Physical, Chemical and Proteomic Evidence of Potato Suberin Degradation by the Plant Pathogenic Bacterium Streptomyces scabiei

Abstract

Potato peels consist of a tissue called phellem, which is formed by suberized cell layers. The degradation of suberin, a lipidic and recalcitrant polymer, is an ecological process attributed to soil fungal populations; however, previous studies have suggested that Streptomyces scabiei, the causal agent of potato common scab, possesses the ability to degrade suberin. In the present study, S. scabiei was grown in medium containing suberin-enriched potato phellem as the sole carbon source and its secretome was analyzed periodically (10- to 60-d-old cultures) with a special focus on proteins potentially involved in cell wall degradation. Although the amount and diversity of proteins linked to polysaccharide degradation remained high throughout the experiment, their abundance decreased over time. In contrast, proteins dedicated to lipid metabolism represented a small fraction of the secretome; however, their abundance increased during the experiment. The lipolytic enzymes detected may be involved in the degradation of the aliphatic fraction of suberin because the results of optical and transmission electron microscopy examinations revealed a loss in the integrity of suberized tissues exposed to S. scabiei cells. Chemical analyses identified a time period in which the concentration of aliphatic compounds in potato phellem decreased and the sugar concentration increased; at the end of the 60-d incubation period, the sugar concentration in potato phellem was significantly reduced. This study demonstrated the ability of S. scabiei to degrade the aliphatic portion of suberin.

Fig. 1

Potato phellem disks after a 12-month incubation in A) the absence or B) presence of Streptomyces scabiei EF-35.

Fig. 2

Transmission electron micrographs of potato phellem incubated in the presence of Streptomyces scabiei EF-35 for 0 to 60 d. PW: primary cell wall; SW: suberized secondary cell wall; TW: tertiary cell wall. ^* shows the zone of secondary wall detachment. White arrows show suberin lamellae detached from the secondary wall. Black arrows show broken suberin lamellae.

Fig. 3

Ratio between concentrations of aliphatic compounds (fatty acids, fatty alcohols, α,ω-dioic acids, ω-hydroxy acids, and ferulic acid) and sugars (arabinose, xylose, rhamnose, fucose, mannose, galactose, and glucose) in potato phellem after an incubation in the presence of Streptomyces scabiei EF-35 for 0 to 60 d. Values accompanied by the same letter did not differ significantly (LSD test).

Fig. 4

Concentration of sugars in potato phellem after an incubation in the presence of Streptomyces scabiei EF-35 for 0 to 60 d. Values within a panel accompanied by the same letter did not differ significantly (LSD test).

Fig. 5

Concentration of aliphatic compounds in potato phellem after an incubation in the presence of Streptomyces scabiei EF-35 for 0 to 60 d. Values within a panel accompanied by the same letter did not differ significantly (LSD test).

Fig. 6

Temporal variations in Streptomyces scabiei protein distribution within functional groups. A) Relative protein abundance (normalized spectral abundance factor) within functional protein groups; B) relative number of proteins assigned to each functional group.

Fig. 7

Similarity index of extracellular protein profiles between 10- to 60-d-old PPM cultures of Streptomyces scabiei EF-35. A) Total extracellular proteins; B) proteins associated with the Carbohydrate metabolism class only, and C) proteins associated with the Lipid metabolism class only.