A Sister of PIN1 gene in tomato (Solanum lycopersicum) defines organ initiation patterns by maintaining epidermal auxin flux
The spatiotemporal localization of the plant hormone auxin acts as a positional cue during early leaf and flower organogenesis. One of the main contributors to auxin localization is the auxin efflux carrier PIN-FORMED1 (PIN1). Phylogenetic analysis has revealed that PIN1 genes are split into two sister clades; PIN1 and the relatively uncharacterized Sister-Of-PIN1 (SoPIN1). In this paper we identify entire-2 as a loss-of-function SlSoPIN1a (Solyc10g078370) mutant in Solanum lycopersicum. The entire-2 plants are unable to specify proper leaf initiation leading to a frequent switch from the wild type spiral phyllotactic pattern to distichous and decussate patterns. Leaves in entire-2 are large and less complex and the leaflets display spatial deformities in lamina expansion, vascular development, and margin specification. During sympodial growth in entire-2 the specification of organ position and identity is greatly affected resulting in variable branching patterns on the main sympodial and inflorescence axes. To understand how SlSoPIN1a functions in establishing proper auxin maxima we used the auxin signaling reporter DR5::Venus to visualize differences in auxin localization between entire-2 and wild type. DR5::Venus visualization shows a widening of auxin localization which spreads to subepidermal tissue layers during early leaf and flower organogenesis, showing that SoPIN1 functions to focus auxin signaling to the epidermal layer. The striking spatial deformities observed in entire-2 help provide a mechanistic framework for explaining the function of the SoPIN1 clade in angiosperm species.\n\nAuthor SummaryThe plant hormone auxin acts as a positional signal in most plant developmental processes. The PIN-FORMED family of auxin transporters are the main contributors to auxin localization, especially PIN-FORMED1, which has been studied extensively in plant model species Arabidopsis thaliana. Members of the PIN-FORMED gene family have been found in all plant species, but there is a scarcity of mutants described outside Arabidopsis thaliana. Using Solanum lycopersicum (tomato) as a system, this study identifies a loss of function mutant from the Sister-Of-PIN1 clade in the SlSoPIN1a gene. The characterization of this mutant reveals the role of SlSoPIN1a in establishing position of organ initiation during shoot and reproductive development, including a role in establishing proper spiral phyllotaxy. We use an auxin visualization technique to conclude SlSoPIN1a functions in specifying auxin presence in proper cell layers to establish organ and tissue positioning. This work gives further evolutionary context to how PIN-FORMED genes act to establish organogenesis in the plant kingdom.