Arabidopsis Lost Its Sister: Why Brachypodium Is a Better Model to Study PIN-Mediated Auxin Transport in the Shoot

How well do model systems represent larger groups? In the Arabidopsis shoot the auxin-transport protein PIN-FORMED1 (AtPIN1) positions incipient organ primordia by concentrating auxin into local maxima in the meristem epidermis. From these maxima, AtPIN1 also transports auxin into internal tissues along emergent paths that pattern vasculature. Using phylogenetic and synteny analyses we identified a PIN clade sister to AtPIN1, here termed Sister-of-PIN1 (SoPIN1), which is present in all sampled angiosperms but lost from Brassicaceae, including Arabidopsis. In the grass Brachypodium, SoPIN1 is highly expressed in the epidermis and consistently polarized toward maxima of the DR5 auxin-signaling reporter, which suggests SoPIN1 functions to localize new primordia. In contrast, the duplicate PIN1a and PIN1b proteins are highly expressed in internal tissues, and polarize away from epidermal DR5 maxima, suggesting a role in vascular patterning. We created a computer model of PIN dynamics that supports the hypothesis that SoPIN1 polarizes up the auxin gradient, while PIN1a/b polarize with the auxin flux. Thus in most angiosperms outside of Brassicaceae multiple PIN family members with different polarization modes may act to mediate organ initiation and vein patterning. Remarkably, heterologous expression of the Brachypodium PINs in Arabidopsis suggests that the polarization mechanisms that act in concert on AtPIN1 may differentially target the Brachypodium SoPIN1 and PIN1a/b proteins, providing evidence that an underlying separation of polarization mechanisms may still exist in Arabidopsis even though the PIN gene family structure common in most other angiosperms does not.