Inhibitory effect of ACC deaminase‐producing bacteria on crown gall formation in tomato plants infected by Agrobacterium tumefaciens or A. vitis

Abstract

This study showed that various rhizosphere bacteria producing the enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase (ACCD), which can degrade ACC, the immediate precursor of ethylene in plants, and thereby lower plant ethylene levels, can act as promising biocontrol agents of pathogenic strains of Agrobacterium tumefaciens and A. vitis. Soaking the roots of tomato (Solanum lycopersicum) seedlings in a suspension of the ACCD-producing Pseudomonas putida UW4, Burkholderia phytofirmans PsJN or Azospirillum brasilense Cd1843 transformed by plasmid pRKTACC carrying the ACCD-encoding gene acdS from UW4, significantly reduced the development of tumours on tomato plants injected 4-5 days later with pathogenic Agrobacterium strains via wounds on the plant stem. The fresh mass of tumours formed by plants pretreated with ACCD-producing strains was typically four-to fivefold less than that of tumours formed on control plants inoculated only with a pathogenic Agrobacterium strain. Simultaneously, the level of ethylene evolution per amount of tumour mass on plants pretreated with ACCD-producing bacteria decreased four to eight times compared with that from tumours formed on control plants or plants pretreated with bacteria deficient in ACCD production. Moreover, transgenic tomato plants expressing a bacterial ACCD were found to be highly resistant to crown gall formation relative to the parental, non-transformed tomato plants. The results support the hypothesis that ethylene is a crucial factor in Agrobacterium tumour formation, and that ACCD-produced rhizosphere bacteria may protect plants infected by pathogenic Agrobacteria from crown gall disease.

Evidence for the involvement of ACC deaminase from Pseudomonas putida UW4 in the biocontrol of pine wilt disease caused by Bursaphelenchus xylophilus

“…Similar results have been obtained with castor bean and tomato plants infected by Agrobacterium tumefaciens. While P. putida UW4 was able to decrease crown gall formation and subsequent damage and loss of plant biomass, the acdS knockout mutant had no significant impact on protecting tomato plants from the A. tumefaciens infection (Hao et al 2007;Toklikishvili et al 2010). These results suggest that ACC deaminase activity, and the consequent lowering of deleterious plant ethylene levels, is the mechanism responsible for P. putida UW4 plant growth promotion activity as well as its ability to protect plants against biotic as well as abiotic stress (Grichko et al 2000;Wang et al 2000;Cheng et al 2007;Glick et al 2007;Hao et al 2007;Gamalero et al 2010;Toklikishvili et al 2010).…”

“…While P. putida UW4 was able to decrease crown gall formation and subsequent damage and loss of plant biomass, the acdS knockout mutant had no significant impact on protecting tomato plants from the A. tumefaciens infection (Hao et al 2007;Toklikishvili et al 2010). These results suggest that ACC deaminase activity, and the consequent lowering of deleterious plant ethylene levels, is the mechanism responsible for P. putida UW4 plant growth promotion activity as well as its ability to protect plants against biotic as well as abiotic stress (Grichko et al 2000;Wang et al 2000;Cheng et al 2007;Glick et al 2007;Hao et al 2007;Gamalero et al 2010;Toklikishvili et al 2010). In addition, it has been previously demonstrated that transgenic plants that express a bacterial acdS gene under the control of a root specific promoter are more resistant to pathogen induced stress as well as abiotic stress caused by salt, flooding and metals (Robison et al 2001a, b;Grichko and Glick 2001;Grichko et al 2000;Stearns et al 2005;Sergeeva et al 2006).…”

“…This enzyme cleaves the ethylene precursor, ACC, into ammonia and a-ketobutyrate (Honma and Shimomura 1978) and thereby prevents ethylene levels in plants from rising to deleterious levels (Glick et al 1998. The ACC deaminase-producing bacterium Pseudomonas putida UW4 has been shown to be an effective PGPB protecting several different plant hosts from a variety of stress conditions including flooding, salt, pathogens and metals (Grichko et al 2000;Wang et al 2000;Grichko and Glick 2001;Cheng et al 2007;Hao et al 2007;Gamalero et al 2010;Toklikishvili et al 2010).…”

Bacterial Modulation of Plant Ethylene Levels

“…In this context, seedling inoculation with bacteria expressing ACC deaminase may reduce pathogen-induced ethylene, e.g. for soil-borne disease caused by pathogenic bacteria such as Pseudomonas syringae pv tomato (Indiragandhi et al, 2008), Agrobacterium tumefaciens (Toklikishvili et al, 2010;Hao et al, 2011), Erwinia spp. (Wang et al, 2000), and fungi, including Pythium ultimum (Wang et al, 2000), Pythium aphanidermatum (El-Tarabily, 2013), and Pyricularia oryzae (Amutharaj et al, 2012).…”

Micro-Level Management of Agricultural Inputs: Emerging Approaches

“…The plant growth promoting effects of ACC deaminase may be most effective during pathogen attack [94,[170][171][172] and in stressful environments (e.g., flooded and heavy-metal contaminated soils) [173,174]. Additionally, under stress conditions plant vitamin synthesis declines.…”