Topography-Driven Shape, Spread, and Retention of Leaf Surface Water Impacts Microbial Dispersion and Activity in the Phyllosphere

Abstract

To study the impact of lateral variation in surface topography on the microbial colonization of plant leaves, we used a two-step casting process to generate topomimetic “replicasts” in polydimethylsiloxane which faithfully resembled leaf surface topography at submicrometer scale. This process revealed that the shape and size of the phyllotelma—the collective body of standing water on a leaf surface—was a function of wetting method and presence of surface features, in particular leaf veins. The use of dyes and fluorescently labeled bacteria showed that these veins, especially on the abaxial side, contributed to the pooling, retention, and lateral spread of water and microorganisms. Bodies of water along veins acted as conduits that allowed bacterial cells to sense chemicals over distances exceeding their body length by four orders of magnitude. Bacterial survival rates under conditions of low relative humidity were twice as high on leaf replicasts as on flat surfaces, suggesting topography-dependent protection from desiccation. Our findings highlight the need for greater quantitative understanding of the impact of leaf surface topography on phyllotelma connectivity and the outcomes of interactions between microorganisms and with their plant host. Such understanding benefits both theory and practice of phyllosphere microbiology in areas such as foliar disease management and food safety of leafy greens.