Abstract
The hormone auxin plays a crucial role in plant morphogenesis. In the shoot apical meristem, the PIN-FORMED1 (PIN1) efflux carrier concentrates auxin into local maxima in the epidermis, which position incipient leaf or floral primordia. From these maxima, PIN1 transports auxin into internal tissues along emergent paths that pattern leaf and stem vasculature. In Arabidopsis thaliana, these functions are attributed to a single PIN1 protein. Using phylogenetic and gene synteny analysis we identified an angiosperm PIN clade sister to PIN1, here termed Sister-of-PIN1 (SoPIN1), which is present in all sampled angiosperms except for Brassicaceae, including Arabidopsis. Additionally, we identified a conserved duplication of PIN1 in the grasses: PIN1a and PIN1b. In Brachypodium distachyon, SoPIN1 is highly expressed in the epidermis and is consistently polarized toward regions of high expression of the DR5 auxin-signaling reporter, which suggests that SoPIN1 functions in the localization of new primordia. In contrast, PIN1a and PIN1b are highly expressed in internal tissues, suggesting a role in vascular patterning. PIN1b is expressed in broad regions spanning the space between new primordia and previously formed vasculature, suggesting a role in connecting new organs to auxin sinks in the older tissues. Within these regions, PIN1a forms narrow canals that likely pattern future veins. Using a computer model, we reproduced the observed spatio-temporal expression and localization patterns of these proteins by assuming that SoPIN1 is polarized up the auxin gradient, and PIN1a and PIN1b are polarized to different degrees with the auxin flux. Our results suggest that examination and modeling of PIN dynamics in plants outside of Brassicaceae will offer insights into auxin-driven patterning obscured by the loss of the SoPIN1 clade in Brassicaceae.
Highlights
Active transport of the plant hormone auxin provides key positional and environmental cues during plant development [1,2]
Computational models and functional studies using the plant Arabidopsis thaliana have led to competing models for how the PIN-FORMED1 (PIN1) auxin transporter polarizes in the cell to create both the maxima required for organ initiation and the narrow streams required for vein patterning
We identify a previously uncharacterized PIN protein most closely related to PIN1 that is present in all flowering plants but lost in the Brassicaceae, including Arabidopsis
Summary
Active transport of the plant hormone auxin provides key positional and environmental cues during plant development [1,2]. The angiosperm PIN family can be divided into ‘‘short’’ and ‘‘long’’ classes based on the length of the hydrophilic region [6,7]. Short PIN proteins are likely involved in auxin homoeostasis within the cell [8]. Long PINs show a characteristic polar localization in the cell plasma membrane that provides directionality to auxin transport [9,10,11,12,13]. The hydrophilic loop domains of long PIN proteins contain phosphorylation sites that control PIN cellular localization [14,15,16]. It is likely that variation in function between PIN family members is at least in part due to differing protein domains within this region
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