatomy of melanocortin-4 receptor pathway in the mouse brain
  63. Lipopolysaccharides promote pulmonary fibrosis in silicosis through the aggravation of apoptosis and inflammation in alveolar macrophages
  64. Influences of advanced glycosylation end products on the inner blood–retinal barrier in a co-culture cell model in vitro
  65. MiR-4328 inhibits proliferation, metastasis and induces apoptosis in keloid fibroblasts by targeting BCL2 expression
  66. Aberrant expression of microRNA-132-3p and microRNA-146a-5p in Parkinson’s disease patients
  67. Long non-coding RNA SNHG3 accelerates progression in glioma by modulating miR-384/HDGF axis
  68. Long non-coding RNA NEAT1 mediates MPTP/MPP+-induced apoptosis via regulating the miR-124/KLF4 axis in Parkinson’s disease
  69. PCR-detectable Candida DNA exists a short period in the blood of systemic candidiasis murine model
  70. CircHIPK3/miR-381-3p axis modulates proliferation, migration, and glycolysis of lung cancer cells by regulating the AKT/mTOR signaling pathway
  71. Reversine and herbal Xiang–Sha–Liu–Jun–Zi decoction ameliorate thioacetamide-induced hepatic injury by regulating the RelA/NF-κB/caspase signaling pathway
  72. Therapeutic effects of coronary granulocyte colony-stimulating factor on rats with chronic ischemic heart disease
  73. The effects of yam gruel on lowering fasted blood glucose in T2DM rats
  74. Circ_0084043 promotes cell proliferation and glycolysis but blocks cell apoptosis in melanoma via circ_0084043-miR-31-KLF3 axis
  75. CircSAMD4A contributes to cell doxorubicin resistance in osteosarcoma by regulating the miR-218-5p/KLF8 axis
  76. Relationship of FTO gene variations with NAFLD risk in Chinese men
  77. The prognostic and predictive value of platelet parameters in diabetic and nondiabetic patients with sudden sensorineural hearing loss
  78. LncRNA SNHG15 contributes to doxorubicin resistance of osteosarcoma cells through targeting the miR-381-3p/GFRA1 axis
  79. miR-339-3p regulated acute pancreatitis induced by caerulein through targeting TNF receptor-associated factor 3 in AR42J cells
  80. LncRNA RP1-85F18.6 affects osteoblast cells by regulating the cell cycle
  81. MiR-203-3p inhibits the oxidative stress, inflammatory responses and apoptosis of mice podocytes induced by high glucose through regulating Sema3A expression
  82. MiR-30c-5p/ROCK2 axis regulates cell proliferation, apoptosis and EMT via the PI3K/AKT signaling pathway in HG-induced HK-2 cells
  83. CTRP9 protects against MIA-induced inflammation and knee cartilage damage by deactivating the MAPK/NF-κB pathway in rats with osteoarthritis
  84. Relationship between hemodynamic parameters and portal venous pressure in cirrhosis patients with portal hypertension
  85. Long noncoding RNA FTX ameliorates hydrogen peroxide-induced cardiomyocyte injury by regulating the miR-150/KLF13 axis
  86. Ropivacaine inhibits proliferation, migration, and invasion while inducing apoptosis of glioma cells by regulating the SNHG16/miR-424-5p axis
  87. CD11b is involved in coxsackievirus B3-induced viral myocarditis in mice by inducing Th17 cells
  88. Decitabine shows anti-acute myeloid leukemia potential via regulating the miR-212-5p/CCNT2 axis
  89. Testosterone aggravates cerebral vascular injury by reducing plasma HDL levels
  90. Bioengineering and Biotechnology
  91. PL/Vancomycin/Nano-hydroxyapatite Sustained-release Material to Treat Infectious Bone Defect
  92. The thickness of surface grafting layer on bio-materials directly mediates the immuno-reacitivity of macrophages in vitro
  93. Silver nanoparticles: synthesis, characterisation and biomedical applications
  94. Food Science
  95. Bread making potential of Triticum aestivum and Triticum spelta species
  96. Modeling the effect of heat treatment on fatty acid composition in home-made olive oil preparations
  97. Effect of addition of dried potato pulp on selected quality characteristics of shortcrust pastry cookies
  98. Preparation of konjac oligoglucomannans with different molecular weights and their in vitro and in vivo antioxidant activities
  99. Animal Sciences
  100. Changes in the fecal microbiome of the Yangtze finless porpoise during a short-term therapeutic treatment
  101. Agriculture
  102. Influence of inoculation with Lactobacillus on fermentation, production of 1,2-propanediol and 1-propanol as well as Maize silage aerobic stability
  103. Application of extrusion-cooking technology in hatchery waste management
  104. In-field screening for host plant resistance to Delia radicum and Brevicoryne brassicae within selected rapeseed cultivars and new interspecific hybrids
  105. Studying of the promotion mechanism of Bacillus subtilis QM3 on wheat seed germination based on β-amylase
  106. Rapid visual detection of FecB gene expression in sheep
  107. Effects of Bacillus megaterium on growth performance, serum biochemical parameters, antioxidant capacity, and immune function in suckling calves
  108. Effects of center pivot sprinkler fertigation on the yield of continuously cropped soybean
  109. Special Issue On New Approach To Obtain Bioactive Compounds And New Metabolites From Agro-Industrial By-Products
  110. Technological and antioxidant properties of proteins obtained from waste potato juice
  111. The aspects of microbial biomass use in the utilization of selected waste from the agro-food industry
  112. Special Issue on Computing and Artificial Techniques for Life Science Applications - Part I
  113. Automatic detection and segmentation of adenomatous colorectal polyps during colonoscopy using Mask R-CNN
  114. The impedance analysis of small intestine fusion by pulse source
  115. Errata
  116. Erratum to “Diagnostic performance of serum CK-MB, TNF-α and hs-CRP in children with viral myocarditis”
  117. Erratum to “MYL6B drives the capabilities of proliferation, invasion, and migration in rectal adenocarcinoma through the EMT process”
  118. Erratum to “Thermostable cellulase biosynthesis from Paenibacillus alvei and its utilization in lactic acid production by simultaneous saccharification and fermentation”
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