Auxin-driven ecophysiological diversification of leaves in domesticated tomato

Abstract

Heterobaric leaves have bundle sheath extensions (BSEs) that compartmentalize the sub-stomatal cavity, whereas homobaric leaves do not. In tomato (Solanum lycopersicum), BSE development is controlled by the OBSCURAVENOSA (OBV) locus. 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 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 alterations to leaf function: Photosynthetic assimilation rate and leaf hydraulic conductance are both reduced in obv. Here, we show that both of these 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 4 (ARF4) also results in defective BSE development, revealing an additional component of a genetic module controlling aspects of leaf development important for ecological adaptation and for breeding selection.

Functional characterization of plant specific Indeterminate Domain (IDD) transcription factors in tomato (Solanum lycopersicum L.)

“…SlIDD5 mutants failed to produce bundle sheath extension cells (homobaric leaves) 78 . Increased chlorophyll content has been observed in obv mutants, such as M82 and CRISPR/ Cas9 mutants of Micro-Tom, where the absence of BSE allowed chloroplast development in leaf veins and reduced water conductivity 79,80 . Moreover, OBV also regulates the leaf insertion angle, leaf margin serration, and fruit shape, and has been shown to work together with auxin signaling 80 .…”