Transpiration from Tomato Fruit Occurs Primarily via Trichome-Associated Transcuticular Polar Pores

Nonstomatal water loss by transpiration through the hydrophobic cuticle is ubiquitous in land plants, but the pathways along which this occurs have not been identified. Tomato (Solanum lycopersicum) provides an excellent system in which to study this phenomenon, as its fruit are astomatous and a major target for desiccation resistance to enhance shelf life. We screened a tomato core collection of 398 accessions from around the world and selected seven cultivars that collectively exhibited the lowest and highest degrees of transpirational water loss for a more detailed study. The transpirational differences between these lines reflected the permeances of their isolated cuticles, but this did not correlate with various measures of cuticle abundance or composition. Rather, we found that fruit cuticle permeance has a strong dependence on the abundance of microscopic polar pores. We further observed that these transcuticular pores are associated with trichomes and are exposed when the trichomes are dislodged, revealing a previously unreported link between fruit trichome density and transpirational water loss. During postharvest storage, limited self-sealing of the pores was detected for certain cultivars, in contrast with the stem scar, which healed relatively rapidly. The abundance of trichome-associated pores, together with their self-sealing capacity, presents a promising target for breeding or engineering efforts to reduce fruit transpirational water loss.