Leaf abaxial and adaxial surfaces differentially affect the interaction of Botrytis cinerea across several eudicots

Abstract

Eudicot plant species have leaves with two surfaces: the lower abaxial and the upper adaxial surface. Each surface varies in a diversity of components and molecular signals, resulting in potentially different degrees of resistance to pathogens. We tested how Botrytis cinerea, a necrotroph fungal pathogen, interacts with the two different leaf surfaces across 16 crop species and 20 Arabidopsis genotypes. This showed that the abaxial surface is generally more susceptible to the pathogen than the adaxial surface. In Arabidopsis, the differential lesion area between leaf surfaces was associated with jasmonic acid (JA) and salicylic acid (SA) signaling and differential induction of defense chemistry across the two surfaces. When infecting the adaxial surface, leaves mounted stronger defenses by producing more glucosinolates and camalexin defense compounds, partially explaining the differential susceptibility across surfaces. Testing a collection of 96 B. cinerea strains showed the genetic heterogeneity of growth patterns, with a few strains preferring the adaxial surface while most are more virulent on the abaxial surface. Overall, we show that leaf–Botrytis interactions are complex with host-specific, surface-specific, and strain-specific patterns.