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Review

Pseudomonas 1-Aminocyclopropane-1-carboxylate (ACC) Deaminase and Its Role in Beneficial Plant-Microbe Interactions

by
Bernard R. Glick
1 and
Francisco X. Nascimento
2,*
1
Department of Biology, University of Waterloo, Waterloo, ON N2L 3G1, Canada
2
iBET, Instituto de Biologia Experimental e Tecnológica, Apartado 12, 2781-901 Oeiras, Portugal
*
Author to whom correspondence should be addressed.
Microorganisms 2021, 9(12), 2467; https://doi.org/10.3390/microorganisms9122467
Submission received: 9 November 2021 / Revised: 26 November 2021 / Accepted: 26 November 2021 / Published: 29 November 2021
(This article belongs to the Special Issue Microbial Plant Hormone Modulation and Its Impact on Plant Growth, Development and Stress Resistance)
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Abstract

:
The expression of the enzyme 1-aminocylopropane-1-carboxylate (ACC) deaminase, and the consequent modulation of plant ACC and ethylene concentrations, is one of the most important features of plant-associated bacteria. By decreasing plant ACC and ethylene concentrations, ACC deaminase-producing bacteria can overcome some of the deleterious effects of inhibitory levels of ACC and ethylene in various aspects of plant-microbe interactions, as well as plant growth and development (especially under stressful conditions). As a result, the acdS gene, encoding ACC deaminase, is often prevalent and positively selected in the microbiome of plants. Several members of the genus Pseudomonas are widely prevalent in the microbiome of plants worldwide. Due to its adaptation to a plant-associated lifestyle many Pseudomonas strains are of great interest for the development of novel sustainable agricultural and biotechnological solutions, especially those presenting ACC deaminase activity. This manuscript discusses several aspects of ACC deaminase and its role in the increased plant growth promotion, plant protection against abiotic and biotic stress and promotion of the rhizobial nodulation process by Pseudomonas. Knowledge regarding the properties and actions of ACC deaminase-producing Pseudomonas is key for a better understanding of plant-microbe interactions and the selection of highly effective strains for various applications in agriculture and biotechnology.

1. Introduction

The unacceptable levels of pollution and other negative environmental impacts caused using chemical fertilizers and pesticides in agriculture is a major threat to food/soil security and overall human and animal health. Hence, achieving sustainable and efficient agricultural practices is one of the major challenges of this century.
The direct application of plant-growth-promoting bacteria (PGPB), beneficial members of the plant and soil microbiome, is a powerful alternative to the use of polluting chemical compounds [1]. These bacteria may facilitate plant growth, development and stress resistance through a wide range of mechanisms, including the manipulation of plant hormone levels [2].
Pseudomonas is a highly diverse bacterial genus that currently encompasses more than 250 species, including common members of the known plant and soil microbiomes worldwide and several PGPB. Because of their increased metabolic versatility, fast growth rate, biocontrol activities, ability to survive in a variety of soils and to directly interact with plant hosts, several Pseudomonas strains are of particular interest for the development of products for agricultural and biotechnological applications. Nevertheless, the selection of highly effective PGP Pseudomonas strains is still a challenge.
One way to address this challenge resides with the selection of Pseudomonas strains presenting the ability to manipulate plant hormone concentrations, specifically the gaseous plant hormone ethylene, which is an important regulator of multiple aspects of plant development as well as stress resistance and plant-microbe interactions [3,4]. In this regard, the expression of 1-aminocyclopropane-1-carboxylate (ACC) deaminase, an enzyme that is responsible for the cleavage of the non-proteinogenic amino acid ACC [5], the immediate precursor of ethylene in all higher plants, plays a key role in the bacterial ability to modulate plant ethylene levels [6]. The capacity to consume plant ACC has been demonstrated to increase the PGP abilities of numerous bacterial strains, including Pseudomonas spp. Importantly, several studies have revealed that the acdS gene encoding the ACC deaminase enzyme is highly prevalent and positively selected in bacteria that closely associate with plants [7], including a large number of rhizobial symbionts (those belonging to both the Alpha and Betaproteobacteria classes) [8]. Moreover, The microbiome of plants that normally grow under stress conditions is typically enriched in acdS-containing bacteria, including Pseudomonas [9,10,11].
In this work, several aspects of Pseudomonas ACC deaminase production and its important role in plant-microbe interactions are reviewed in detail.

2. Pseudomonas: Common and Important Members of the Plant Microbiome

Bacteria belonging to the genus Pseudomonas are commonly found worldwide in soils and in close association with plants. This diverse group of bacteria (polyphyletic) [12] can be found in the plant rhizosphere (the portion of soil directly associated with the plant roots) [13,14,15], but also colonizing internal plant tissues (acting as endophytes) [16,17], external plant tissues such as shoots and leaves (acting as epiphytes) [18,19], as well as some specialized plant organs like leguminous plant root nodules [20,21,22]. Soil- and plant-associated Pseudomonas strains may also present different ecological roles, ranging from beneficial actions to pathogenicity (e.g., P. syringae group species) [23].
Beneficial Pseudomonas play key roles in soil nutrient cycles (N, P, K, C), soil health via the catabolism of several deleterious compounds (e.g., heavy metals and aromatic compounds) and the suppression of several pathogens by producing a wide range of antimicrobial compounds such as lipopeptides and antibiotics [24,25,26,27]. When associated with plants, Pseudomonas strains may potentiate its host’s growth by facilitating nutrient acquisition (P, N, K, Fe) [28,29,30,31], or by the modulation of plant hormone concentrations (e.g., indoleacetic acid (IAA) biosynthesis and catabolism, biosynthesis of cytokinins, catabolism of ACC) [32,33,34,35]. Moreover, several Pseudomonas strains activate plant defense responses and induce systemic resistance through the activation of specific plant signaling mechanisms via their Microbe-Associated Molecular Patterns (MAMPs), effectors and other synthesized compounds [36].

3. Ethylene and ACC: Master Regulators of Plant Growth, Development, and Plant-Microbe Interactions

Ethylene (C2H4) is a gaseous plant hormone that is synthesized in plants via an ACC-dependent pathway in which methionine and S-adenosyl-l-Methionine (SAM) are the major precursors (Yang cycle) [37]. Plant SAM is converted to ACC by the enzyme ACC synthase, and then, ACC may be directly converted to ethylene by the enzyme ACC oxidase. These represent the key and limiting steps in ACC and ethylene biosynthesis. Additionally, ACC may be conjugated to other forms such as M-ACC (malonyl-ACC), G-ACC (glutamyl-ACC) and J-ACC (jasmonoyl-ACC) that can be accumulated and transported within plant tissues [3].
Ethylene regulates several aspects of plant growth and development, such as root and shoot elongation, leaf growth, flowering, fruit development and ripening, and root nodule development [38]. Ethylene also regulates the direct responses to biotic and abiotic stresses [4], as well as general plant-bacterial interactions [3], including the symbiotic nodulation process [39].
While ACC was first thought to act only as the ethylene precursor, recent studies have revealed that the role of this non-proteinogenic alpha amino acid is more important than previously thought. These studies showed that ACC may regulate several processes of plant development (e.g., cell division, root elongation) and act as a signaling molecule, independently from ethylene [40,41,42,43,44,45,46,47]. Importantly, Tsang and colleagues [41] showed that bacterial flagellin, a major MAMP and a known inducer of the plant defense response, activated an ACC-dependent and ethylene-independent mechanism involved in the regulation of root elongation. This result indicates that ACC plays a significant role in plant-microbe interactions. Since plant ACC can be transported and exuded [48,49,50], it may also play a significant role as a signaling molecule in the rhizosphere and phyllosphere [3].

4. Bacterial ACC Deaminase and the Manipulation of Plant ACC and Ethylene Levels

The ACC deaminase enzyme directly cleaves ACC, resulting in its conversion into ammonia and alpha-ketobutyrate [5] that can then be used as sole N and C sources by plant-associated bacteria (Figure 1A). ACC deaminase, encoded by the acdS gene, is a multimeric enzyme with a subunit molecular mass ranging from 36–42 KDa that is mostly prevalent within soil and plant-associated Proteobacteria (Alpha, Beta, Gamma) and Actinobacteria [7], although it is also found in several other types of bacteria and some fungi. This enzyme is located in the bacterial cytoplasm (i.e., it is not secreted) [51], which is consistent with the lack of transmembrane and/or signal peptides in its sequence, as well as the data regarding its optimal functioning conditions (pH 7–8, the cytoplasmic pH).
Importantly, ACC deaminase-producing bacteria (rhizospheric, endophytic, or epiphytic) can modulate the concentrations of ACC (i) in the rhizosphere and phyllosphere by consuming plant’s exuded ACC, or (ii) within plant tissues (e.g., the endosphere and root nodules), thus, directly limiting the actions of ACC, and subsequently limiting the production of ethylene by the plant host (Figure 1B).
The production of ACC deaminase by plant-associated bacteria and the consequent decrease of plant ACC and ethylene levels results in increased (i) bacterial colonization/competitiveness [52,53], (ii) bacterial nodulation abilities [54,55,56], (iii) plant growth promotion [57,58,59], and (iv) plant tolerance to biotic and abiotic stress [17,60,61,62,63]. Due to its significant impact in plant-microbe interactions, the acdS gene is positively selected in plant-associated bacteria including many rhizobial symbionts [8]. For instance, the acdS gene was detected in 234 of 395 NodC-containing rhizobia (Alpha and Betaproteobacteria), and in many of these strains the acdS gene is maintained in transmissible symbiotic islands and plasmids that also contain the nod (nodulation) and nif (nitrogen fixation) genes [8]. Moreover, the prevalence of acdS genes in rhizobial populations is connected to their ability to nodulate specific leguminous plant hosts, suggesting that the plant host plays a role in the selection of ACC/ethylene-modulating genes.
The acdS gene is also highly prevalent in the microbial communities of plants subjected to stress conditions [9,10,11]. For example, the abundance of ACC deaminase-producing bacteria was significantly increased in the rhizosphere of wild barley growing under stressful conditions when compared to wild barley grown under non-stressful conditions [9]. Similarly, the presence of ACC deaminase-producing bacteria was increased in the Brassica napus (canola) rhizosphere when the plant was cultivated in a heavy metal contaminated soil [10]. Moreover, the seeds of Arabidopsis thaliana exposed to cadmium for several generations contained more ACC deaminase-producing bacteria, including Pseudomonas spp., than the seeds of plants that were never exposed to cadmium stress [11].

5. Insights into the Prevalence and Evolution of ACC Deaminase in the Genus Pseudomonas

The ACC deaminase gene is present in 2591 Pseudomonas genomes (accessed in August 2021), including 39 Pseudomonas type strain genomes (Table 1). ACC deaminase was mostly detected in members of the following Pseudomonas genomic groups/subgroups (previously determined in Girard et al. [64]): P. syringae group (P. syringae, P. amygdali, P. avellanae, P. asturiensis, P. cannabina, P. capsici, P. caricapapayae, P. caspiana, P. cichorii, P. congelans, P. ficuserectae, P. floridensis, P. foliumensis, P. tremae, P. triticumensis, P. viridiflava); P. fluorescens subgroup (P. grimontii, P. marginalis, P. palleroniana, P. panacis), P. corrugata subgroup (P. bijieensis, P. brassicacearum, P. kilonensis, P. ogarae, P. tehranensis, P. thivervalensis, P. viciae; P. zarinae); P. mandelii subgroup (P. farris, P. migulae); P. massiliensis group (P. typographi); P. gessardii group (P. gessardii); P. asplenii subgroup (P. fuscovaginae); P. straminea group (P. flavescens); P. anguilliseptica group (P. benzenivorans); P. oryzihabitans group (P. oryzihabitans, P. psychrotolerans, P. rhizoryzae).
Overall, the majority of the AcdS-containing Pseudomonas strains clustered in specific Pseudomonas groups/subgroups (Figure 2A) and most of acdS genes presented similar GC% when compared to the strain overall genome GC% (Table 1), indicating that the presence and evolution of ACC deaminase is mostly linked to the overall strain’s genomic properties/evolutionary history [7]. Nevertheless, the phylogenetic and comparative analysis based on 576 core genes (Figure 2A) and AcdS (Figure 2B) sequences showed that AcdS evolution in some Pseudomonas clades is difficult to resolve. The data suggests that some clades (e.g., P. fluorescens group) have possibly acquired acdS genes via past horizontal gene transfer (HGT) or recombination events between Pseudomonas strains that occurred in a more recent time. For example, members of the P. fluorescens subgroup could be easily distinguished based on their core genes (576 protein sequences) (Figure 2A), however, its AcdS sequences were highly similar to those of members of the P. corrugata and P. mandelli subgroups (Figure 2B). Alternatively, the acdS gene is less prone to modifications in these Pseudomonas subgroups.
Pseudomonas flavescens LMG 18387T and P. fuscovaginae ICMP 5940T seem to have indeed acquired acdS genes via HGT from other members of the Pseudomonas genus. The analysis also suggested that some Pseudomonas may have acquired acdS genes through more distant HGT events (between less related strains). This seems to be the case for P. benzenivorans DSM 8628T, which possesses an acdS gene presenting a GC% of 55.4 despite presenting an overall genomic GC% of 65.2. The phylogram based on AcdS sequences (Figure 2B) showed that P. benzenivorans DSM 8628T AcdS formed a unique cluster. BLASTp analysis revealed that the AcdS sequence from P. benzenivorans DSM 8628T was mostly similar (~85% identity) to the AcdS of Alphaproteobacteria, namely, Bosea, Methylobacterium, and Bradyrhizobium. These results suggest that P. benzenivorans DSM 8628T, possibly acquired an acdS gene from an Alphaproteobacteria donor via HGT.
The phylogram based on AcdS sequences (Figure 2B) also demonstrated that members of the P. oryzihabitans group present a different ACC deaminase compared to other Pseudomonas (~56% identity) (Figure 2B). In a previous report, Nascimento et al. [7] observed that members of the P. oryzihabitans group formed a unique AcdS cluster, distantly from the AcdS of other Proteobacteria. At this point it is difficult to ascertain the true evolutionary history of the P. oryzihabitans group AcdS. However, members of the P. oryzihabitans group possess high GC% genomes (~65%) compared to other Pseudomonas (58–61% GC content) (Table 1) and the acdS genes of these strains also present a high GC% content and are shorter (1014 bp) (Table 1). These data suggest that either (i) the adaptation to a high GC% genome impacted the P. oryzihabitans group ACC deaminase evolution; or (ii) the high GC% P. oryzihabitans group acquired a high GC% acdS gene from an unknown donor. New studies are necessary to understand the evolution of ACC deaminase in the P. oryzihabitans group.
Interestingly, Pseudomonas AcdS+ groups/clades are predominantly composed of plant-associated Pseudomonas (both PGPB and plant pathogens) (Table 1), which is consistent with previous studies reporting the increased prevalence of acdS genes in plant-associated bacteria [7,8]. The acquisition and/or maintenance of acdS genes seems to be favored in specific but not all plant-associated Pseudomonas. The factors regulating this selection remain to be determined.
Ultimately, due to its increased prevalence in both PGP and plant pathogenic Pseudomonas (e.g., P. syringae group), the mere presence of acdS genes cannot be used to predict beneficial interactions with a plant host.

6. Pseudomonas ACC Deaminase

The Pseudomonas ACC deaminase protein sequences present some variability, which is consistent with the different distribution patterns of acdS genes in the different Pseudomonas groups (Figure 2B). Alignments showed that Pseudomonas AcdS sequences are somewhat conserved, presenting 37.8% identical sites. These include the Lys51, Ser78, Tyr295, Glu296 and Leu322 residues that are necessary for ACC deaminase activity [70]. The Pseudomonas acdS genes present similar sizes (1014–1017 bp), and, consequently, generate similar proteins with a predicted subunit weight of ~36.6 KDa.
The ACC deaminase enzyme of Pseudomonas sp. GR12-2 [51] and Pseudomonas sp. UW4 have been characterized in some detail [65]. The enzyme of strain GR12-2 was found in the bacterial cytoplasm, presented a subunit molecular mass of 35 kDa and its activity was optimal at 30 °C and a pH optimum of 8.5 [51]. The Pseudomonas sp. UW4 ACC deaminase presented a molecular weight of ~41 kDa and showed a KM = 3.4 ± 0.2 mM and kcat = 146 ± 5 min−1 at pH 8.0 and 22 °C. The strain UW4 enzyme was thermodynamically stable presenting a melting temperature of 58 ± 1 °C. The Pseudomonas sp. UW4 ACC deaminase KM and kcat values are comparable to those of other ACC deaminase-producing bacteria (Table 2), including Methylobacterium strains [71] and Amycolatopsis methanolica 239 [72]. However, the enzyme of Pseudomonas sp. UW4 presented a higher KM (indicating less tight binding of the substrate ACC) and an increased kcat and presented a different temperature optimum (37 °C) when compared to the ACC deaminase from these other strains.
Several studies have suggested that the ACC deaminase from bacterial strains form homotetramers (Table 2). The modeling of different Pseudomonas AcdS (Figure 3), including those of P. benzenivorans DSM 8628T and P. oryzihabitans DSM 6835T, revealed that this conformation is favored. The obtained AcdS structural models presented increased values of overall quality (Figure 3), indicating structural conservation amongst Pseudomonas ACC deaminases.

7. The Role of ACC Deaminase in Beneficial Pseudomonas Plant Growth Promotion and Plant Protection Abilities

Several authors have obtained acdS mutants (including both loss and gain of function) of different beneficial Pseudomonas strains in an effort to understand the direct role of ACC deaminase in Pseudomonas plant growth promotion and plant protection abilities. These studies have revealed that the expression of ACC deaminase greatly impacts the performance of the different Pseudomonas strains, and clearly regulates their ability to modify several aspects of plant growth and development (Table 3).

7.1. Root Development Induced by Pseudomonas

The loss of the ability to promote plant root length development is one of the most described effects in Pseudomonas ACC deaminase minus mutants (loss of function) (Table 3). For instance, the acdS− mutants of Pseudomonas sp. GR12-2, Pseudomonas sp. UW4, P. brassicacearum YsS6 (formerly P. fluorescens) and P. migulae 8R6 all lost the ability to promote canola root elongation [17,35]. The acdS− mutant of P. ogarae F113 (formerly P. kilonensis) did not promote root length and root numbers in the maize cultivar EP1 [75]. On the other hand, P. protegens CHA0, expressing an exogenous ACC deaminase gene, gained the ability to promote canola root elongation [76], and, P. putida ATCC 17399 containing the broad-host-range plasmid pRKACC and expressing an exogenous ACC deaminase gene, gained the ability to promote root length development and adventitious root formation in tomato plants subjected to flooding [50].

7.2. Delay in Flower Senescence by Endophytic Pseudomonas

The inoculation of mini-carnation cut flowers with the ACC deaminase-producing endophytes, P. brassicacearum YsS6 and P. migulae 8R6, resulted in a delay in flower senescence of several days, and, consequently, an increased flower shelf-life [72]. These effects were not observed when the plants were inoculated with the respective Pseudomonas acdS− mutants of these strains [77]. Interestingly, the ACC deaminase-producing endophytes provided 2 additional days of shelf-life compared to the application of 1-aminoethoxyvinylglycine (AVG), a chemical compound known to limit the biosynthesis of ethylene. Moreover, the incubation of cut flowers with Pseudomonas sp. UW4, a rhizospheric strain (unable to colonize the plant interior) did not affect the senescence of cut flowers. This data clearly indicates that the use of Pseudomonas endophytes with ACC deaminase activity has the potential to replace the chemicals that are currently used by the cut flower industry to increase the life of cut flowers.

7.3. Plant Protection against Abiotic Stress

Pseudomonas acdS− mutant strains are greatly impaired in their ability to protect plants from abiotic stress (Table 3). For example, the Pseudomonas sp. UW4 acdS− mutant presented a decreased ability to protect canola from salt stress. Cheng and colleagues [61] observed that in the presence of 150 mmol/L salt, canola plants inoculated with wild-type Pseudomonas sp. UW4 presented similar biomass values compared to plants grown with no salt added. On the other hand, plants inoculated with the Pseudomonas sp. UW4 acdS− mutant only accumulated approximately 65% of the amount of biomass observed in the absence of salt [61]. Similarly, the Pseudomonas sp. UW4 acdS− mutant also presented a decreased ability to promote cucumber [79] and tomato [81] salt stress resistance compared to its wild-type counterpart. The endophytes, P. brassicacearum YsS6 and P. migulae 8R6, both presenting ACC deaminase activity, not only promoted tomato plant growth in the absence of stress conditions but also induced the accumulation of much higher fresh and dry biomass, higher chlorophyll contents, and a greater number of flowers and buds in tomato plants subjected to salt stress compared to non-inoculated plants or those inoculated with the respective Pseudomonas acdS− mutants [17]. Recently, Liu and colleagues [85] observed that the inoculation of tomato plants with the ACC deaminase-producing P. azotoformans CHB 1107 resulted in increasing plant shoot and root dry weights and a significant reduction in the plant ethylene emission in response to salt stress. These beneficial effects were lost when plants were inoculated with P. azotoformans CHB 1107 M (acdS− mutant). Moreover, P. azotoformans CHB 1107 significantly increased plant K, Ca, and Mn uptake compared with P. azotoformans CHB 1107 acdS− mutant [85].
Root inoculation of Rumex palustris and Arabidopsis thaliana plants with ACC deaminase-producing Pseudomonas sp. UW4 significantly decreased the shoot cadmium concentration and total content compared to the Pseudomonas sp. UW4 ACC deaminase-deficient mutant (acdS−) inoculation and the non-inoculated control [87]. The Pseudomonas sp. UW4 ability to decrease heavy metal accumulation in some plant tissues was correlated with its capacity to express ACC deaminase and decrease plant ethylene levels [87].
The expression of exogenous ACC deaminase genes in Pseudomonas also leads to their increased ability to protect plants from other abiotic stresses. Tomato plants inoculated with P. putida ATCC 17399 pRKACC, expressing ACC deaminase, had an increased ability to tolerate flooding stress [50]. Similarly, the inoculation of P. frederiksbergensis OS211-acdS (carrying the pRKACC plasmid and expressing ACC deaminase), resulted in a reduced ethylene emission, less ACC accumulation and lower ACC oxidase activity (52%, 75.9% and 23.2%, respectively) in tomato plants subjected to chilling stress (compared to non-inoculated plants) [86]. The transformed strain, P. frederiksbergensis OS211-acdS, showed a better plant growth promotion/protection performance when compared to the wild-type strain that lacked ACC deaminase [86], clearly demonstrating the beneficial effect of ACC deaminase expression.

7.4. Plant Protection against Biotic Stress

Several ACC deaminase-producing Pseudomonas strains, but not their acdS− mutants or wild-type counterparts that do not express acdS, demonstrated an increased capacity to protect plants from stress induced by pathogens (Table 3). The Pseudomonas sp. UW4 acdS− mutant showed a decreased ability to suppress tomato crown gall development induced by Agrobacterium, compared to the Pseudomonas sp. UW4 wild-type strain [63,88]. Moreover, the level of ethylene per mass of internodes carrying Agrobacterium-induced galls was significantly lower in plants pretreated with Pseudomonas sp. UW4, than in plants pretreated with the Pseudomonas sp. UW4 acdS− mutant [63].
The inoculation of pine seedlings with the ACC deaminase-producing Pseudomonas sp. UW4 led to a significant increase in the plant’s ability to resist the infection caused by the pinewood nematode, Bursaphelenchus xylophilus, and reduced the development of pine wilt disease symptoms [60]. This result was not observed when the pine seedlings were inoculated with the Pseudomonas sp. UW4 acdS− mutant [60].
The expression of ACC deaminase by the endophyte, P. migulae 8R6, played a key role this bacterium’s ability to improve the resistance of Catharantus roseus (Madagascar Periwinkle) to phytoplasma infection [62]. On the other hand, the P. migulae 8R6 acdS− mutant was not able to significantly reduce the disease symptoms [62].

7.5. Promotion of the Rhizobial Nodulation Process

The expression of ACC deaminase by P. brassicacearum YsS6 played a significant role in its ability to promote the nodulation process of both alpha (Rhizobium tropici CIAT 899) and beta-rhizobia (Cupriavidus taiwanensis STM 894), and, ultimately, leguminous plant growth [82]. The co-inoculation of rhizobial strains with the P. brassicacearum YsS6 acdS− mutant did not result in any increase in the rhizobial nodulation or growth of legume plants [82]. In addition, it was recently shown that Pseudomonas sp. Q1 (P. palleroniana), but not its acdS− mutant, promoted the symbiotic performance of R. leguminosarum bv. trifolii ATCC 14480T and Ensifer meliloti ATCC 9930T under both normal and excess Mn stress conditions [84].

8. ACC-Deaminase-Producing Pseudomonas and Their Potential Application in the Field

A formulation containing the ACC deaminase-producing P. fluorescens TDK1 was developed and applied in two consecutive field trials in saline soils, resulting in the increase of groundnut plant height, number of pods per plant, pod filling per cent and 100 seed weigh [89]. The P. fluorescens TDK1 strain greatly improved groundnut growth and saline stress resistance compared to the non-inoculated control and other formulations containing Pseudomonas that did not presented ACC deaminase activity [89].
The use of a bacterial consortia composed of ACC deaminase-producing P. palleroniana DPB13, P. palleroniana DPB16, Pseudomonas sp. DPB15 and Ochrobactrum anthropi DPC9 significantly increased several key parameters of rice and wheat growth and nutrient content [90]. For example, the inoculated rice and wheat plants significantly increased their nitrogen, phosphorus, potassium, calcium, and sodium contents. The treated plants also increased their 1000 grain weight (10.2%, 40.7%; rice and wheat, respectively), number of grains per panicle/spike (45.5%, 60.6%, rice and wheat respectively), and tillers (32.2%, 106.6%, rice and wheat respectively)[90].
The application of a bacterial inoculant based on four ACC deaminase-producing Pseudomonas strains improved sweet corn (Zea mays L. var. saccharata) productivity under the limited availability of irrigation water [91]. The study demonstrated that the combination of Pseudomonas sp. strains P1, P3, P8, and P14 significantly increased the ear and canned seed yield of sweet corn (44%, and 27%, respectively) compared to the non-inoculated control [91].

9. Conclusions and Future Perspectives

Beneficial plant-associated Pseudomonas containing ACC deaminase are of great interest for the study of plant-microbe interactions and for the development of novel inoculants for agricultural and biotechnological applications, especially those subjected to stress conditions. These unique strains have evolved in close association with plants worldwide and this has led to an important bacterial adaption to the soil/plant environment. The plant-associated lifestyle may be vital for the increased success of these strains as commercial bacterial inoculants, and ultimately, the most relevant factor for differentiating ACC deaminase-producing Pseudomonas groups from other pseudomonads.
Numerous other Pseudomonas species that are commonly found in the rhizosphere and associated with plants do not possess acdS genes (only 39 strains from hundreds of type strains possess acdS genes). This raises some questions:
  • What are the factors regulating the selection of ACC deaminase genes in specific Pseudomonas groups (including many Pseudomonas plant pathogens)?
  • Is the presence of ACC deaminase linked to a specific Pseudomonas lifestyle/mode of action (e.g., strong plant colonization and activation of plant defense responses)?
  • Which genes were co-selected and co-evolved with ACC deaminase genes in the genomes of beneficial and pathogenic plant-associated Pseudomonas?
  • If ACC deaminase-producing Pseudomonas strains are key players in promoting plant growth and stress resistance, what is their impact in the overall plant microbiome assembly?
  • Which beneficial ACC deaminase-producing Pseudomonas groups could be selected for future field applications worldwide?
Future studies will be necessary to address these questions and gain additional insight into the genomics and physiology of ACC deaminase-producing Pseudomonas.

Author Contributions

Conceptualization, B.R.G. and F.X.N.; methodology, F.X.N.; formal analysis, F.X.N.; data curation, F.X.N.; writing—original draft preparation, B.R.G. and F.X.N.; writing—review and editing, B.R.G. and F.X.N. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

Francisco X. Nascimento gratefully acknowledges funding from INTERFACE Programme, through the Innovation, Technology and Circular Economy Fund (FITEC).

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Schematic representation of (A) bacterial 1-aminocylopropane-1-carboxylate (ACC) deaminase activity and (B) the modulation of plant ACC and ethylene concentrations. ACC-1-aminocyclopropane-1-carboxylate; ET-ethylene; ACCD-ACC deaminase.
Figure 1. Schematic representation of (A) bacterial 1-aminocylopropane-1-carboxylate (ACC) deaminase activity and (B) the modulation of plant ACC and ethylene concentrations. ACC-1-aminocyclopropane-1-carboxylate; ET-ethylene; ACCD-ACC deaminase.
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Figure 2. (A) Phylogram based on 576 core genes protein sequences from Pseudomonas type strains that possess acdS genes. The core genes (single copy genes found in all tested strains) were selected based on GHOSTKOALA functional annotation [66] and a python script built in house. The core genes were individually aligned using MAFFT [67] and concatenated using a python script built in house. The phylogenetic analysis was conducted in GalaxyPasteur server [68] using FastTree v2.1.10 [69], the LG model and a bootstrap of 100 replications. (B) Phylogram based on the AcdS sequences of Pseudomonas type strains. The sequences were obtained from the NCBI database and aligned using MAFFT [67]. The phylogenetic analysis was conducted in GalaxyPasteur server [68] using FastTree v2.1.10 [69], the LG model and a bootstrap of 1000 replications.
Figure 2. (A) Phylogram based on 576 core genes protein sequences from Pseudomonas type strains that possess acdS genes. The core genes (single copy genes found in all tested strains) were selected based on GHOSTKOALA functional annotation [66] and a python script built in house. The core genes were individually aligned using MAFFT [67] and concatenated using a python script built in house. The phylogenetic analysis was conducted in GalaxyPasteur server [68] using FastTree v2.1.10 [69], the LG model and a bootstrap of 100 replications. (B) Phylogram based on the AcdS sequences of Pseudomonas type strains. The sequences were obtained from the NCBI database and aligned using MAFFT [67]. The phylogenetic analysis was conducted in GalaxyPasteur server [68] using FastTree v2.1.10 [69], the LG model and a bootstrap of 1000 replications.
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Figure 3. Models of the different ACC deaminase enzymes from selected Pseudomonas. The models were created in Swiss-Model [73] using the crystal structure of ACC deaminase from Burkholderia (formerly Pseudomonas) sp. ACP as template (SMTL ID: 1tzm.1) [74]. GMQE—Global Model Quality Estimate; QMEANDisCo is a composite score for single model quality estimation.
Figure 3. Models of the different ACC deaminase enzymes from selected Pseudomonas. The models were created in Swiss-Model [73] using the crystal structure of ACC deaminase from Burkholderia (formerly Pseudomonas) sp. ACP as template (SMTL ID: 1tzm.1) [74]. GMQE—Global Model Quality Estimate; QMEANDisCo is a composite score for single model quality estimation.
Microorganisms 09 02467 g003
Table
Table 1. Properties of ACC deaminase-containing Pseudomonas type strains.
Table 1. Properties of ACC deaminase-containing Pseudomonas type strains.
Pseudomonas GroupsType StrainIsolation SourceIsolation
Country		Genome GC%acdS GC%acdS length (bp)
P. syringae groupP. syringae KCTC 12500Syringa vulgarisGreat Britain58.961.31017
P. amygdali ICMP 3918Prunus amygdalusGreece58.259.71017
P. avellanae JCM 11937Corylus avellataGreece58.561.41017
P. asturiensis DSM 100247Glycine maxSpain59.161.81017
P. cannabina DSM 16822Cannabis sativaHungary58.560.81017
P. capsici Pc19-1Capsicum annuumUSA58.460.41017
P. caricapapayae CCUG 32775Carica papayaBrazil58.359.81017
P. caspiana FBF102CitrusIran57.057.61017
P. cichorii DSM 50259Cichorium endiviaGermany58.159.81017
P. congelans DSM 14939Phyllosphere of grassesGermany59.361.71017
P. ficuserectae ICMP 7848Ficus erectaJapan57.9601017
P. floridensis GEV388TomatoUSA59.260.11017
P. foliumensis DOAB 1069Wheat phyllosphereCanada57.257.91017
P. meliae CFBP 3225Melia azedarachJapan58.459.41017
P. savastanoi ICMP4352Olea europaeaYugoslavia58.059.71017
P. viridiflava DSM 6694Dwarf or runner beanSwitzerland59.462.01017
P. tremae DSM 16744Trema orientalisJapan57.859.31017
P. triticumensis DOAB 1067Wheat phyllosphereCanada59.361.21017
P. corrugata subgroupP. brassicacearum CCUG 51508Rhizoplane of Brassica napusFrance60.857.31017
P. bijieensis L22-9Cornfield soilChina60.9601017
P. kilonensis DSM 13647Agricultural soilGermany60.958.31017
P. thivervalensis DSM 13194Rhizoplane of Brassica napusFrance61.258.41017
P. viciae 11K1Rhizosphere broad beanChina60.359.81017
P. tehranensis SWRI196Rhizosphere of wheatIran60.561.41017
P. straminea groupP. flavescens LMG 18387Walnut tree, canker tissueUSA63.560.11017
P. asplenii subgroupP. fuscovaginae ICMP 5940Oryza sativaJapan61.456.61017
P. gessardii subgroupP. gessardii DSM 17152Mineral waterFrance60.459.91017
P. mandelii subgroupP. farris SWRI79Rhizosphere of wheatIran58.759.91017
P. migulae NBRC 103157Mineral waterFrance59.159.71017
P. fluorescens subgroupP. grimontii DSM 17515Mineral waterFrance60.159.41017
P. marginalis ICMP 3553 Cichorium intybus leafUSA60.458.11017
P. palleroniana CCUG 51524Oryza sativaCameroon60.558.01017
P. panacis DSM 18529Ginseng root lesionsSouth Korea61.159.41017
P. massiliensis groupP. typographi CA3AEuropean Bark Beetle (Ips typographus)Czech Republic62.161.71017
P. anguilliseptica group
(High GC%)		P. benzenivorans DSM 8628SoilUSA65.255.41014
P. oryzihabitans group
(High GC%)		P. oryzihabitans DSM 6835Rice paddyJapan66.267.01014
P. psychrotolerans DSM 15758WaterAustria65.366.21014
P. rhizoryzae RY24Rice seedsChina64.865.11014
The study of the prevalence of AcdS in Pseudomonas type strains was conducted by BLASTp (standard parameters) in the NCBI database, using the Pseudomonas sp. UW4 functional AcdS protein sequence (WP_015096487.1) as query [65]. Positive hits were considered for values of identity > 50%.
Table
Table 2. Properties of the Pseudomonas sp. UW4 and other studied bacterial ACC deaminase enzymes.
Table 2. Properties of the Pseudomonas sp. UW4 and other studied bacterial ACC deaminase enzymes.
StrainKM (mM)kcat (min−1)pH OptimumTemperature Optimum (°C)Structure and Molecular Mass (KDa)Reference
Pseudomonas sp. UW43.4 ± 0.2146 ± 58.037Homotetramer
168 kDa		[65]
Methylobacterium nodulans ORS20600.8 ± 0.04111.8 ± 0.28.050Homotetramer
144 kDa		[71]
Methylobacterium radiotolerans JCM28311.8 ± 0.365.8 ± 2.88.045Homotetramer
144 kDa		[71]
Amycolatopsis methanolica 2391.7 ± 0.25.1 ± 0.28.560Homotetramer
144 kDa		[72]
Table
Table 3. Studies on the role of ACC deaminase (acdS gene expression) in different Pseudomonas strains.
Table 3. Studies on the role of ACC deaminase (acdS gene expression) in different Pseudomonas strains.
Pseudomonas StrainEffects of acdS DeletionReference
Pseudomonas sp. GR12-2
▪
Unable to promote canola root elongation
[35]
Pseudomonas sp. UW4
▪
Unable to promote canola root elongation
▪
Decreased ability to protect canola, cucumber, and tomato from salt stress
▪
Decreased ability to reduce cadmium accumulation in several plants
▪
Unable to promote the colonization process of mycorrhiza
▪
Decreased ability to protect tomato from Agrobacterium infection
▪
Decreased ability to promote pine growth and protect it from nematode infection
[60,61,63,78,79,80,81]
P. brassicacearum Yss6
▪
Lost the ability to decrease flower senescence
▪
Decreased ability to promote tomato growth and protect it from salt stress
▪
Lost the ability to promote the nodulation process of alpha and beta-rhizobia
[17,77,82]
P. migulae 8R6
▪
Lost the ability to decrease flower senescence
▪
Decreased ability to promote tomato growth and protect it from salt stress
▪
Decreased ability to protect periwinkle from phytoplasma infection
[17,62]
P. ogarae F113
▪
Lost the ability to promote maize root growth and seed germination
[75,83]
P. palleroniana Q1
▪
Decreased ability to promote the nodulation process of rhizobia
[84]
P. azotoformans CHB 1107
▪
Decreased ability to promote tomato plant growth and resistance to salt stress
[85]
Effects of Exogenous acdS Expression
P protegens CHA0
▪
Gained the ability to promote canola root elongation
▪
Improved its ability to protect cucumber against Pythium damping-off, and potato tubers against Erwinia soft rot
[76]
P. putida ATCC 17399
▪
Increased plant growth promotion activities (shoot, root)
▪
Increased ability to protect tomato plants from flooding stress
[50]
P. frederiksbergensis OS211
▪
Increased plant growth promotion activities
▪
Increased ability to protect tomato plants from chilling stress
[86]
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Glick, B.R.; Nascimento, F.X. Pseudomonas 1-Aminocyclopropane-1-carboxylate (ACC) Deaminase and Its Role in Beneficial Plant-Microbe Interactions. Microorganisms 2021, 9, 2467. https://doi.org/10.3390/microorganisms9122467

AMA Style

Glick BR, Nascimento FX. Pseudomonas 1-Aminocyclopropane-1-carboxylate (ACC) Deaminase and Its Role in Beneficial Plant-Microbe Interactions. Microorganisms. 2021; 9(12):2467. https://doi.org/10.3390/microorganisms9122467

Chicago/Turabian Style

Glick, Bernard R., and Francisco X. Nascimento. 2021. "Pseudomonas 1-Aminocyclopropane-1-carboxylate (ACC) Deaminase and Its Role in Beneficial Plant-Microbe Interactions" Microorganisms 9, no. 12: 2467. https://doi.org/10.3390/microorganisms9122467

APA Style

Glick, B. R., & Nascimento, F. X. (2021). Pseudomonas 1-Aminocyclopropane-1-carboxylate (ACC) Deaminase and Its Role in Beneficial Plant-Microbe Interactions. Microorganisms, 9(12), 2467. https://doi.org/10.3390/microorganisms9122467

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