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Article

Isolation, Characterization, and Genome Insight of Pseudomonas jordanii: A Novel Endophyte Enhancing Durum Wheat (Triticum turgidum ssp. durum) Growth under Salinity Stress

by
Randa N. Albdaiwi
1,*,
Tareq Alhindi
2,3,
Hala Khyami-Horani
2,
Shireen Hasan
3 and
Hesham M. Al-Younes
2
1
Department of Allied Medical Sciences, Zarqa University College, Al-Balqa Applied University, Al-Salt 19117, Jordan
2
Department of Biological Sciences, School of Science, The University of Jordan, Amman 11942, Jordan
3
Hamdi Mango Center for Scientific Research (HMCSR), The University of Jordan, Amman 11942, Jordan
*
Author to whom correspondence should be addressed.
Appl. Sci. 2024, 14(15), 6681; https://doi.org/10.3390/app14156681
Submission received: 1 June 2024 / Revised: 12 July 2024 / Accepted: 26 July 2024 / Published: 31 July 2024
(This article belongs to the Section Applied Microbiology)
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Abstract

:

Featured Application

Pseudomonas jordanii strain G34 is a newly identified bacterial species with unique genomic features that holds great potential as a biofertilizer to boost wheat productivity in saline soils.

Abstract

Pseudomonas jordanii strain G34 is a moderately halophilic endophytic bacterium isolated from the root tissue of durum wheat plants growing in the saline environment of the Jordan Valley’s Ghor Sweimeh region. Microscopic and biochemical analyses of P. jordanii strain G34 revealed that it is a Gram-negative, non-motile rod. It also exhibits capsule formation, catalase and oxidase positive reactions, indole positivity, citrate utilization, and non-glucose fermenting capability. Pseudomonas jordanii strain G34 showed growth-promoting effects on durum wheat seedlings grown under severe salinity stress conditions up to a 200 mM NaCl concentration. The draft genome of P. jordanii strain G34 comprises 5,142,528 base pairs (bp) and possesses a G + C content of 64.0%. It contains 57 RNA coding genes and is predicted to encode a total of 4675 protein-coding genes. Putative genes linked to various aspects of the bacterial endophyte lifestyle were identified including ion transport, motility, secretion, adhesion, delivery systems, and plant cell wall modification. Performing a comprehensive phylogenomic analysis identified P. jordanii as a new species, with its closest relative being P. argentinensis LMG 22563, sharing only around 40.2% digital DNA-DNA hybridization identity. Pseudomonas jordanii strain G34 holds great potential for future use as a biofertilizer in saline environments.

1. Introduction

The Jordan Valley, a region stretching from the Sea of Galilee to the Dead Sea, is known for its status as the lowest point on Earth, at an elevation of over 400 m below sea level. This region, also known as the Ghor, has a rich history of cultivation spanning thousands of years. However, in recent times, the area has faced challenges due to low rainfall and an increase in soil salinity. Soil salinity escalation is a significant global issue, affecting various regions in semi-arid areas such as the Jordan Valley [1]. Salinity exerts profound effects on cellular processes, leading to a range of morphological, physiological, and molecular alterations in plants [2,3]. The primary impact of salinity on plant growth and development arises from the imposition of osmotic stress, which directly affects water availability. This stress induces the cellular build-up of toxic ions, such as sodium (Na+) and chloride (Cl−), disrupts nutrient balance, and causes oxidative stress injury [4,5].
Numerous plant species have shown remarkable adaptations to thrive in these challenging habitats [6]. Plants commonly establish symbiotic relationships with endophytic bacteria, which facilitate their growth under stress conditions through various mechanisms. These bacteria enhance nutrient absorption by stimulating the uptake of nutrients, producing siderophores to capture iron, solubilizing phosphorus, and engaging in nitrogen fixation [7,8]. Additionally, they have the ability to generate specific bioactive secondary metabolites like phytohormones [9]. Furthermore, endophytic bacteria play a crucial role in maintaining plant health by combating pathogens such as fungi and bacteria [10].
Pseudomonas bacteria are classified within the phylum Pseudomonadota and belong to the family Pseudomonadaceae. This genus includes several motile, Gram-negative, rod-shaped species. Some of them are considered pathogenic, such as P. aeruginosa [11], an opportunistic human pathogen, and P. syringae, a plant pathogen [12], while other species have been identified as plant growth-promoting endophytes such as P. fluorescens [13], P. migulae [14], and P. graminis [15]. In a previous study, several bacterial endophytes colonizing durum wheat (Triticum turgidum ssp. durum) roots were isolated from saline fields in the Ghor region [16,17]. Here, we report the isolation and characterization of a new halotolerant endophyte, P. jordanii strain G34, associated with the roots of durum wheat plants in the saline environment of the Ghor Sweimeh region. Pseudomonas jordanii strain G34 significantly promotes durum wheat growth under severe salinity stress conditions. The draft genome of P. jordanii strain G34 has been sequenced, and detailed descriptions of its genome sequence and plant growth-promoting effects are provided. In conclusion, P. jordanii strain G34 is a new bacterial species with potential as a biofertilizer to enhance durum wheat growth in saline soils.

2. Materials and Methods

2.1. Endophytic Bacteria Isolation

A durum wheat root sample was collected from a cultivated saline field (EC = 6.50 dS/m) in Ghor Sweimeh (31°48′52″ N; 35°37′42″ E; elevation: −249 m below sea level), as described previously [16]. To isolate endophytic bacteria, root samples from a selected durum wheat plant were washed under tap water for 10 min to remove adhering soil particles. Subsequently, root tissues were disinfected by immersing them in 70% ethanol for 1 min, followed by rinsing with sterile distilled water. Surface sterilization was then performed using a 3% sodium hypochlorite solution with a small amount of Tween 20® (Sigma-Aldrich, Steinheim, Germany) for 10 min, followed by six rinses with sterile distilled water. The effectiveness of the root surface sterilization was confirmed by plating an aliquot (100 μL) from the sixth rinse solution onto nutrient agar (NA) supplemented with 10% NaCl and incubating for 5 days at 28 °C to check for microbial growth.
After ensuring the roots were sterile, the surface-sterilized root tissue (1 g) was macerated with a mortar and pestle in 10 mL of 1% NaCl solution. Thereafter, serial dilutions of the macerate were then prepared. Thereafter, 1 mL of the root extracts and the dilutions were spread onto NA medium supplemented with 10% NaCl. Afterwards, the plates were incubated at 28 °C and observed for bacterial colony formation for up to one week, following established protocols [18].
Distinct colonies showing unique morphological features were selected and purified through three rounds of subculturing on NA media supplemented with 10% NaCl and stored in a glycerol stock at −80 °C. One isolate, designated G34, was assigned a unique code indicating the collection site, with “34” representing the isolate number.

2.2. Characterization of Isolate G34

Cellular morphology, Gram staining, microscopic shape, capsule and endospore formation, and motility were assessed as previously described [19]. Additionally, colonies were examined for their morphological characteristics, including appearance, size, shape, margin, elevation, texture, pigmentation, and optical properties.
For Gram staining, one-day-old bacterial colonies grown on NA plates were smeared on microscopic slides, fixed, and stained using the conventional Gram stain technique [20]. The Gram stain results were evaluated microscopically using an oil immersion lens to determine the Gram reaction and cell morphology. Capsule presence was investigated using the India ink staining method, which allows visualization of the capsule as a clear halo surrounding the bacterial cell under a microscope. Endospore formation was assessed using the malachite green staining procedure, which stains endospores green while vegetative cells appear pink, followed by microscopic examination.
Bacterial motility was evaluated using two methods: the hanging drop technique and culturing in a semi-solid medium. For the hanging drop technique, a drop of bacterial suspension was placed on a glass depression slide and observed under a microscope to assess motility. For the semi-solid medium method, bacteria were inoculated into nutrient agar slant tubes, and motility was determined based on the spread of bacterial growth away from the inoculation site.
Various biochemical tests were conducted to detect specific enzymes and metabolic end products, as described previously [21]. These tests included assays for catalase and oxidase activities, as well as tests for indole production, IAA production, citrate utilization, and carbohydrate fermentation using Kligler’s Iron Agar (KIA).

2.3. Plant Growth Promoting Effect Assay

The growth-promoting effect of the isolate G34 on selected durum wheat lines during the germination stage under varying salinity conditions was investigated following the work in [11]. For this purpose, two durum wheat lines with contrasting salinity tolerance were selected: Tamaroi, an Australian cultivar known for its sensitivity to salt, and a salt-tolerant BC4F2 homozygous line carrying the TmHKT1;5-A gene (Line 5004, also known as NAX2) [22]. Seeds of both genotypes were sterilized by first washing with 70% ethanol for 1 min, followed by three rinses with sterile distilled water. Then, the seeds were soaked in a 1.5% sodium hypochlorite solution for 5 min, followed by six successive rinses with sterile water to ensure complete removal of the disinfectant. To verify the efficacy of the sterilization process, seeds from each genotype were plated on NA medium for 7 days, and the plates were carefully observed for any signs of microbial growth.
The bacterial inoculum was prepared from log-phase cultures (OD600 of 0.60) of isolate G34. The culture was centrifuged at 5000 rpm for 10 min, and the pellet was washed three times with sterile distilled water before being resuspended in 25 mL of sterile distilled water. For the growth-promoting effect assay, sterilized seeds were immersed in the bacterial suspension for 1 h, while control seeds were immersed in sterile water. After immersion, the seeds were air-dried under a laminar airflow cabinet for 2 h. The seeds were then placed in sterile plastic boxes lined with sterile filter papers soaked in 30 mL of varying NaCl concentrations (0, 80, 120, 160, and 200 mM). Each treatment had three replicates with 20 seeds per plate (10 seeds of Tamaroi and 10 seeds of Line 5004). The boxes were incubated in complete darkness at 22 °C for the first 3 days, followed by a photoperiod cycle of 14 h light and 10 h darkness for the remaining 7 days. The experiments were repeated twice. Germination percentage was assessed after 10 days, and the impact of bacterial inoculation on the root projected area, root length, and root volume (6 replicates) was evaluated using the WinRhizo root scanning software system (version 2009c; Regent Instruments, Inc., Quebec City, QC, Canada).

2.4. Genomic DNA Isolation, Library Preparation, and Sequencing

For the isolation of total genomic DNA (gDNA), the Wizard® Genomic DNA Purification Kit (Promega, Madison, WI, USA) was used following the manufacturer’s protocol using a 5 mL culture of isolate G34. The quality of the isolated gDNA was assessed using a 1% agarose gel stained with Red Safe (Intron, Biotek, Daejeon, Republic of Korea) and visualized with the Gel DocTM XR Gel Documentation System (Bio-Rad, Hercules, CA, USA). Additionally, the concentration of the gDNA was determined using a spectrophotometer (Smart-SpecTM plus spectrophotometer, BIO-RAD, Hercules, CA, USA). Subsequently, the gDNA underwent sequencing at Macrogen Inc. (Seoul, Republic of Korea) as a service, utilizing the Illumina NovaSeq® platform with TruSeq Nano DNA (350) library type and reads configured as paired-ends, with a read length of 151 bp (Illumina Way, San Diego, CA, USA).

2.5. Pre-Processing, Genome Assembly, and Annotation

FastQC v0.11.9 [23] was employed to evaluate the quality of the raw reads, followed by Fastp [24] for the removal of adaptor sequences and filtering out low-quality, short, or N-rich reads. De novo assembly of the sequence reads was conducted using SKESA v2.4.0 [25] with default parameters, resulting in a draft genome sequence comprising 36 scaffolds, which was subsequently submitted to NCBI databases. Genome annotation was performed using the Department of Energy Systems Biology Knowledgebase (KBase) server [26] and the Rapid Annotations using Subsystems Technology (RASTtk), both implemented in the PATRIC server [27], utilizing the default settings.

2.6. Bioinformatics Analysis

A set of phylogenetic trees were constructed suing the P. jordanii strain G34 draft genome and ten closely related Pseudomonas species, each with available published genomes: P. argentinensis LMG22563, P. straminea JCM 2783, P. punonensis CECT 8089, P. flavescens LMG 18387, P. daroniae FRB 228, P. seleniipraecipitans LMG 25475, P. dryadis FRB 230, P. yangonensis JCM 33396, P. guguanensis JCM 18416, P. sediminis PI11, and Staphylococcus aureus DSM 20231 as an outgroup. Phylogenomic analysis began with the KBase server [26], employing the species tree builder and OrthoANI (Orthologous Average Nucleotide Identity) via the Orthologous Average Nucleotide Identity Tool (OAT 0.93.1) software [28]. The genomic signature dissimilarity phylogenetic tree was constructed based on octanucleotide frequencies using the GScompare server (http://gscompare.ehu.eus/ accessed on 9 July 2024).
Digital DNA-DNA hybridization was performed using the Genome-to-Genome Distance Calculator 3.0 (GGDC) [29] available on the TYGS server (https://tygs.dsmz.de/ accessed on 9 July 2024), according to the formula d4. Phylogenetic tree construction utilized FastME 2.1.6. [30], employing Genome Blast Distance Phylogeny (GBDP) with branch lengths scaled according to the GBDP distance formula d5. Branch support values above 60% from 100 replications were included above the branches, with an average branch support of 80.6% [31].
Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR) prediction was conducted using the CRISPRCasFinder online program, (https://crisprcas.i2bc.paris-saclay.fr/CrisprCasFinder/Index, accessed on 1 March 2024) [32]. A pan-genomic analysis was performed using the KBase Compute Pangenome function and Pangenome Circle Plot [26]. The distribution of genome annotations was visually represented in a circular graphical display using the Comprehensive Genome Analysis function on the PATRIC server [33].

3. Results and Discussion

3.1. Isolate G34 Characteristics

Microscopic examination of the Gram-stained P. jordanii strain G34 revealed that the bacteria are Gram-negative rods (Figure 1), a common characteristic of many Pseudomonas species [34]. Moreover, P. jordanii strain G34 appeared to possess capsules but were non-endospore formers. The presence of capsules around the bacteria indicates potential adaptations for survival in various environments, possibly aiding in protection against environmental stresses [35]. Clearly, the bacteria cells were non-motile, as assessed by using the depression slide technique and the agar slant tubes, although some flagellar genes were identified during genome sequencing, but several Flagellin genes were missing. As to their arrangement, bacteria were seen as singles, confirmed microscopically by the Gram stain and the hanging drop methods.
Pseudomonas jordanii strain G34 is catalase positive, which can break down toxic hydrogen peroxide into water and oxygen (Figure 1). Catalase plays a crucial role in enhancing bacterial survival under oxidative stress conditions [36]. Also, P. jordanii strain G34 is oxidase positive, which can oxidize a colorless reagent into purple color. Pseudomonas jordanii strain G34 is indole positive because the red ring appeared at the top after the addition of a reagent and was able to produce indole-3-acetic acid (IAA), a growth-promoting hormone. The capability to produce IAA suggests a potential role for P. jordanii strain G34 in enhancing plant growth and development through hormone-mediated mechanisms [37]. For citrate, bacteria utilize citrate as a source of carbon, and the pH was reduced to change the color from blue into green. The bacteria cannot ferment glucose, as shown in the KIA test (Figure 1).

3.2. Plant Growth Promoting Assay

The influence of inoculating P. jordanii strain G34 on the germination and seedling growth of Tamaroi and Line 5004 genotypes under varying salinity levels was examined (Figure 2; Table 1). Salinity levels exceeding 80 mM led to a significant decrease in germination rates in both genotypes’ inoculated seeds. Remarkably, Line 5004 (with NAX2) displayed significantly higher germination rates and root growth under elevated NaCl concentrations (>80 mM) compared to Tamaroi. Incremental salinity levels up to 200 mM NaCl resulted in reduced root numbers in both wheat genotypes.
For non-saline conditions, both genotypes inoculated with P. jordanii strain G34 exhibited substantial growth improvement, evidenced by increased root length and related traits (Table 1). Previous studies have documented the ability of Pseudomonas spp. to promote plant growth through diverse mechanisms, including phytohormone production such as IAA and degradation by ACC deaminase activity, which aid in modulating plant stress responses [38]. Previous studies have shown that Pseudomonas species, among others, play a crucial role in promoting plant growth under saline conditions by solubilizing phosphate, producing phytohormones, and reducing salt-stress damage [39,40]. For example, Pseudomonas sp. (Q6B) increased seed germination and promoted the seedling height of tomato plants, while other isolates such as Q1B enhanced the leaf number [41]. Additionally, P. putida and P. aeruginosa have been reported to mitigate salt-stress in wheat plants by lowering levels of ethylene levels in stressed plants [42]. These findings highlight the potential use of Pseudomonas spp. to enhance plant growth in saline soils, making them effective biofertilizers for improving crop productivity and stress tolerance. Recent findings have further demonstrated significant positive effects on overall plant growth for both genotypes inoculated with P. jordanii strain G34, observed under greenhouse and field conditions, irrespective of saline or non-saline environments [43].

3.3. Pseudomonas jordanii Strain G34 Genome Insight

Pseudomonas jordanii strain G34’s draft genome comprised 30 contigs with a collective length of 5,142,528 bp, featuring a G + C content of 64.01% and an N50 value of 353,980 bp (Table S1). The predicted number of coding genes was 4766, including 57 RNA coding genes and 4675 protein-coding genes, with the RNA coding genes consisting of 54 transfer RNAs (tRNAs) and 3 rRNAs. Taxonomic analysis based on whole-genome sequencing indicated a close relationship between P. jordanii strain G34 and P. argentinensis LMG22563, with a shared digital DNA-DNA hybridization (dDDH) identity of 40.2%, as shown in Figure 3A. This finding is supported by comparing genomic signatures, emphasizing the novelty of P. jordanii strain G34 as a distinct species and highlighting its promising potential as a biofertilizer, similar to P. argentinensis LMG22563.
A pangenome analysis was carried out to assess the differences between P. jordanii strain G34 and the closely related species revealed through whole-genome alignment (shown in the phylogenetic trees of Figure 3). The analysis covers all genes within a group of related organisms that are classified by sequence homology. At first, specific gene clades were identified by comparing the genomes of P. jordanii strain G34 with P. argentinensis LMG22563, using P. stutzeri as an outgroup (Figure 4A). Later on, the comparison was broadened to encompass all 21 closely related species identified during the whole-genome alignment step (Figure 4B). The pangenome analysis revealed significant differences, especially the abundance of unique sequences (base singletons) between P. jordanii strain G34 and P. argentinensis LMG22563, reinforcing the classification of P. jordanii strain G34 as a distinct species. This genomic divergence is significant in elucidating the distinct characteristics and potential applications of strain G34, particularly in enhancing plant growth under stress conditions [44]. The prevalence of unique sequences in P. jordanii strain G34 suggests specialized adaptations that could be harnessed for the development of agricultural biofertilizers, akin to other beneficial Pseudomonas species [45].
RASTtk annotation, available through the PATRIC server [26], was utilized to classify the functional genes in P. jordanii strain G34. Among the annotated genes, 992 were hypothetical proteins, while 3764 had functional assignments (Table S2). Of these, 1126 were assigned Enzyme Commission (EC) numbers, 961 had Gene Ontology (GO) assignments, and 849 were mapped to KEGG pathways [46,47,48]. Furthermore, the annotation revealed 4516 proteins belonging to cross-genus protein families (PGFams) and 4485 proteins belonging to genus-specific protein families (PLFams) [49]. In addition, four CRISPR systems were identified in P. jordanii strain G34 (Table S3). Intriguingly, the genome of P. argentinensis LMG22563 lacks a CRISPR system entirely. The classification of CRISPR-Cas variants is deemed significant in comparative genomic analysis for understanding the evolutionary relationships among related species [50].
The annotation analysis revealed a substantial number of predicted genes involved in carbohydrate metabolism, encompassing pathways for fructose, xylose, and the biosynthesis of menaquinone and quinone cofactors. These genes hold potential as alternative electron transporters in photosynthesis, potentially acting as vital redox molecules (Figure 5). Moreover, genes linked to nitrogen, phosphate, sulfur, iron, and sodium acquisition were detected. Additionally, genes involved in IAA biosynthesis, a pivotal plant hormone, were observed, indicating their potential significance in the symbiotic interactions between plants and bacteria [51].
Genes potentially involved in various crucial processes such as plant cell wall modification, secretion, membrane proteins, and transport systems, along with transcriptional regulators, ammonia and sulfur assimilation, and siderophores production, were identified. Furthermore, genes associated with tolerance mechanisms against osmotic and heat stress, detoxification, and heavy metal stress, including cobalt, zinc, and copper, were also detected (Table S4). Moreover, the presence of antibiotic resistance genes against fluoroquinolones, bleomycin, and fosmidomycin was detected (the annotated genes list is available online: BioProject PRJNA991609). Notably, the ACC deaminase gene, often linked to plant growth promotion in some endophytes, was absent in P. jordanii strain G34, suggesting alternative mechanisms for its contribution to alleviate stress effects on plant growth [52].
Several metabolic pathways identified in P. jordanii strain G34 hint at its potential for promoting plant growth and align well with its endophytic nature. These pathways include plastoquinone biosynthesis, carbon fixation, carotenoid biosynthesis, nitrogen metabolism, sulfur metabolism, and steroid hormone biosynthesis. Moreover, enzymes associated with the degradation of phenol, starch, sucrose, and xenobiotics were also detected, suggesting potential applications in the bioremediation industry. Notably, the presence of antibiotic biosynthesis monooxygenase hints at a possible role in the biosynthesis of aromatic polyketides.
Given the draft genome of P. jordanii strain G34 as a new species, future investigations into its transcriptome and molecular analyses are needed to offer insights into the functions of the novel proteins identified herein. These studies hold promise for uncovering the mechanisms through which this endophyte enhances plant growth [53]. Recent research on the closely related species P. argentinensis LMG22563 revealed its effectiveness in enhancing plant growth under drought conditions through ABA-mediated root architecture and epigenetic reprogramming [54]. Additionally, P. jordanii strain G34 demonstrated efficacy in enhancing growth under both greenhouse and field conditions and in mitigating negative salinity effects in a salt-sensitive genotype [43]. However, further investigation is needed to elucidate genotype-specific responses and the molecular mechanisms underlying genotype–bacteria interactions under saline conditions. In conclusion, bacterial whole-genome sequencing, coupled with comparative genomic analysis, continues to prove essential and effective for distinguishing closely related bacterial species. This approach not only enhances our understanding but also accelerates the identification of new species within environmental samples with potential use in crop improvement under stress conditions [55,56,57].

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/app14156681/s1, Table S1: Genome features of P. jordanii strain G34; Table S2: Protein features of P. jordanii strain G34; Table S3: Clustered Regularly interspaced Short Palindromic Repeats (CRiSPR) sequences present within P. jordanii strain G34 identified using CRiSPRCasFinder; Table S4: List of key specialty genes present in P. jordanii strain G34.

Author Contributions

R.N.A. and T.A. conceived and designed the experiments, collected and analyzed the data, and wrote the manuscript. Sample collection, identification, and microbiological work were performed by R.N.A., H.K.-H. and H.M.A.-Y. The plant growth-promoting effect assays were conducted by R.N.A. and S.H. Bioinformatic analysis was carried out by T.A. All authors contributed to the manuscript’s critical review and editing. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by the Deanship of Scientific Research—The University of Jordan, Grant Number 2350.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The draft genome project’s data, including raw sequences and the assembled genome consisting of 30 scaffolds, are available in GenBank under BioProject ID PRJNA991609 and BioSample ID SAMN36307955. Further details can be found in the article and Supplementary Materials.

Acknowledgments

We would like to acknowledge and thank the Deanship of Scientific Research at the University of Jordan for their financial support and Hamdi Mango Center for Scientific Research (HMCSR), The University of Jordan for their technical support.

Conflicts of Interest

The authors have no conflicts of interest to declare.

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Figure 1. Cellular, colonial morphology, and biochemical tests of P. jordanii strain G34.
Figure 1. Cellular, colonial morphology, and biochemical tests of P. jordanii strain G34.
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Figure 2. Pseudomonas jordanii strain G34 growth-promoting effect on the seedling root growth of Tamaroi and Line 5004 durum wheat genotypes subjected to different levels of salinity.
Figure 2. Pseudomonas jordanii strain G34 growth-promoting effect on the seedling root growth of Tamaroi and Line 5004 durum wheat genotypes subjected to different levels of salinity.
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Figure 3. (A) Phylogenetic tree based on whole-genome sequences; species clusters are indicated with corresponding color codes, the GC% is represented in the blue color intensity. The genome size is indicated by a black bar and the protein count are represented by the brown bars, respectively. (B) The genomic signatures-based phylogenetic tree showing octanucleotides frequencies along the scale beneath the tree.
Figure 3. (A) Phylogenetic tree based on whole-genome sequences; species clusters are indicated with corresponding color codes, the GC% is represented in the blue color intensity. The genome size is indicated by a black bar and the protein count are represented by the brown bars, respectively. (B) The genomic signatures-based phylogenetic tree showing octanucleotides frequencies along the scale beneath the tree.
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Figure 4. Pangenome analysis results: (A) Comparing the genomes of P. jordanii strain G34 with P. argentinensis LMG22563, with P. stutzeri as an outgroup. (B) Comparing the genome of P. jordanii strain G34 with 21 closely related species. The red lines denote singletons, representing genes that lack sequence homology with genes in any other genomes; Non-core genes are represented by the cyan lines; Clade-specific core orthologs identified in all genomes except the outgroup are represented by the purple lines; The dark blue lines represent core ortholog sets with at least one gene from the ortholog set present in each of the genomes; Pangenome non-core orthologs between core and singleton clusters present in more than one genome are represented by the grey lines.
Figure 4. Pangenome analysis results: (A) Comparing the genomes of P. jordanii strain G34 with P. argentinensis LMG22563, with P. stutzeri as an outgroup. (B) Comparing the genome of P. jordanii strain G34 with 21 closely related species. The red lines denote singletons, representing genes that lack sequence homology with genes in any other genomes; Non-core genes are represented by the cyan lines; Clade-specific core orthologs identified in all genomes except the outgroup are represented by the purple lines; The dark blue lines represent core ortholog sets with at least one gene from the ortholog set present in each of the genomes; Pangenome non-core orthologs between core and singleton clusters present in more than one genome are represented by the grey lines.
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Figure 5. (A) The graphical circular display illustrates the distribution of genome annotations for P. jordanii strain G34. The outer to inner rings describe contigs (1), coding sequences (CDS) on the forward (2) and reverse (3) strands, GC content (4), and GC skew (5), RNA genes (6), CDS with homology to known virulence factors (7), and CDS with homology to known antimicrobial resistance genes (8). (B) The functional classification of predicted genes in the P. jordanii G34 genome performed using RASTtk annotation.
Figure 5. (A) The graphical circular display illustrates the distribution of genome annotations for P. jordanii strain G34. The outer to inner rings describe contigs (1), coding sequences (CDS) on the forward (2) and reverse (3) strands, GC content (4), and GC skew (5), RNA genes (6), CDS with homology to known virulence factors (7), and CDS with homology to known antimicrobial resistance genes (8). (B) The functional classification of predicted genes in the P. jordanii G34 genome performed using RASTtk annotation.
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Table 1. Effect of inoculation with P. jordanii strain G34 on germination (%) and root characteristics (surface area (cm2), length (cm), and volume (cm3)) in Tamaroi and Line 5004 durum wheat genotypes subjected to different salinity levels after 10 days of culture.
Table 1. Effect of inoculation with P. jordanii strain G34 on germination (%) and root characteristics (surface area (cm2), length (cm), and volume (cm3)) in Tamaroi and Line 5004 durum wheat genotypes subjected to different salinity levels after 10 days of culture.
Germination %Surface AreaLengthVolume
Salt levelBacteriaTamaroiLine 5004TamaroiLine 5004TamaroiLine 5004TamaroiLine 5004
0 mMControl100%100%4.44 ± 1.01 *5.66 ± 0.4430.89 ± 2.4334.70 ± 2.590.46 ± 0.080.47 ± 0.11
P. jordanii100%100%8.82 ± 0.738.92 ± 0.2964.95 ± 3.1267.28 ± 3.030.43 ± 0.020.42 ± 0.01
80 mMControl100%100%2.07 ± 0.053.36 ± 0.3010.34 ± 0.3718.14 ± 0.980.64 ± 0.040.65 ± 0.18
P. jordanii100%100%5.20 ± 0.216.12 ± 0.1738.32 ± 1.5545.00 ± 1.950.43 ± 0.010.43 ± 0.02
160 mMControl71.67%81.67%0.46 ± 0.061.00 ± 0.162.13 ± 0.323.11 ± 0.130.66 ± 0.041.02 ± 0.14
P. jordanii86.67%100%3.30 ± 0.123.91 ± 0.2323.36 ± 0.1628.54 ± 0.240.45 ± 0.020.44 ± 0.03
200 mMControl53.33%66.67%0.44 ± 0.030.72 ± 0.170.78 ± 0.241.78 ± 0.421.90 ± 0.541.28 ± 0.07
P. jordanii81.67%86.67%1.53 ± 0.212.79 ± 0.2710.67 ± 0.2317.31 ± 1.180.46 ± 0.050.51 ± 0.03
* values are the mean (n = 6) ± standard deviation.
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Albdaiwi, R.N.; Alhindi, T.; Khyami-Horani, H.; Hasan, S.; Al-Younes, H.M. Isolation, Characterization, and Genome Insight of Pseudomonas jordanii: A Novel Endophyte Enhancing Durum Wheat (Triticum turgidum ssp. durum) Growth under Salinity Stress. Appl. Sci. 2024, 14, 6681. https://doi.org/10.3390/app14156681

AMA Style

Albdaiwi RN, Alhindi T, Khyami-Horani H, Hasan S, Al-Younes HM. Isolation, Characterization, and Genome Insight of Pseudomonas jordanii: A Novel Endophyte Enhancing Durum Wheat (Triticum turgidum ssp. durum) Growth under Salinity Stress. Applied Sciences. 2024; 14(15):6681. https://doi.org/10.3390/app14156681

Chicago/Turabian Style

Albdaiwi, Randa N., Tareq Alhindi, Hala Khyami-Horani, Shireen Hasan, and Hesham M. Al-Younes. 2024. "Isolation, Characterization, and Genome Insight of Pseudomonas jordanii: A Novel Endophyte Enhancing Durum Wheat (Triticum turgidum ssp. durum) Growth under Salinity Stress" Applied Sciences 14, no. 15: 6681. https://doi.org/10.3390/app14156681

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