A sister of PIN1 gene in tomato (Solanum lycopersicum) defines leaf and flower organ initiation patterns by maintaining epidermal auxin flux

Ciera C Martinez,Daniel Koenig,Daniel H Chitwood,Neelima R Sinha

doi:10.1016/j.ydbio.2016.08.011

Abstract

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 S.lycopersicum.

Highlights

In plants, cell fate and subsequent tissue formation are mainly determined by positional information rather than cell lineage
Previous phylogenetic analysis places both SlSoPIN1a and SlSoPIN1b genes together on a single branch tip, suggesting a recent Sister of PIN1 clade” (SoPIN1) gene duplication event in the branch leading to S. lycopersicum [36,37]
These reports suggested that a duplication event in the SoPIN1 clade in S. lycopersicum occurred roughly sometime after the divergence between S

Summary

Introduction

Cell fate and subsequent tissue formation are mainly determined by positional information rather than cell lineage. The plant hormone auxin acts as a positional cue for proper patterning in many developmental processes, including embryogenesis [1,2], leaf and leaflet initiation [2,3,4,5,6], vascular patterning [5,7,8,9], root organogenesis [10] and flower initiation [3,11,12]. The multifaceted role of auxin necessitates a coordinated regulation of auxin influx and efflux carriers which guide auxin transport in a polar fashion, and make up the Polar Auxin Transport (PAT) network. Unlike other known plant hormones, auxin is actively transported in a directional fashion, allowing the creation of spatio-temporally regulated auxin concentrations. The largest contributors of directional transport in the PAT system are the PIN-

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Conclusion