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

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.

[1]  J. Nowak,et al.  Inhibitory effect of endophyte bacteria on Botrytis cinerea and its influence to promote the grapevine growth , 2002 .

[2]  T. Burr,et al.  CROWN GALL OF GRAPE: Biology and Disease Management. , 1999, Annual review of phytopathology.

[3]  P. Newell,et al.  A novel procedure for rapid isolation of plant growth promoting pseudomonads , 1995 .

[4]  M. Chilton,et al.  Fingerprints of Agrobacterium Ti plasmids. , 1978, Plasmid.

[5]  B. Glick,et al.  A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria , 1998, Journal of theoretical biology.

[6]  P. Vandamme,et al.  Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant-beneficial properties. , 2005, International journal of systematic and evolutionary microbiology.

[7]  B R Glick,et al.  Reduced symptoms of Verticillium wilt in transgenic tomato expressing a bacterial ACC deaminase. , 2001, Molecular plant pathology.

[8]  Harry J. Klee,et al.  Ethylene Regulates the Susceptible Response to Pathogen Infection in Tomato , 1998, Plant Cell.

[9]  K. Fischer,et al.  Ethylene production and ACC‐accumulation in Agrobacterium tumefaciens‐induced plant tumours and their impact on tumour and host stem structure and function , 1999 .

[10]  R. Aloni,et al.  Biology of Crown Gall Tumors , 2008 .

[11]  Bernard R. Glick,et al.  Effect of transferring 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase genes into Pseudomonas fluorescens strain CHA0 and its gacA derivative CHA96 on their growth-promoting and disease-suppressive capacities. , 2000 .

[12]  Brendan J. McConkey,et al.  Promotion of Plant Growth by Bacterial ACC Deaminase , 2007 .

[13]  C. Koncz,et al.  Opines in crown gall tumours induced by biotype 3 isolates of Agrobacterium tumefaciens , 1988 .

[14]  W. Hartung,et al.  Development of Agrobacterium tumefaciens C58-induced plant tumors and impact on host shoots are controlled by a cascade of jasmonic acid, auxin, cytokinin, ethylene and abscisic acid , 2002, Planta.

[15]  T. Burr,et al.  Crown Gall of Grape: Biology of Agrobacterium vitis and the Development of Disease Control Strategies. , 1998, Plant disease.

[16]  B. Glick,et al.  The presence of a 1-aminocyclopropane-1-carboxylate (ACC) deaminase deletion mutation alters the physiology of the endophytic plant growth-promoting bacterium Burkholderia phytofirmans PsJN. , 2009, FEMS microbiology letters.

[17]  E. Szegedi,et al.  Agrobacterium: A disease-causing bacterium , 2008 .

[18]  B. Glick,et al.  Transgenic plants with altered ethylene biosynthesis or perception. , 2003, Biotechnology advances.

[19]  F. B. Abeles,et al.  Ethylene in Plant Biology , 2022 .

[20]  T. Tzfira,et al.  Agrobacterium: from biology to biotechnology. , 2008 .

[21]  I. Galis,et al.  Agrobacterium tumefaciens AK-6b gene modulates phenolic compound metabolism in tobacco. , 2004, Phytochemistry.

[22]  Trevor C. Charles,et al.  ACC deaminase from plant growth-promoting bacteria affects crown gall development. , 2007, Canadian journal of microbiology.

[23]  Trevor C. Charles,et al.  An ACC Deaminase Minus Mutant of Enterobacter cloacae UW4No Longer Promotes Root Elongation , 2000, Current Microbiology.

[24]  L. Chernin,et al.  Biological Control of Crown Gall in Grapevine and Raspberry by Two Pseudomonas spp. with a Wide Spectrum of Antagonistic Activity , 1998 .

[25]  Tokuji Shimomura,et al.  Metabolism of 1-Aminocyclopropane-1-carboxylic Acid , 1978 .

[26]  X. Liu,et al.  The Global Regulator Genes from Biocontrol Strain Serratia plymuthica IC1270: Cloning, Sequencing, and Functional Studies , 2004, Journal of bacteriology.

[27]  D. Hornby,et al.  Biological control of crown gall. , 1990 .

[28]  R. Aloni,et al.  The never ripe mutant provides evidence that tumor-induced ethylene controls the morphogenesis of agrobacterium tumefaciens-induced crown galls on tomato stems , 1998, Plant physiology.

[29]  G. Barry,et al.  Control of ethylene synthesis by expression of a bacterial enzyme in transgenic tomato plants. , 1991, The Plant cell.

[30]  G. Holguin,et al.  Transformation of Azospirillum brasilense Cd with an ACC Deaminase Gene from Enterobacter cloacae UW4 Fused to the Tetr Gene Promoter Improves Its Fitness and Plant Growth Promoting Ability , 2003, Microbial Ecology.

[31]  E. Szegedi Host range and specific smallcap˜L(+)tartrate utilization of biotype 3 of Agrobacterium tumefaciens. , 1985 .

[32]  J. Fages,et al.  Characterization of Azospirillum associated with maize (Zea mays) in France, using biochemical tests and plasmid profiles , 1992 .