A Division in PIN-Mediated Auxin Patterning during Organ Initiation in Grasses

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.

Genome-Wide Study ofKNOXRegulatory Network Reveals Brassinosteroid Catabolic Genes Important for Shoot Meristem Function in Rice

“…The auxin pathway is also regulated by KNOX proteins (Bolduc et al, 2012). Auxin triggers initiation of lateral primordia and accumulates distally in developing leaves (Reinhardt et al, 2003;O'Connor et al, 2014).…”

Diversity of phyllotaxis in land plants in reference to the shoot apical meristem structure

“…Furthermore, in light of the fact that similar developmental impairments have been shown in some monocots [113][114][115][116][117] and that homologs of PIN genes have been identified in gymnosperms [118,119], it is generally thought that the auxin mechanism of phyllotaxis regulation may be universal throughout the seed plants. Sequencing analyses have suggested that PIN genes may be present in the seedless land plants as well [119], and PAT has been shown to be present in Physcomitrella [120] and Selaginella [121], indicating that the auxin mechanism of phyllotaxis formation may be common to all land-plant lineages.…”

Leaf development and morphogenesis

“…Distinct regulators of PIN1 localization were shown to be involved in these different phases -whereas the localization towards the convergence point is regulated in part by the serine/threonine kinase PINOID (Friml et al, 2004), which phosphorylates PIN1 (Huang et al, 2010), the switch to basal polarization is regulated by the MAB4 gene family (Cheng et al, 2008;Furutani et al, 2014). In angiosperm species other than the Brassicaceae, leaf initiation and vascular formation were suggested to be regulated by distinct members of the PIN family (O'Connor et al, 2014).…”