Auxin-driven ecophysiological diversification of leaves in domesticated tomato

Abstract

SummaryThe study of crop diversification has focussed mainly on the genetic changes underlying traits favoured by humans. However, the passage from natural habitats to agronomic settings probably operated changes beyond those comprising the classical domestication syndrome. A deeper understanding of these traits and their genetic signature would be valuable to inform conventional crop breeding and de novo domestication of crop wild relatives. Heterobaric leaves have bundle sheath extensions (BSEs) that compartmentalise the sub-stomatal cavity whereas homobaric leaves do not; BSE development is known to be controlled by the OBSCURAVENOSA (OBV) locus and the obv mutant lacks BSEs whereas leaves carrying the wild type allele have BSEs. Here we identify the OBV gene and the causative mutation, a non-synonymous amino acid change. This mutation exists as a rare balanced polymorphism in the natural range of wild tomatoes, but has increased in frequency in domesticated tomatoes suggesting that the latter diversified into heterobaric and homobaric leaf types. The mutation disrupts a C2H2 zinc finger motif in the OBV protein, resulting in the absence of BSEs in leaves and here we show that this and other pleiotropic effects, including changes in leaf insertion angle, leaf margin serration, minor vein density and fruit shape, are controlled by OBV via changes in auxin signalling. Loss of function of the transcriptional regulator AUXIN RESPONSE FACTOR (ARF4) also results in defective BSE development, revealing an additional component of a novel genetic module controlling aspects of leaf development important for ecological adaptation and subject to breeding selections.One sentence summaryDistribution of heterobaric and homobaric leaves is controlled by natural variation in an auxin-related transcription factor