A Model For the Lowering of Plant Ethylene Concentrations by Plant Growth-promoting Bacteria

“Once established, they can enhance plant health and/ or growth by producing plant growth regulating compounds such as indole acetic acid (IAA), acetoin (3-hydroxy-2-butanone), 2,3butanediol and cytokinins, or metabolize compounds like phenyl acetic acid (PAA), gamma-aminobutyrate (GABA) or the stress ethylene precurso…”

“Through this, ACC deaminase–producing PGPRs help in utilization of ACC to decrease the level of ACC outside the plants to equalize with that of inside levels (Glick et al., 1998).”

“decrease the ethylene level thus preventing the inhibition of the root growth by ethylene (Glick et al. 1998).”

“These bacteria, when present in the root vicinity, substantially decrease ethylene production in inoculated roots which results in the promotion of root growth (Glick et al. 1998; Glick 2004; Shaharoona et al. 2007b).”

“These PGPR bound to plant roots act as sink for ACC (Glick et al. 1998) and there by lower the level of ethylene in a developing seedling or stressed plant (Mayak et al.”

“Thus, decrease in the level of ACC affects biosynthesis of the stress hormone Frontiers in Microbiology | www.frontiersin.org 3 September 2015 | Volume 6 | Article 937 ethylene in host plants and stimulate plant growth (Honma et al., 1993; Glick et al., 1998).”

“The plant growth promotion by rhizosphere bacteria was observed by several authors (Belimov et al., 2005; Glick et al., 1998; Gupta et al., 2002) and reported to be due to the utilization of ACC, synthesis of phytohormones and solubilization of minerals.”

“[12] to explain the role of bacterial ACC deaminase and IAA in promoting plant growth.”

“4 Hypothetical model illustrating the steps involved in lowering of plant ethylene levels and other activities of Methylobacterium in plant growth promotion (modified from Glick et al. 1998).”

“Glick et al. (1998, 2007) FEMS Microbiol Lett 305 (2010) 42–48 Journal compilation c 2010 Federation of European Microbiological Societies Published by Blackwell Publishing Ltd.”

“A very similar phenomenon has been reported for a number of rhizobacteria that express the enzyme 1-aminocyclopropane-1-carboxylate deaminase and are capable of lowering the plant endogenous levels of another plant hormone, ethylene (12).”

“, 2017), they vigorously promote plant biomass accumulation (Glick, 2003), allowing faster remediation than without PGPR application (Glick et al., 1998).”

“ACC deaminase inhibits stress ethylene synthesis and was shown to mitigate stress caused by the presence of heavy metals in plant tissues (Burd et al. 1998; Glick et al. 1998).”

“In this study, we were interested in studying another mechanism known to be used by plant growth-promoting bacteria to decrease ethylene levels in plants (9, 10).”

“In addition, PGP bacteria can overcome growth inhibition caused by heavy metal stress via the metabolization of 1-aminocyclopropane-1-carboxylic acid (ACC), the immediate precursor of ethylene ( Glick et al , 1994 ; Glick, Penrose, and Li, 1998 ; Glick, 2004 ).”

“IAA promotes root growth by stimulating cell elongation and division (Glick et al., 1998).”

“Inoculation of various plants with ACC deaminase-producing PGPR had been reported to lower the level of ACC and thus ethylene within the plant, reduce the extent of its inhibition of root elongation (Glick et al. 1998; Penrose et al. 2001; Glick and Penrose 2004) and promote plant growth (Belimov et al.”

“…the plant ethylene precursor ACC to ammonia and α-ketobutyrate, thereby lowering the level of ethylene under various biotic and abiotic stresses (Glick et al. 1998), such as salt stress (Cheng et al. 2007, Mayak et al. 2004a; Zahir et al. 2009), flooding stress (Grichko and Glick 2001),…”

“Organisms that produce ACC deaminase normally bind to plant tissues, and take up ACC to convert into ammonia and aketobutyrate [2].”

“…signalling have been reported (see, for review, Dodd et al., 2010), such as decreased ethylene production via bacterial ACC deaminase activity (Glick et al., 1998; Belimov et al., 2009), changes in cytokinin–ABA balance (Figueiredo et al., 2008; Cohen et al., 2009) or changes in auxin…”

“to ammonia and α-ketobutyrate which consequently reduces the extent of ethylene growth inhibition [43, 44].”

“Moreover, PGPR contain enzymes that modulate plant growth and development (Glick et al. 1998 ; Sheng and Xia 2006 ; Ma et al. 2009 ) .”

“This study is consistent with the work of Moon and Ali [99] mentioned above as well as a model of ACC deaminase functioning postulated earlier [90].”

“The IAA released by bacteria enhances plant growth directly by stimulating elongation of the cell or affecting cell division (Glick et al., 1998).”

“The ability of ACC-utilizing PGPR to eliminate plant growth inhibition caused by ethylene was postulated as an important mechanism of plant– bacteria interactions (Glick et al. 1998).”

“Higher levels of NO 3 in the rooting medium stimulate ACC-oxidase activity leading to increased ethylene production, which is generally believed to be inhibitory to root growth (Glick et al., 1998).”

“ACC producing bacteria have the ability to supply the nitrogen and energy to plants [32].”

“The ACC, the immediate precursor of C2H4, when hydrolysed by ACC deaminase results in NH3 and α-ketobutyrate formation (Glick et al. 1998; Penrose and Glick 2003; Reed et al. 2005; Safronova et al. 2006), and hence, it strongly alleviates the stress induced by ethylene-mediated impact on plants by…”

“In a model described by Glick et al. (1998), PGPB colonize the seed or root of a developing plant and, in response to tryptophan and other small molecules in seed or root exudates (Bayliss et al. 1997; Penrose and Glick 2001), the bacteria synthesize and secrete IAA (Patten and Glick 1996, 2002).”

“ACCD production has also been proposed as a key beneficial factor in PGPR action (Glick et al., 1998) and used as a selection criterion in primary screening for many PGPRs.”

“, 1999); production of phytohormones which can enhance the growth of plants (Glick et al., 1998); and solubilisation of phosphate (Gupta et al.”

“Previously, several papers have reported that some PGPR strains reduce ethylene levels in plant tissues by producing ACC deaminase, which is an enzyme that degrades endogenous ethylene (Glick et al., 1998).”

“In a model developed previously to explain the role of ACC deaminase in the promotion of plant growth by free-living root surface-binding bacteria (i.e. plant growth-promoting rhizobacteria), the following scenario was suggested (Glick et al., 1998).”

“Several bacterial endophytes have been reported to support plant growth by providing phytohormones, low-molecular compounds or enzymes (Lambert & Joos, 1989; Frommel et al., 1991; Glick et al., 1998).”

“…been shown to stimulate plant growth through the activity of 1-aminocyclopropane-1-carboxylate (ACC) deaminase, which reduces plant ethylene level under unfavorable conditions and confers resistance to stress, by catalyzing the conversion of ACC into ammonia and α-ketobutyrate (Glick et al. 1998).”

“Indeed, these bacteria may improve plant growth and developmental processes (Glick 1995; Glick et al. 1998; Ryan et al. 2008; Schulz and Boyle 2006) by producing a range of nutrient products and facilitating primary and secondary nutrient uptake through atmospheric nitrogen fixation (Gothwal et al.…”

“Glick et al. (1998) previously proposed that ACC might be exuded from plant roots and that soil bacteria containing ACC deaminase could convert this for their growth.”

“ACC is exuded from seeds or plant roots and then metabolized by bacteria expressing ACC deaminase activity, which stimulates plant ACC efflux, decreasing the root ACC concentration and root ethylene evolution and increasing root growth (39).”

“A model describing the role of ACC deaminase in plant-growth-promoting bacteria suggests that Rhizobacteria, attached to the surface of the plants seeds or roots, can take up some of the ACC that is exuded from the seeds or roots and cleave it thereby decreasing the level of ethylene in the plant and its inhibitory ef…”

“Bacteria that produce the enzyme ACC deaminase can directly use plant-synthesized ACC as carbon and nitrogen sources, and, at the same time, lower the ACC levels within plant tissues (Glick et al., 1998; Penrose et al., 2001; Belimov et al., 2009).”

“These bacteria bind to plant roots and act as a sink for ACC (Glick et al. 1998), hydrolyzing it to ammonia and a-ketobutyrate and thereby lowering the level of ethylene in developing seedlings of stressed plants (Mayak et al.”

“One group of plant growth-promoting bacteria (PGPB) (also referred to as PGPR, plant growth-promoting rhizobacteria) is comprised of bacterial strains that can lower plant ethylene levels and promote plant growth via the enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase (Glick et al. 1998; Gerhardt, Greenberg,…”

“, 2006; Veerubommu and Kanoujia, 2011), competition for space, nutrients and ecological niches, production of antimicrobial substances, or through production of phytohormones and peptides acting as bio stimulants without negative effects on the user, consumer or the environment (Glick et al., 1998; Johnsson et al., 19…”

“Lowering of plant ethylene levels by plant growth-promoting bacteria containing 1-aminocyclopropane1-carboxylate (ACC) deaminase can reduce the harmful effects of these and other stresses (Glick et al. 1998; Grichko and Glick 2001; Mayak et al. 2004a, 2004b; Burd et al. 1998, 2000; and Wang et al. 2000).”

“Furthermore, plant stress can be reduced by ACC deaminase-producing bacteria which can lower the level of the plant stress hormone ethylene (Okon and Itzigsohn 1995; Glick et al. 1998, 2007 ; O kon et al.1998 ;D obbelaere et al.1999; Belimov et al. 2009).”

“This enzyme has been reported to be responsible for the stimulation of plant growth by causing a decrease in ethylene levels (Wang et al. 2002; Glick et al. 1998; Sun et al. 2009).”

“The first, leading to a reduction in ethylene production, is the result of the bacterium sequestering the ethylene precursor 1-aminocyclopropane-1-carboxylate (ACC) from the plant and then hydrolyzing it through the action of the enzyme ACC deaminase ( Glick et al. 1994, 1998, Hall et al. 1996).”

“A model proposed by Glick et al. (1998) suggests that ACC is exuded from seeds or plant roots, and it is metabolized by bacteria expressing ACC deaminase activity.”

“The optimal temperature for ACC deaminase activity is 30°C (Glick et al., 1998).”

“Several bacterial endophytes have been shown to support plant growth and increase nutrient uptake by providing phytohormones (Jacobson et al. 1994), low molecular weight compounds (Frommel et al. 1991), enzymes ( Glick et al. 1998 ), antimicrobial substances like antibiotics (Bangera and Thomashow 1996) and siderophor…”

“It has been demonstrated that in areas with abiotic stress factors, plants are more dependent on microorganisms that are able to enhance their ability to combat stress [8],[9],[10],[11] and [12].”

“It has been suggested that organic acids play an important role in heavy metal tolerance, for example, citrate for Zn tolerance (Godbold et al., 1984) and malate for Ni tolerance (Yang et al., 1997). Jones and Darrah (1994) indicated that citric acid secreted by plant roots is an effective Al-chelator for decreasing A…”

“…composition of root exudates and soil pH (Chen et al. 2015), bacteria have been shown to alleviate toxicity of heavy metals (Farwell et al. 2007) and hence increase plant growth via reduction in ethylene production under stress, nitrogen fixation and specific enzyme activity (Glick et al. 1998).”

“A number of bacterial strains expressing ACC deaminase have been isolated in laboratory conditions worldwide and reported their PGPR activity [57, 58].”