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Thaxtomin A: a promising alternative to synthetic herbicides

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(1)

Benoit Deflandre

1

, Samuel Jourdan

1

, Isolde M Francis

2

, Rosemary Loria

3

and Sébastien Rigali

1

1

InBioS - Center for protein engineering, Dpt. of Life Sciences, University of Liège, Liège, Belgium

2

Department of Biology, California State University, Bakersfield, California, USA

3

Department of Plant Pathology, University of Florida, Gainesville, Florida, USA

Contact:

benoit.deflandre@doct.uliege.be

Thaxtomins are natural phytotoxins produced by pathogenic Streptomyces sp.

[1.]

[2.]

A promising bioherbicide interfering with cellulose biosynthesis mechanisms

Streptomyces scabies is the model and most widely-studied pathogenic Streptomyces species. It is responsible for the common scab (CS) disease affecting tuber crops and notably potato (Solanum tuberosum) cultures causing significant yield losses. Thaxtomin A is the main virulence determinant produced by S. scabies and other related species. Its yellow pigmentation is used as a natural reporter system for the phytotoxin production. [1.] Electron microscope view of a growing S. scabies mycelium perforating the surface of a potato tuber; [2.] Chemical structure of thaxtomin A; [3.] Potato tubers showing surface lesions caused by the CS disease upon infection by a pathogenic Streptomyces sp.

Thaxtomin A was shown to be active at very low concentrations (0.4 – 40 ppb), causing symptoms such as cell hypertrophy, root/shoot stunting and tissue necrosis at higher concentrations. Although its precise action mechanism is still unclear, standard phytotoxicity assays have shown that thaxtomins induce symptoms similar to isoxaben, a well-known cellulose inhibitor. [4.] Developmental impact of thaxtomin A treatment (1 µM, right) on Arabidopsis thaliana seedling compared to control untreated seedling (left); [5.] Potato tuber tissue treated (a) or not (b) with 100 nM of thaxtomin A. The treated slice displays necrosis induced by thaxtomin; [6.] Thaxtomin A causes cell hypertrophy on a radish hypocotyl (lateral view in (a) and cross section in (b)) compared to an untreated hypocotyl (c); [7.] Length of onion seedlings exposed to increasing concentrations of thaxtomin A (0.05 – 0.5 µM); [8.] Thaxtomin inhibits14C-glucose incorporation into the cellulosic cell wall fraction of A. thaliana seedlings. Black bars: Cellulosic (acid-insoluble)

cell wall fraction ; Cross-hatched bars: Acid-soluble cell wall fraction; White bars: Percentage of label in the cellulose fraction relative to the amount of total label in the cell wall.

© Loria et al. 2003

[4.]

© Loria et al. 2003

[3.]

© Loria et al. 2003

[5.]

© Loria et al. 2006

[7.]

© Fry and Loria 2006

[8.]

© Scheible et al. 2003

[6.]

© Loria et al. 1997

Unexpected constitutive thaxtomin

production after deletion of a β-glucosidase

How computational predictions helped

improving thaxtomin yields

Using the PREDetector software, two CebR-binding sites (cbs) have been highlighted in the gene cluster involved in thaxtomin biosynthesis [9.]. CebR, the master repressor of cellulose utilization has been deleted to generate a new S. scabies (∆cebR) strain capable of producing thaxtomin A constitutively [10.]. This strain also produces significantly more thaxtomin A without requiring the addition of expensive cello-oligosaccharides (CebR allosteric effectors) to the culture medium.

bglC is a gene located in the ceb operon which controls the import and processing of cellulose oligo-saccharides. BglC is a β-glucosidase that processes cello-oligosaccharides into glucose (Glc) [11.]. As [Glc]2and

[Glc]3 are inducers of thaxtomin

biosynthesis, deleting an enzyme responsible for their depletion was expected to increase thaxtomin production compared to the wild-type strain. Indeed, S. scabies ∆bglC produced more thaxtomin A, but this mutant was also shown to be a constitutive producer [12.]. This unexpected phenotype is valuable because this strain is even more efficient than the ∆cebR mutant for thaxtomin production. Understanding the mechanisms responsible for this thaxtomin A overproduction in the ∆bglC mutant could help us improving production strains.

[12.]

[10.]

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