The polyphenolic suberized peridermal skin of the Sikkim cucumber acts as an effective chemical barrier against Botrytis cinerea infection

Abstract

Certain species of fleshy fruit that undergo skin cracking are capable of forming a specialized polyphenolic periderm to seal the wounded skin. Some of the genetic and metabolic components pertaining periderm formation have been identified, however it remains unknown if, and to what extent, this specialized tissue can act as an efficient barrier against the invasion of pathogenic fungi. We monitored the infection process of Botrytis cinerea on the cuticle-coated skin of the common cucumber (Cucumis sativus) or on the polyphenolic suberized peridermal skin of the Sikkim cucumber (C. sativus var. sikkimensis). In vivo inoculation assays inferred that while B. cinerea can successfully penetrate and form necrotic lesions on sativus fruit, it is incapable of penetrating the peridermal skin of sikkimensis fruit. Gas chromatography-mass spectrometry (GC-MS) profiling of fruit skin extracts, in vitro conidial germination and germ tube elongation assays, and qRT-PCR cutinase-encoding gene expression analyses, inferred that the accumulation of suberin monomers in the peridermal skin of sikkimensis fruit stimulate increased elongation of B. cinerea germ tubes and significantly alters the differential expression of cutinase-encoding genes. Among them, Bcin0607010, Bcin08g01580 and Bcin07g06480, three yet unidentified cutinases, whose expression is specifically increased in the presence of sikkimensis fruit skin extracts. Our data demonstrate that a polyphenolic suberized peridermal skin in cucumber fruit can shape the interactions with B. cinerea and implies that suberization of fleshy fruit may provide a means for reducing damage imposed by this and other pathogens.