Abstract
Plants are immobile and are exposed to various biotic and abiotic stresses, including heat, cold, drought, flooding, nutrient deficiency, heavy metal exposure, phytopathogens, and pest attacks. The stressors significantly affect agricultural productivity when exceed a certain threshold. It has been reported that most of the stressed plants are reported to have increased ethylene synthesis from its precursor 1-aminocyclopropane-1-carboxylic acid (ACC). Ethylene is a plant hormone that plays a vital role in the regulation of various physiological processes, such as respiration, nitrogen fixation, and photosynthesis. The increment in the plant hormone ethylene would reduce plant growth and development, and if the ethylene level increased beyond the limit, it could also result in plant death. Therefore, plant growth–promoting bacteria (PGPB) possessing ACC deaminase activity play an essential role in the management of biotic and abiotic stresses by hydrolysing 1-aminocyclopropane-1-carboxylic acid using ACC deaminase. In this review, the importance of ACC deaminase–producing bacteria in promoting plant growth under various abiotic stressors is discussed.
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Introduction
The plant growth rate and agricultural productivity are significantly affected by physiological and environmental factors. These factors include plant genotype, unfavorable growth conditions, physical and chemical parameters of the soil, and nutrient deficiency. In addition to these parameters, biotic (pathogen attack) and abiotic factors (salinity, drought, waterlogging, heavy metals, temperature, and pH) are also responsible for deleterious effect on plants, crop yield, and production (Gamalero and Glick 2012; Fahad et al. 2021a). More than 50% of crop productivity is affected by abiotic stress (Boyer 1982; Bray 2000). Because of global climate change, abiotic stresses may exaggerate the future. Under all environmental stresses, ethylene is produced in large amounts in plants, which is detrimental to sustainable agricultural production (Sapre et al. 2019). If the ethylene level exceeds its threshold level, it becomes a stress hormone that may hinder plant growth and development. In regular and stressful ecosystems, ethylene affects function and efficiency by sharing information with other signaling pathways (Fahad et al. 2021c). Similarly, Khan et al. (2008) reported that when ethephon, an ethylene-releasing compound was applied at lower concentration, it enhanced ethylene evolution and increased the leaf area of mustard. However, at higher concentrations, it inhibited the growth, photosynthesis, and nitrogen accumulation of the mustard plants. Pierik et al. (2006) also stated that depending on the concentration of ethylene, it promotes, inhibits or induces senescence, and governs the development of leaves, fruits, and flowers. Plants employ several strategies to enhance their growth and productivity in stressful environments (Fahad et al. 2015a, b) including the use of ACC deaminase–producing bacteria. Nonetheless, ethylene hormone stress can be reduced by inoculating plants with PGPB, providing ACC deaminase activity by producing 1-aminocyclopropane-1-carboxylic acid deaminase (ACCD) (Glick et al. 2007a, b). ACCD enzyme helps in the breakdown of a compound ACC, “an immediate precursor of ethylene” into α- ketobutyrate and ammonia. This reduces the level of the plant hormone ethylene and promotes plant growth and development (Honma and Shimomura 1978; Glick 2014). This ACCD activity and some additional mechanisms of PGPB help the host plant to become tolerant to environmental stresses known as systemic-induced tolerance (Yang et al. 2009) (Fig. 1). Therefore, to increase crop yields, management of ethylene generation is becoming an attractive strategy for abiotic stress management and sustainable agricultural production. In this regard, ACC deaminase producing PGPB called as “stress modulator” which modulates plant growth under extreme environmental conditions by lowering ethylene concentration in plants.
Numerous literature reviews have addressed the beneficial traits of PGPR and their applications as plant growth promoters, biocontrol agents, nitrogen fixers, and phosphate solubilizers to alleviate drought, salinity, temperature, and heavy metal stress by focusing on a particular trait of bacteria to alleviate a particular type of abiotic stress. This may be due to the lack of understanding the mechanisms of PGPR and plant interactions. Chandran et al. (2021) reported the use of salt-tolerant PGPR to alleviate salinity stress and to improve global food production. Glick (2012) reported that siderophores produced by Pseudomonas, Enterobacter, Bacillus, Azotobacter, Rhizobium, and Serratia alleviate heavy metal stress in the host plant. Likewise, some studies have illustrated the role of ACC deaminase–producing bacteria in plant growth promotion as well as in abiotic stress tolerance through symbiotic associations between plants in the native rhizosphere and PGPR (Murali et al. 2021). The present review sheds light on the use of ACC deaminase–producing bacteria to combat various types of abiotic stresses, such as drought, salinity, flooding, heavy metals, heat, and cold, by understanding the potential roles, advantages, and mechanisms involved in overcoming tolerance to various abiotic stresses. This review also discusses the prospects of ACC deaminase–producing bacterial exploitation for better crop productivity under adverse environmental conditions for sustainable agriculture. The specific goals of this review were to (i) explore the underlying mechanisms of beneficial ACC deaminase producers in mitigating abiotic stresses, (ii) accelerate the multivariate features of ACC deaminase–producing bacteria to mitigate climate change–related stress conditions, and (iii) introduce an eco-friendly approach to feed the global population and for sustainable agriculture. Therefore, the present review focuses on the role of ACC deaminase–producing bacteria in ameliorating environmental stresses and studies the importance of ethylene hormones in plant growth and development under various abiotic stresses.
Mechanism of ACC deaminase in plant growth and development
ACC deaminase is comprised of multiple polypeptide chains with monomers of approximately 35–42 kDa molecular mass. ACCD was first found in microorganisms in the soil, where it converts ACC into α-ketobutyrate and ammonia (deamination) which is further metabolized by a group of microorganisms (Honma and Shimomura 1978). This enzyme uses pyridoxal-5-phosphate as the cofactor. ACCD is tightly bound to the pyridoxal phosphate cofactor at one molecule per subunit. Among the D-amino acids, D-cysteine and D-serine are considered substrates of ACCD, whereas L-serine and L-alanine were competitive inhibitors of ACCD. The purification of ACCD has been reported in P. putida and P. chloroaphis (Klee et al. 1991) (Fig. 2).
The X-ray crystallographic study indicated that the β-subunit of the tryptophan synthase enzyme, ACCD also consists of two domains: an open twisted α/β structure (Yao et al. 2000). The ACCD cofactor pyridoxal phosphate is secreted within the protein molecule, similar to other members of the β family of pyridoxal phosphate-dependent enzymes. The enzyme ACCD comprises two essential amino acid residues at cysteine 162, a reactive thiol group situated in the internal gap between two protein molecule domains and at lysine 51 at the pyridoxal phosphate binding site.
For the breakdown of ACC, generally, two types of reactions take place with the help of ACCD enzyme: First, hydrogen atoms are separated using a series of hydrolytic reactions by Lys51, and the cyclopropane ring is opened. Second, ACC contains a β-carbon atom. When a nucleophilic attack occurs on this β-carbon atom, the cyclopropane ring opens and then, with the help of a basic residue, the Lys51 β-proton is separated at the pro-R carbon (Zhao et al. 2003). During the reaction of PLP with the ACCD enzyme residue Lys as a cofactor, the substrate ACC reacts with internal aldimine and converts it into an external aldimine with an intermediate aminyl called an intermediate aminyl as the trans-aldimination process. During this process, two routes are generally proposed: (i) direct extraction or separation of β-hydrogen and (ii) nucleophilic addition followed by β-hydrogen extraction.
ACC: a menace for various threats
Role of ACC deaminase in drought tolerance
In the twenty-first century, climate change has become a significant threat to agricultural productivity. According to the literature review, plant growth and development are mainly affected by the adverse effects of environmental stresses and global warming. Drought stress is a significant factor that can severely influence agricultural productivity in terms of crop quality and quantity (Morison et al. 2007; Blum 2011). Several plants under drought stress close their stomata and limit gas exchange, resulting in a decreased photosynthetic activity (Fahad et al. 2021b). Globally, approximately 70% of crops are damaged by abiotic stresses, and more yield is lost owing to drought stress (Bray 2000). The development of osmotic pressure in plants owing to drought stress may lead to stomatal closure, loss of turgor, protein structure disturbance, photorespiration stimulation, reduction of CO2 fixation, and reactive oxygen species (ROS). All these conditions may damage the cell membrane, thereby affecting plant growth (Hossain and Dietz 2016). Plants produce several physiological, biochemical, morphological, and molecular responses to protect themselves from various stressors. However, analysis of these parameters is complicated (Conesa et al. 2016; Chandra et al. 2019). Plants produce different enzymatic responses such as CAT, GR, APX, and SOD, and non-enzymatic responses such as proline, cysteine, and ascorbic acid, during drought stress, which helps the plants to trigger oxidative damage (Mittler 2002; Chandra et al. 2018).
It has been found that in plant roots, ACC—ethylene precursor gets accumulated and then transported to aerial part of the plant which gets converted to ethylene due to the presence of oxygen which may trigger petiole epinasty (Vidoz et al. 2010). The intermediates S-adenosyl methionine (SAM) and 1-aminocyclopropane-1-carboxylic acid (ACC) stimulate methionine under drought stress. SAM synthetase converts methionine to SAM, and ACC synthase converts SAM to ACC which is then oxidized to ethylene by ACC oxidase. Therefore, ethylene levels increase, and affect plant growth, development, and productivity. Therefore, to enhance crop productivity, it is necessary to reduce ethylene stress (Muller et al. 2003).
To date, various methods have been developed to make plant resistant to drought stress. Different genomic approaches (comparative, functional, and structural studies) have recently been attempted to make plants resistant to drought stress. These molecular approaches in modern times help in the identification of metabolic processes and the genes responsible for making plants tolerant to drought stress. However, the major drawback associated with the use of this approach is the lack of knowledge in implementing such methods (Ishitani et al. 2004; Mir et al. 2012). Therefore, using a biological agent such as PGPB possessing ACC deaminase activity is the best way to overcome the stress generated in plants during drought conditions (Glick et al. 2007a, b; Tiwari et al. 2018; Singh et al. 2019).
Under drought conditions, the hormone ethylene was overexpressed in response to oxidative stress (Arshad et al. 2007; Glick 2014), which affects the agricultural productivity of crop plants, particularly tomatoes (Gerszberg and Hnatuszko-Konka 2017; Dubois et al. 2018). Thus, a possible solution to reduce the stress is to inoculate the plants with PGPB-producing ACC deaminase activity, which degrades the ACC compound into α-ketobutyrate and ammonia. This leads to a decrease in ethylene stress and increases enzymatic and non-promoting plant growth and development (Glick 2014). ACC deaminase–producing rhizobacteria have been reported to belong to the genera Burkholderia, Methylobacterium, Rhizobium, Enterobacter, Bacillus, and Pseudomonas, which promote plant growth and development under drought stress (Penrose et al. 2001; Glick et al. 2007a, b; Chandra et al. 2019; Singh et al. 2019) (Table 1, Fig. 3).
Saikia et al. (2018) reported the combined action of ACC deaminase–producing bacteria such as Ochrobactrum pseudogrignonense RJ 12, Pseudomonas sp RJ 15, and Bacillus subtilis. Their research showed that inoculation with ACC deaminase–producing bacteria enhanced root length, seed germination rate, chlorophyll content, and production of antioxidant enzymes and cellular osmolytes in black gram and garden pea plants during drought stress. In addition to consortia, individual ACC deaminase–producing bacteria also alleviated water stress in the tested plants by solubilizing phosphate, providing iron, nitrogen, and inhibiting pathogens (Saikia et al. 2018). Similarly, Zafar-ul-Hye et al. (2019) reported that drought stress affects vegetative growth and physiological processes of plants, resulting in low productivity due to ethylene synthesis, thereby inhibiting root elongation. Therefore, ACC deaminase–producing B. amyloliquefaciens combined with 30 mg ha−1 biocharcoal produced ACCD, which catabolized ethylene under water stress and enhanced growth and crop productivity. It was observed that enhancement varied for each crop; straw yield (50%), grain yield (36%), and biological yield (40%) under three irrigations and straw yield (75%), grain yield (77%), and below-ground biomass (77%) under two irrigations in the wheat plant during drought stress. The authors concluded that instead of the individual application of B. amyloliquefaciens and biocharcoal, the combined application of both mitigates drought stress and enhances crop productivity (Zafar-ul-Hye et al. 2019). In a recent study, Gowtham et al. (2020) reported that ACC deaminase–producing B. subtilis SF 48 enhanced plant growth parameters and relative water content (RWC) compared with untreated plants during drought stress in maize (Zea mays) by reducing oxidative damage caused by drought stress. Enzymatic (SOD and APX), non-enzymatic (proline, MDA, and H2O2), biochemical, and histochemical studies (H2O2 and superoxide anion) also revealed that ACC deaminase–producing bacteria play a role in mitigating drought stress in maize plants (Gowtham et al. 2020).
Role of ACC deaminase in salt tolerance
Soil salinity is one of the major abiotic stressors responsible for reducing agricultural productivity (Santoyo et al. 2017). Primary and secondary salinization are the two main types of salinity. Primary salinization is a natural phenomenon where, due to the presence of high salt content in groundwater, soluble salts accumulate through natural processes, whereas secondary salinization is the result of improper management of irrigation facilities, unstable quality of irrigation water, and poor soil drainage conditions (Fahad et al. 2015a, b). According to the US Department of Agriculture, salinity laboratory standard, a soil is saline when the electrical conductivity (EC) of a saturated paste extract is equal to or greater than 4 dS/m. Approximately 800 and 1000 million hectares of soil worldwide are significantly affected by salt concentration, which may include saline, alkaline-saline, and acid-saline soils (Rengasamy 2010). If the concentration of soluble salts such as CaCl2, MgCl2, and NaCl2 increases, the EC of saline soils also increases (Sairam et al. 2016).
Apart from saline water, anthropogenic activities and crop irrigation facilities are also responsible for increasing salt concentrations in the soil. Horie et al. (2012) and Bharti and Barnawal (2019) reported that approximately 20% of the cultivated areas face the problem of hypersalinity, as the salt penetrates inside plant cells and outside the roots, resulting in osmotic stress and ionic stress generated inside the plants. As a consequence of ionic stress, an influx of excess sodium ions and an overall efflux of potassium ions occur accelerats the senescence of mature leaves in plants. Under osmotic pressure, salts accumulate in the soil near plant roots and dehydration occurs in plant cells, affecting cell elongation and lateral bud development, as well as inhibiting the growth of young leaves (Fahad et al. 2021b). Toxic ions such as sodium accumulate in leaves due to salt stress. If this amount exceeds the threshold limit, it may hinder various physiological processes such as photosynthesis and ROS generation (Horie et al. 2012; Bharti and Barnawal 2019). ROS are generated by saline stress, but various other stresses, such as drought, heavy metal contamination, and flooding, are also responsible for toxicity (Covarrubias and Cabriales 2017; Forni et al. 2017). Furthermore, ROS is responsible for damaging secondary DNA, breaking double-stranded DNA, loss of bases, and DNA–protein crosslinks (Santoyo et al. 2008). Heydarian et al. (2018) concluded through his research study that ACC deaminase–producing PGPB can tolerate high salinity stress and prevent cell damage through the modulation of genes involved in ROS, ethylene, and abscisic acid–dependent signaling. It has been observed that the transgenic line Camelina sativa can tolerate increased salinity stress by modulating the expression of genes involved in ROS production.
Kang et al. (2019) reported that IAA and ACC deaminase–producing strains of Leclercia adecarboxylata (MO1) promoted the growth of tomato plants and improved their salinity stress tolerance levels. This may be due to activation of ACC synthase transcription and promote plant growth through IAA production. As a result, the amount of ethylene synthesized increased, which inhibited IAA signal transduction, thereby limiting plant growth. However, due to the presence of ACC deaminase, the ethylene level was lowered, thereby decreasing the feedback inhibition. The researchers concluded that IAA promoted plant growth. Simultaneously, ACC deaminase from PGPB lowers the ethylene levels, improving the plant’s ability to tolerate salinity stress (Kang et al. 2019).
Salinity stress also modifies the soil microbial community, which may lead to changes in plant-crop interactions, protection against plant pathogens, biogeochemical cycles, plant growth, development and production, and soil fertility. Many studies have shown that salinity stress prevents the survival of halo-susceptible microbes, including bacteria, fungi, and mycorrhizal fungi (Yaish et al. 2016). A plant response to any stress is initiated by increased ethylene production (Glick 2014). The increased amount of ethylene may result in yellowing of leaves, abscission of leaves, petals, and flowers, senescence of plant organs, premature death, inhibition of nodule formation in leguminous plant roots, and reduction in nitrogen-fixing ability (Zahir et al. 2009; Kong et al. 2015; Nascimento et al. 2016). Therefore, to counteract the biosynthesis of ethylene and mitigate ROS-induced damage to the plant, PGPB possessing ACC deaminase activity is a positive aspect for managing salinity stress by regulating the expression of genes involved in ROS, thereby preventing damage to plant cells. Several ACC deaminase–producing bacterial isolates reported to promote plant growth and development under salinity stress belong to the genera Pseudomonas, Bacillus, Achromobacter, Halobacillus, Mesorhizobium, Arthrobacter, Bulkhorderia, Serratia, Lysinibacillus, Streptomyces, Klebsiella, Aneurinibacillus, Paenibacillus, Micrococcus, Brevibacterium, and Enterobacter (Saravanakumar and Samiyappan 2007; Yildrim et al. 2008; Grover et al. 2011; Chookietwattana and Maneewan 2012; Brigido et al. 2013; Barnawal et al. 2014; Maxton et al. 2018; Mahmood et al. 2019; Acuna et al. 2019; Gupta and Pandey 2019; Del Carmen Orozco-Mosqueda et al. 2020) (Table 2).
Del Carmen Orozco-Mosqueda et al. (2020) reported that ACC deaminase–producing bacteria belonging to the genus Bacillus promoted plant growth because of their ability to sporulate and combat various environmental stressors such as salt stress. It has also been reported that the ACC deaminase–containing bacterium Arthrobacter protophormiae enhances rhizobial nodulation and mycorrhizal colonization, making the Pisum sativum plant tolerant to salt stress by interacting with other beneficial microorganisms (Barnawal et al. 2014).
Role of ACC deaminase in heavy metal stress tolerance
Various anthropogenic activities, such as increased industrialization, intensive agricultural practices, extensive mining activities, rapidly growing urbanization, and an increasing population, have disturbed our ecosystem. These developments affected the availability of natural resources, disturbed the essential components of life on Earth, and natural biogeochemical cycles. Furthermore, the anthropogenic activities have led to the accumulation of heavy metals in the biosphere, posing a threat to human and environmental health (Emamverdian et al. 2015).
Heavy metals are non-biodegradable inorganic chemical constituents, with an atomic mass over 20 and higher than 5 gcm−3. Heavy metals are responsible for mutagenic, cytotoxic, and genotoxic effects on humans, animals, and plants, thereby disturbing the food chain, soil composition, irrigation facilities, aquatic life, and atmosphere (Wuana and Okieimen 2011). Soil is comprised of two types of metals: essential and non-essential micronutrients. Essential micronutrients, such as Fe, Zn, Cu, Mg, Mo, and Ni, are required for normal plant growth. At the same time, non-essential micronutrients such as Cd, Cr, Pb, Co, Ag, and As have unknown biological and physiological functions (Zhou et al. 2014). Heavy metals occupy both the underground and aboveground plant surfaces. Essential elements play a crucial role in enzyme structure and proteins and required in small amounts for plant growth, metabolism, and development.
The presence of both essential and non-essential elements in excess amounts inhibit plant growth and results in retarded plant growth. Increased amounts of heavy metals are toxic to plants and hinder various metabolic processes and plant cell functioning. This includes (1) disturbance in building blocks of protein structure due to bond formation between heavy metals and sulfhydryl groups; (2) reduction of the essential metal functionality in biomolecules such as enzymes or pigments; (3) affecting the crucial activities of plants such as respiration, photosynthesis, enzymatic activities; and (4) repression of the integrity of the cytoplasmic membrane (Hall 2002; Hossain et al. 2012).
Sources of heavy metals and metalloids include agrochemicals, metal industries, and sewage sludge. Once heavy metals accumulate in the soil, they penetrate the ground and exert toxicity. The toxicity of heavy metals may affect the composition of microbes, including PGPR and their metabolic activity. Plant roots absorb heavy metals and transport them to other parts of the plant, affecting plant growth and crop productivity and leading to impaired metabolism (John et al. 2009). Once plants are exposed to metal toxicity, they generate ROS such as superoxide free radicals (O2−) and non-free radical species such as singlet oxygen (O2*), hydrogen peroxide (H2O2), and hydroxyl free radicals (OH−). Furthermore, cytotoxic compounds such as methylglyoxal (MG) under heavy metal stress conditions lead to oxidative stress, thereby increasing SOD and lipoxygenase activity (Baisak et al. 1994). Such stress conditions may lead to several deteriorative disorders such as ion leakage, oxidation of proteins and lipids, redox imbalance, oxidative DNA attack, denaturation of the cell membrane, and cell structure, leading to activation of programmed cell death (Rellan et al. 2006; Sharma et al. 2012; Tuma 2016).
The synthesis of higher amounts of ethylene leads to a reduction in plant growth and viability due to ethylene stress. Under such conditions, PGPR possessing ACC deaminase activity helps to remove some of the metal toxicity. They also promote plant growth and nutrient supply. In addition to mitigating metal toxicity, ACC deaminase also helps plants develop longer roots during the early stages of growth (Burd et al. 1998; Glick et al. 1998) increases the germination rate of seeds and biomass production (Glick 2003). It has been reported that a combination of Pseudomonas sp., Bacillus sp., and B. cereus mitigates metal toxicity (Grobelak et al. 2018) (Table 3).
Zafar-ul-hye et al. (2018) reported that the ACC deaminase–producing Agrobacterium fabrum CdtS5 and Stenotrophomonas maltophilia CdtS7 could tolerate Cd up to 2.5 and 5 mg/L respectively, and reduced Cd uptake by wheat plants when used as inocula. These ACC deaminase producers enhance the wheat plant growth and photosynthetic pigments in wheat seedlings under Cd toxicity (Zafar-ul-hye et al. 2018). Danish et al. (2019) reported that the ACC deaminase producers Agrobacterium fabrum and Leclercia adecarboxylata were found to tolerate Cr stress and improved the dry weight of the root, shoot, length of roots and shoots, leaves, and height of maize (Zea mays) plants when inoculated with 500 μM Fe. The researchers also reported that the uptake of NPK in leaves (N, 64.7%; P, 70% and 183.3%; K, 53.8% with a 3.40-fold increase) and roots (N, 25.6% and 122.2%; P, 25.6% and 122.2%; K, 33.3%) was improved at 50 and 100 mg kg−1 of Cr toxicity when ACC deaminase–producing A. fabrum treated with 500 μM Fe (Danish et al. 2019). ACC deaminase production by B. gibsonii PM11 and B. xiamenensis PM 14 found to tolerate metal stress (Cr, Ni, Cd, and Cu) from 50 to 1000 mg/L (Zaineb et al. 2020). These bacteria increased the root and shoot length, fresh, and dry weight, chlorophyll content, proline content, and antioxidant enzymatic activity of flax plants (Linum usitatissimum) by reducing metal-induced stress conditions (Zaineb et al. 2020).
Bacteria isolated from metal-polluted soils have been reported to facilitate the mobilization and immobilization of metals in plants. However, little information is available on the deterioration caused by the toxic effects of heavy metals on plants. Another viable option to mitigate metal toxicity is by phytoremediation methods. Bioremediation practices that use plants alone have certain limitations. If metal-resistant plants form an association with metal-resistant PGP bacteria, this approach efficiency increases several-fold.
Role of ACC deaminase in temperature stress tolerance
Global warming is one of the most critical issues affecting all living organisms worldwide. Natural disasters, such as drought, elevated carbon dioxide, floods, high temperatures, cold waves, and cyclones, are some of the abiotic stresses that cause economic losses and global warming (Zhang et al. 2019). Chimner et al. (2017) evaluated the impacts of warming and reported that the primary reason for the increase in average ambient temperature is the release of greenhouse gases. If this situation persists, then the mean temperature per decade will rise by 0.3 °C and result in a temperature increase of approximately 1 and 3 °C by 2025 and 2100, respectively. Therefore, in agriculture, heat or temperature stress is a significant problem in dealing with and sustaining high productivity of crops in agricultural fields (Zhang et al. 2019).
Temperature stress may lead to the improper functioning of plants such as inadequate seed germination, plant metabolism, seedling growth, and reduced plant yield (Khan et al. 2019). Enhanced production of ROS ultimately leads to oxidative stress as a major consequence of high-temperature stress (Fahad et al. 2016). However, based on the duration and severity of temperature stress, the agricultural crop yield was significantly affected (Hedhly et al. 2009). Munir et al. (2015) reported the impacts of climatic warming on all water table treatments and inferred that warming significantly enhanced the CO2 sink function of drained hummocks and shrub growth. Higher temperatures, ranging from 30 to 38 °C, inhibit or delay the seed germination process (Prasad et al. 2014). It has been reported that the reproductive stages of lentil, chickpea, mung bean, sorghum, and wheat plants are more sensitive to higher temperatures or heat stress (Sita et al. 2017). Fahad et al. (2018) reported in their review paper that by the end of twenty-first century, a 41% reduction in rice yield was estimated owing to global temperature change. However, an increase in the temperature could also result in an additive effect. Similarly, Samson et al. (2018) hypothesized that the increased temperature and decreased water table levels would result in increased carbon loss via respiration. Proline plays a crucial role in plant growth and flowering. However, under abiotic stress, the amino acid proline accumulates in the plants. Therefore, proline transport is disrupted. Under high temperatures during male reproductive processes, sugar metabolism causes fruit setting failure, especially in tomato plants (Mattioli et al. 2008; Siddique et al. 2018).
Crop productivity can be improved by mitigating abiotic stress using beneficial microbes (Gill et al. 2016). Under abiotic stress conditions, plant growth is facilitated by the application of PGPB either by a direct mechanism, such as enhancement of nutrient availability and production of plant growth regulators, or by an indirect mechanism, such as ISR, suppression of plant pathogens by antibiosis, and synthesis of lytic enzymes (Glick 2014). The literature reveals that bacteria have the ability to produce ACC deaminase to supply nitrogen and energy to plants in appropriate amounts during abiotic stress conditions. Bacteria possessing ACC deaminase activity help plants induce longer roots and take up more water under stress conditions, thereby increasing the efficiency of plants under abiotic stress conditions (Zahir et al. 2009).
Kaur et al. (2018) reported that ACC deaminase producers Azotobacter sp. and Streptomyces badius mitigated climate change and enhanced wheat plant growth and yield. The experiments conducted over two consecutive years enhanced plant height, spike length, grain weight, grains per spike, and grain yield. Furthermore, inoculation of ACC deaminase–producing bacterium B. cereus promoted root and shoot length, fresh and dry weight, leaf surface area, and EPS production in Solanum lycopersicum L. (tomato plant) by reducing the adverse effects of heat stress (Mukhtar et al. 2020) (Table 4). Other mechanisms such as siderophore production, phytohormone production (indole-3-acetic acid, cytokinins, gibberellic acid, and abscisic acid), and antibiotics also play a vital role in managing abiotic stress conditions. The bacteria possessing the ability to produce antioxidants helps in degrading reactive oxygen species and enhance abscisic acid accumulation (Mukhtar et al. 2020).
Management of some miscellaneous environmental stresses by ACC deaminase–producing bacteria
ACC deaminase–producing bacteria helps in managing the impact of different environmental stressors on plants. The symbiotic performance of many rhizobial strains increases because of both endogenous and exogenous ACC deaminase genes. ACC deaminase production helps plants enhance their tolerance to different environmental stressors (Nascimento et al. 2012).
Flooding
Flooding is a significant abiotic stress factor affecting plant growth and agricultural productivity. Plant roots become hypoxic- or oxygen-limited due to flooding, thereby increasing the amount of ACC synthase enzyme and other stress proteins (Li et al. 2013). Plants cannot convert newly synthesized ACC into ethylene in their roots because of the lack of ethylene oxygen. Therefore, plants transport ACC to the plant shoot, where ACC can be converted into ethylene in an aerobic environment (Glick 2014). During flooding, ethylene production results in a reduced biomass yield and conditions of leaf chlorosis, necrosis, and epinasty (wilting). It has been reported that the damage caused by flooding can be managed to some extent by treating plants with ACC deaminase–producing PGPR (Barnawal et al. 2012; Li et al. 2013). Pseudomonas putida UW4, Bradyrhizobium and Enterobacter cloacae are some of the ACC deaminase producers that reduce the damage caused by flooding (Grichko and Glick 2001; Fougnies et al. 2007; Grover et al. 2011) (Table 5).
Flower wilting
In most plants, senescence of flowers is initiated by ethylene. Woltering and Dan (1988) reported that not all flowers are sensitive to ethylene. Many cut flowers, such as lilies and carnations, are first treated with either silver thiosulfate or a chemical ethylene inhibitor before sale. If the concentration of silver thiosulfate is high, it is a phytotoxic and hazardous to the environment (Abeles et al. 2012). Application of PGP bacteria–possessing ACC deaminase activity act as an alternative to silver thiosulfate, which is an environmentally friendly alternative to treat cut flowers that naturally limits ethylene production (Ali et al. 2012).
It has been shown that application of PGP bacteria–possessing ACC deaminase activity to the stems of cut flowers (carnations) decreases the flower senescence. Therefore, it is essential to dissect petals from carnation flowers before treating them with bacteria-possessing ACC deaminase activity to delay petal senescence by approximately 5–6 days (Nayani et al. 1998). Ali et al. (2012) reported that in maltese cross (Lychnis) flower senescence, the application of PGPB delayed senescence by up to 2–3 days compared to untreated flower petals. This indicates that bacteria-possessing ACC deaminase activity mimic the chemical inhibitors of cut flowers. It has been demonstrated that compared to root adhering bacteria, endophytic bacteria with ACC deaminase activity delayed flower senescence by 2–3 days (Ali et al. 2012).
Conclusions and future prospects
In today’s scenario, the human population is increasing daily, and feeding them all is a significant constraint. Moreover, agricultural productivity is greatly influenced by climatic factors such as temperature, heat, cold, precipitation, drought, salinity, and metal stress. These climatic changes have had negative impacts on the hydrological, arable, and livestock sectors. Climate change in agricultural ecosystems may result in changes in biodiversity, resulting in blight and pests. Due to climate change, changing patterns of disease and insect pests have raised the need for eco-friendly approaches and improved agricultural practices for sustainable crop production. Therefore, to feed the world or to meet the people’s demand, it is required that the agricultural productivity should also get an increase. In this context, a large agricultural field, increased use of chemical fertilizers, herbicides, pesticides, greater use of transgenic crops, farm mechanization, and the expanded use of PGPB are required at the initial level. The emerging pandemic situation like covid has increased consumer demand for organic and healthy food, which should be free from pesticide residues and chemical fertilizers. Currently, people are aware of the benefits of using biofertilizers instead of chemical fertilizers. For long-term solution, increasing the use of PGP bacteria is a viable option. Application of PGPB are eco-friendly biological solutions that promote plant development, and it has been revealed that plants produce an excess amount of ethylene during stress (climate change) conditions result in a decrease in agricultural productivity. Therefore, PGP bacteria–possessing ACC deaminase activity lower the ethylene level in plants by reducing ACC to ammonia and α-ketobutyrate, thereby directly improving the plant growth and productivity.
The research on ACC deaminase–producing bacteria may become a mainstay of plant agriculture in the future. It is evident that the bacteria-possessing ACC deaminase activity may have a higher chance of surviving under abiotic environmental stressors. Thus, it has been concluded that the bacteria-possessing ACC deaminase activity can help farmers protect plants by mitigating various environmental stresses as stress modulators. Hence, common people as well as farmers will be benefitted in terms of increased crop productivity, decreased post-harvest spoilage as well as good quality and quantity of crop availability. In conclusion, for the management of abiotic stresses, ACC deaminase–producing bacteria can be utilized as bioinoculants to attain sustainable agriculture in the near future by maintaining the equilibrium in ethylene content, which is crucial for plant growth and development under abiotic stress conditions.
Data availability
All data generated or analyzed during this study are included in this published article.
Abbreviations
- PGPB:
-
Plant growth–promoting bacteria
- α :
-
Alpha
- ACC:
-
1-Aminocyclopropane-1-carboxylic acid
- PGPR:
-
Plant growth–promoting rhizobacteria
- ACCD:
-
1-Aminocyclopropane-1-carboxylic acid deaminase
- kDa:
-
Kilo dalton
- Lys:
-
Lysine
- PLP:
-
Pyridoxal-5-phosphate
- β:
-
Beta
- CO2 :
-
Carbon dioxide
- ROS:
-
Reactive oxygen species
- CAT:
-
Catalase
- GR:
-
Glutathione reductase
- APX:
-
Ascorbate peroxidase
- SOD:
-
Superoxide dismutase
- dS/m:
-
Decisiemens per meter
- CaCl2 :
-
Calcium chloride
- MgCl2 :
-
Magnesium chloride
- NaCl2 :
-
Sodium chloride
- ISR:
-
Induced systemic resistance
- RWC:
-
Relative water content
- Cr:
-
Chromium
- Fe:
-
Iron
- NPK:
-
Nitrogen, phosphorus, and potassium
- Ni:
-
Nickel
- Cd:
-
Cadmium
- Cu:
-
Copper
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This work was supported by the Gujarat Environmental Management Institute (GEMI), Govt. of Gujarat, Gandhinagar, under Research and Development proposals for researchers to NA (GEMI/726/1002/2017).
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NA: designed the study and edited final manuscript; SC: collected the data and wrote the manuscript.
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Chandwani, S., Amaresan, N. Role of ACC deaminase producing bacteria for abiotic stress management and sustainable agriculture production. Environ Sci Pollut Res 29, 22843–22859 (2022). https://doi.org/10.1007/s11356-022-18745-7
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DOI: https://doi.org/10.1007/s11356-022-18745-7