Unravelling the physiological and anatomical basis of divergent adaptations in cultivated and wild tomatoes

Distinct physiological and anatomical traits can lead to substantial variation in photosynthetic efficiency among plant varieties, which may, in turn, impact agronomically important traits. We conducted a comprehensive comparative analysis of leaf physiology, anatomy, and biochemistry in Solanum lycopersicum (LEA), a modern inbred variety suited for the processing industry, and Solanum pennellii (Lost, accession LA5240), a drought-tolerant, green-fruited wild species, to investigate differences in photosynthetic performance and stomatal physiology. Lost exhibited higher photosynthetic capacity due to both biochemical and anatomical features. Chlorophyll fluorescence revealed that photosynthesis operates at a higher rate in Lost, due to greater electron sink capacity and efficient electron flow through the photosystems. Lost also showed higher Rubisco content as well as greater chlorophyll a/b ratio and total soluble protein levels than LEA, demonstrating investments in carbon capture relative to light harvesting to support superior photosynthetic performance at higher light intensities. Equal stomatal numbers on the abaxial and adaxial surface for Lost supported its greater leaf thickness and higher photosynthetic capacity, whilst LEA's greater stomatal density on the abaxial surface is typical of commercial broadleaf crops. Grafting experiments demonstrated that LEA scions grafted onto Lost rootstocks displayed improved photosynthesis compared with non-grafted LEA and LEA self-grafted plants, demonstrating successfully transferred enhanced photosynthetic traits from rootstock of Lost to LEA scions. Our study highlights the photosynthetic advantages of Lost and suggests avenues for enhancing tomato productivity through trait transfer.