Table 2.

Recent studies indicating how PGPB help to ameliorate salt stress.

Plant	Bacteria	Comments	Reference
Arabidopsis thaliana (thale cress)	Paraburkholderia phytofirmans PsJN	A. thaliana plants inoculated with strain PsJN showed higher survival rate when exposed to long-term salinity and reduced Na+ accumulation within leaf tissues compared to uninoculated plants. Mutants defective in ACC deaminase, auxin catabolism, N-acyl-homoserine-lactone production, and flagellin synthesis showed a low relevance of these functions to salinity tolerance. Bacterial release of volatile organic compounds (mainly 2-undecanone, 7-hexanol, 3-methylbutanol and dimethyl disulphide) reproduced the effects of direct bacterial inoculation of roots, increasing plant growth rate and tolerance to salt stress conditions. Exposure of A. thaliana to different amounts of these molecules demonstrated their capability to affect growth, while exposure to a mixture of the first three compounds mimicked the effects of the bacterial strain on plant growth stimulation and salinity tolerance.	[73]
Arachis hypogaea L. (peanut)	Klebsiella sp., Pseudomonas sp., Agrobacterium sp., and Ochrobactrum sp. isolated from the halophyte Arthrocnemum indicum	Five diazotrophic salt-resistant strains of Klebsiella, Pseudomonas, Agrobacterium, and Ochrobactrum produced IAA and ACC deaminase, fixed N2, and solubilized phosphate. All of the isolates promoted peanut growth under non-stressful conditions and increased the N content in plants. In plants that were previously inoculated with these bacterial strains and then exposed to salt stress, accumulation of ROS-modulating enzymes and increased biomass was recorded compared to uninoculated ones.	[74]
Brassica campestris L. (canola)	Brevibacterium epidermidis RS15 and Bacillus aryabhattai RS341	120 mM NaCl reduced the rate of seed germination by 50%. Inoculation with B. epidermidis RS15 and B. aryabhattai RS34, both halotolerant and able to synthesize ACC deaminase, enhanced seed germination under salt stress and reduced the ACC content in seeds. Inoculation with both bacterial strains increased hydrolytic enzyme activities (amylase, invertase, and protease) and decreased ethylene levels compared to uninoculated seeds exposed to salt stress.	[75]
Camelina sativa (camelina or false flax)	Pseudomonas putida UW4, two root endophytes Pseudomonas migulae 8R6 and Pseudomonas fluoresces YsS6 (both ACC deaminase producing strains), and the acdS minus mutants 8R6M and YsS6M	Soil inoculation with wild-type strains increased shoot length without salt, and seed yield under moderate salinity. Transgenic plants that expressed the acdS gene, encoding the enzyme ACC deaminase, showed reduced inhibition of root lengthening and biomass development, and increased seed production, better seed quality, and higher levels of seed oil production under salt stress.	[76]
Camelina sativa (camelina or false flax)	Pseudomonas migulae 8R6	Both of the C. sativa plants treated with the ACC deaminase producing endophyte P. migulae 8R6 and transgenic plants expressing acdS demonstrated increased tolerance to salt. Inoculation with strain 8R6 positively impacted ethylene- and abscisic acid-dependent signalling. The expression of acdS in transgenic plants altered auxin, jasmonic acid, and brassinosteroid signalling and/biosynthesis. Expression of genes involved in carbohydrate metabolism were up-regulated, as was the expression of genes modulating the level of ROS released. The expression of the acdS gene also positively effected the expression of photosynthesis genes.	[77]
Camelina sativa (camelina or false flax)	Pseudomonas migulae 8R6	Treatment of C. sativa, grown under salt stress, with the endophyte P. migulae 8R6, able to synthesize ACC deaminase, induced a negative modulation of ethylene signaling as well as auxin and jasmonic acid biosynthesis and signaling, while genes involved in regulation of gibberellin signaling were positively affected. In plants cultivated with salt and inoculated with 8R6, a moderate expression of the acdS gene under the control of the rolD promoter occurred, which was highly efficient in lowering the expression of the genes involved in the synthesis of ethylene and its signaling.	[78]
Capsicum annuum (pepper)	Brevibacterium iodinum RS16, Bacillus licheniformis RS656, and Zhihengliuela alba RS111	Brevibacterium iodinum RS16, Bacillus licheniformis RS656, and Zhihengliuela alba RS111 were identified as both halotolerant and ACC deaminase producers. Single inoculation with the three bacterial strains in red pepper plants grown at three salinity levels induced lower ethylene production. Plant biomass and salt tolerance index (the ratio of the biomass of salt stressed to non-stressed plants) in inoculated plants was higher compared to non-inoculated plants.	[79]
Capsicum annuum L. (red pepper)	Pseudomonas frederiksbergensis OS261	Plants were inoculated with strain OS261 and grown with three levels of salt. Growth parameters (height and plant biomass) of plants were increased by the presence of the bacterial strain compared to uninoculated controls. The amount of ethylene synthesized by plants grown under salinity stress was high, but inoculation with strain OS261 reduced the release of this hormone. The level of antioxidant enzyme activity in leaves of inoculated plants grown in salinity was increased, while the H+ concentration was reduced.	[80]
Capsicum annuum L. cv. Bulmat (red pepper)	Pseudomonas frederiksbergensis OB139, Pseudomonas vancouverensis OB155	Plants were cultivated under four levels of salt concentration and inoculated or not with one or both strains. Salt stress inhibited plant growth through increased ethylene synthesis and the disruption of photosynthetic parameters compared to uninoculated plants. The combination of the two bacterial strains, both able to synthesize ACC deaminase, lowered ethylene levels in plants and increased catalase activity, leading to increased plant growth compared to a single bacterium or the uninoculated control.	[81]
Cicer arietinum L. (chickpea)	Mesorhizobium ciceri EE-7 (salt-sensitive) and Mesorhizobium ciceri G-55 (salt-tolerant)	Two isolates of M. ciceri, one that was salt sensitive and another that was salt tolerant, were transformed with an isolated acdS gene encoding ACC deaminase. Salt stress reduced the biomass of plants inoculated with the wild-type strains. The salt-tolerant bacterial strain induced a higher nodulation rate in chickpeas compared to the salt-sensitive strain. The shoot dry weight was increased in plants inoculated with the salt-sensitive transformant strain. In plants inoculated with the salt-sensitive transformant strain, nodulation was found to be comparable to that induced by the salt-tolerant strain.	[82]
Coriandrum sativum L. (coriander)	Azospirillum brasiliense and Azotobacter chroococcum	Inoculation of coriander seeds, exposed to four levels of salt stress, with a mixture of A. brasiliense and A. chroococcum enhanced chlorophyll content and increased grain yield and plant biomass compared to uninoculated plants. Combined inoculation and salt stress increased catalase and decreased the level of ascorbate peroxidase and guaiacol peroxidase compared to untreated plants. Inoculation with both PGPB lowered Na and increased the K concentration in coriander leaves compared to untreated plants. The presence of PGPB improved plant growth in both the absence and presence of salt stress conditions.	[83]
Cucumis sativus (cucumber)	Pseudomonas fluorescens, Bacillus megaterium, and Variovorax paradoxus	The ability to solubilize phosphates and synthesize ACC deaminase, siderophores, and IAA was assessed in the three PGPB strains grown at two salt concentrations (2 and 5% NaCl w/v). While B. megaterium was the least affected by high salinity, ACC deaminase activity as well as siderophore and IAA production in P. fluorescens remained unaffected under salt stress. On the contrary, V. paradoxus was not tolerant to salt, and its expression of plant beneficial traits was reduced by salinity. When inoculated onto cucumber plants grown at three different salinity levels, P. fluorescens was the most effective of the three strains at decreasing the inhibitory effects of salinity.	[84]
Hordeum vulgare L. (barley), Trifolium repens L. (clover), and Pennisetum glaucum L.R. Br. (pearl millet)	Pseudomonas putida UW3 and UW4	Barley, clover, and pearl millet plants grown in the presence of salt and inoculated with P. putida UW3 and UW4. P. putida UW4 increased barley biomass compared to uninoculated plants. Strain UW3 increased the biomass of the three crops. Shoot and root length and weight were increased in inoculated plants, suggesting a more efficient photosynthetic activity in the presence of the bacterial strains. Data from pulse amplitude modulation fluorometry showed that the reduction of plant photosynthetic activity induced by salt stress was recovered once the strains were applied.	[85]
Medicago sativa L. (alfalfa)	Bacillus megaterium NRCB001, Bacillus subtilis subsp. subtilis NRCB002, and Bacillus subtilis NRCB003	Thirteen bacterial strains were isolated from the rice rhizosphere and characterized for their plant beneficial traits. B. megaterium NRCB001, B. subtilis subsp. subtilis NRCB002, and B. subtilis NRCB003 synthesized auxin, siderophores, NH3, and ACC deaminase and solubilized phosphate and potassium. Strains NRCB001 and NRCB002 tolerated 1750 mM NaCl. The three strains were inoculated onto M. sativa grown under normal conditions and salinity stress. Strains NRCB002 and NRCB003 increased the dry weight of alfalfa compared with non-inoculated seedlings treated with 130 mM NaCl.	[86]
Oryza sativa L. (rice)	Streptomyces sp. GMKU 336 and its ACC deaminase-deficient mutant	Plants of Thai jasmine rice cultivar Khao Dok Mali 105 grown under salt stress were inoculated with the endophyte Streptomyces sp. GMKU 336 or with its mutant lacking ACC deaminase activity. Strain GMKU 336 increased plant growth and chlorophyll, proline, K+, Ca+, and water content. The amount of released ethylene was reduced, as was the content of ROS and Na+, and the Na+/K+ ratio, compared to uninoculated plants or to those inoculated with the mutant. Plants treated with the wild type showed down-regulation of genes involved in the ethylene synthesis pathway, ACO1 and EREBP1, while acdS was up-regulated. Genes involved in osmotic balance, Na+ transport, calmodulin, and antioxidant enzymes were upregulated.	[87]
Oryza sativa (rice)	Bacillus tequilensis 10b (UPMRB9)	The effect of strains 10b UPMRB9′ on the growth of rice that was grown in the presence of salt was assessed. Strain 10b UPMRB9′ improved osmoprotectant properties such as proline, the soluble sugar concentration, and the levels of the antioxidant enzymes uperoxide dismutase, peroxidase, and catalase. Rice inoculated with strain UPMRB9 accumulated a greater amount of N and Ca in plant tissues, suggesting that this strain could behave as a bio-augmenter to improve biochemical and nutritional features in rice plants under salinity stress.	[88]
Panax ginseng (ginseng)	Paenibacillus yonginensis DCY84T	The impact of strain DCY84T, able to synthesize IAA and siderophore and solubilize phosphate, was assessed under short- and long-term salinity stress. Ginseng seedlings inoculated with the bacterial strain, following exposure to salt stress, were protected by the induction of plant defense-related systems (ion transport, ROS scavenging enzymes, proline content, total sugars, and ABA biosynthetic genes), as well as genes involved in root hair formation. The metabolome of the seedlings treated with DCY84T and exposed to salt stress overlapped with that of control plants.	[89]
Pisum sativum (pea)	Bacillus marisflavi (CHR JH 203) and Bacillus cereus (BST YS1_42)	Inoculation of pea plants with B. marisflavi CHR JH 203 and B. cereus BST YS1_42, both synthesizing a high amount of ACC deaminase, grown under salinity, improved plant biomass as well as the amount of plant carbohydrates, reducing sugars, proteins, chlorophylls, phenol, flavonoids, and antioxidant enzymes levels. In addition, plant ROS scavenging genes, defense genes, and cell rescue genes were all overexpressed in inoculated plants in the presence of 1% NaCl.	[90]
Seidlitzia rosmarinus Ehrenb. ex Boiss (perennial-green desert species of saltwort)	Rothia terrae, Kocuria palustris, Pseudomonas baetica, Pseudomonas fluorescens Staphylococcus warneri, Staphylococcus epidermidis, Staphylococcus succinus, Paenibacillus amylolyticus, Brevibacterium frigoritolerans, Stenotrophomonas pavanii, Halomonas sulfidaeris, Planococcus salinarum, Planomicrobium koreense, Planococcus halocryophilus, Planomicrobium soli	Culturable endophytic bacteria from the halophytic plant Seidlitzia rosmarinus Ehrenb. ex Boiss. were isolated and characterized to evaluate their plant beneficial traits under salt stress. Root endophytes belonged to genera Rothia, Kocuria, Pseudomonas, Staphylococcus, Paenibacillus, and Brevibacterium; shoot isolates belonged to Staphylococcus, Rothia, Stenotrophomonas, Brevibacterium, Halomonas, Planococcus, Planomicrobium, and Pseudomonas genera; Staphylococcus, Rothia, and Brevibacterium occurred in both roots and shoots. Synthesis of IAA and ACC deaminase was higher in bacteria from roots than from shoots. Finally, S. pavanii JST3 and P. fluorescens JST2 improved both shoot and root growth of Lepidium sativuum under salinity conditions.	[91]
Solanum lycopersicum (tomato)	Pseudomonas azotoformans CHB 1107	Strain CHB 1107 wild-type (producing ACC deaminase) lowered ethylene and proline levels in tomato plants exposed to high salt levels, increasing the dry weights of shoots and roots compared with uninoculated plants. Plants that were inoculated with a mutant that lacked ACC deaminase activity showed reduced K, Ca, and Mn uptake compared with plants inoculated with the wild-type strain. The wild-type strain CHB 1107 reduced the uptake of Na by tomato plants compared with the mutant strain under salt stress. Tomato plants inoculated with the wild-type strain yielded a higher K/Na ratio than those that were inoculated with the mutant.	[92]
Sorghum vulgare (sorghum)	Pseudomonas migulae SVB3R2, SVB3R3, SVB3R4, Pseudomonas sp. SVB3R5, Pseudomonas brassicacearum SVB6R1	Sorghum, tomato, and cucumber bacterial endophytes were characterized by 16S rRNA sequence determination and tested for plant beneficial traits. The activity of five endophytes was tested on plants grown with salinity stress. Strains SVB3R3 and SVB3R4 increased plant biomass, and strains SVB3R3 and SVB3R4 and SVB6R1 decreased the symptoms of plant salinity stress. Only strain SVB6R1 could produce ACC deaminase.	[93]
Triticum aestivum (wheat)	Bacillus pumilus SU3, Bacillus aquimaris SU8, Bacillus pumilus SU10, Bacillus arsinicus SU13, Arthrobacter sp. SU18, Bacillus cereus SU24, Pseudomonas mendocina SU40, Bacillus aquimaris SU44, and Bacillus subtilis SU47	Salt-tolerant (ST) PGPB positively influenced the growth and yield of wheat in saline soil. All nine tested strains improved plant growth in saline soil under greenhouse conditions, with strain DU18 being the most efficient. Under field conditions, strains SU44 and SU8 were the best in increasing plant biomass. Plant inoculation with strain SU8 led to higher proline content and total soluble sugar accumulation in wheat, while strain SU44 resulted in a higher accumulation of reducing sugars. The amounts of N, K, and P in wheat leaves increased significantly after inoculation with all the strains; B. subtilis SU47 lowered the sodium (Na) content in wheat leaves.	[94]
Triticum aestivum (wheat)	Serratia marcescens CDP-13	Serratia marcescens CDP-13 is halotolerant, produces ACC deaminase, solubilizes phosphate, synthesizes siderophores and IAA, and fixes N2. Wheat inoculation with strain CDP-13 increased plant biomass under salinity stress, reducing inhibition of plant growth caused by salt and lowering the amount of osmoprotectants (such as proline, malondialdehyde, soluble sugar), protein, and IAA content in plants.	[95]
Triticum aestivum L. (wheat).	Bacillus megaterium PN89	B. megaterium PN89, able to synthesize IAA, induced increased germination rate and root and shoot length in wheat plants exposed to salt stress, compared to non-inoculated controls.	[96]
Triticum aestivum (wheat)	Brevibacterium frigoritolerans, Bacillus velezensis, and Bacillus thuringiensis	The expression of plant-beneficial traits of Br. frigoritolerans alone or in combination with B. velezensis and B. thuringiensis under six salinity levels was characterized, and the effects on wheat of these strains alone or in combination under salt stress were assessed. B. frigoritolerans was the most effective, both for physiological trait expression and wheat plant growth promotion. Under salinity stress, the mixed inoculation of the three bacterial strains was more efficient than any single inoculation.	[97]
Triticum durum (wheat)	Fourteen strains of the genera Streptomyces and Nocardiopsis	Fourteen Actinomycetes strains were tested for expression of plant-beneficial activities under salinity conditions. The isolates could solubilize inorganic phosphate and synthesize IAA, HCN, and ammonia when grown in the presence of different salt concentrations. The majority of the strains produced ACC deaminase. Plant inoculation with these strains improved biomass and yielded an increased amount of chlorophyll and proline compared to uninoculated plants, both with and without salt.	[98]
Vigna radiata L. (mung bean)	Enterobacter cloacae KBPD	Strain KBPD is an ACC deaminase producer, able to solubilize phosphates and synthesize IAA, siderophore, ammonia, hydrogen cyanide, and exopolysaccharide. V. radiata plants exposed to salinity and inoculated with this bacterial strain showed increased shoot length, root length, and fresh and dry weights. Inoculation with strain KBPD also reduced proline content in plants grown with salt stress.	[99]
Vigna radiata (L.) R. Wilczekspring (mung bean)	Rhizobium sp. LSMR-32 and Enterococcus mundtii LSMRS-3	Under salt stress conditions, separate inoculation with the two bacterial strains induced increased seed germination, grain yield, plant height, biomass, chlorophyll content, and nutrient uptake compared to uninoculated plants. Inoculation with both strains increased both symbiotic parameters (nodulation rate, nodule biomass, and leghaemoglobin amount) and soil phosphatase and dehydrogenase levels. The microbial consortium enhanced the level of proline and anti-oxidative enzymes.	[100]
Zea mays (maize)	Azospirillum lipoferum or Azotobacter chroococcum	Maize (corn) plants that were exposed to salt stress had reduced growth parameters, pigments, soluble proteins, K+, and a K+/Na+ ratio. Salinity led to increased levels of soluble sugars, proline, Na+, malondialdehyde, and peroxidase and catalase activity, while the activity of plant ascorbate peroxidase remained unaffected. Plants inoculated with A. lipoferum or A. chroococcum increased growth parameters, pigments, K+, osmolytes, K+/Na+ ratio, and the antioxidative enzymes in salt-affected maize. Both bacterial strains also lowered malondialdehyde and Na+ in maize plants.	[101]