Morphological Diversity and Transcriptomic Profiling of Multicellular Trichomes in Kiwifruit

Fruit trichomes and pericarp architecture are pivotal for biological defense and postharvest resilience in the genus Actinidia. However, the evolutionary diversity of these structures and the molecular mechanisms governing their development—particularly under the influence of polyploidization—remain poorly understood. We performed a systematic evaluation of 21 Actinidia species and 14 cultivars using scanning electron microscopy (SEM) and histological analysis. To determine the effects of genome doubling, an autotetraploid line was induced from diploid A. chinensis cv. 'Donghong', followed by comparative transcriptomic and temporal expression profiling. Morphological characterization identified three distinct evolutionary groups based on fruit surface traits: glabrous, caducous-spotted, and persistent-pubescent. All observed trichomes featured a unique bipartite multicellular architecture. Kiwifruit pericarp thickness (59.8–534.6 μm) was locally reinforced at trichome insertion sites. Among kiwifruit cultivars, polyploidization significantly increased both trichome length and total amount. Transcriptomic analysis revealed 235 differentially expressed genes (DEGs) enriched in hormonal signaling and flavonoid pathways. Two key candidate genes, Achv4p15g023764.t1 and Achv4p01g000003.t1, were identified as candidate gene for stage-specific regulators governing early morphogenesis and late maturation. These findings provide a structural roadmap of Actinidia epidermal evolution and identify specific genetic targets for the molecular breeding of cultivars with optimized surface protection and postharvest resilience.