Paralogous Radiations of PIN Proteins with Multiple Origins of Noncanonical PIN Structure

Abstract

The plant hormone auxin is a conserved regulator of development which has been implicated in the generation of morphological novelty. PIN-FORMED1 (PIN) auxin efflux carriers are central to auxin function by regulating its distribution. PIN family members have divergent structures and cellular localizations, but the origin and evolutionary significance of this variation is unresolved. To characterize PIN family evolution, we have undertaken phylogenetic and structural analyses with a massive increase in taxon sampling over previous studies. Our phylogeny shows that following the divergence of the bryophyte and lycophyte lineages, two deep duplication events gave rise to three distinct lineages of PIN proteins in euphyllophytes. Subsequent independent radiations within each of these lineages were taxonomically asymmetric, giving rise to at least 21 clades of PIN proteins, of which 15 are revealed here for the first time. Although most PIN protein clades share a conserved canonical structure with a modular central loop domain, a small number of noncanonical clades dispersed across the phylogeny have highly divergent protein structure. We propose that PIN proteins underwent sub- and neofunctionalization with substantial modification to protein structure throughout plant evolution. Our results have important implications for plant evolution as they suggest that structurally divergent PIN proteins that arose in paralogous radiations contributed to the convergent evolution of organ systems in different land plant lineages.

Algal ancestor of land plants was preadapted for symbiosis

“…It must be noted that, until multiple additional genomes from charophyte and chlorophyte species have been sequenced, the presence of genes not detected in transcriptomes cannot be ruled out. However, when a similar dataset for liverworts and other bryophytes with an even lower coverage of the species space was used, all the symbiotic genes were recovered, in line with results obtained in the study of other processes (44)(45)(46) and lending support to our conclusions.…”

Directional Auxin Transport Mechanisms in Early Diverging Land Plants

“…Also, if a canonical or long PIN protein was present in the last common ancestor of land plants [13], our data would suggest that PM-localized PIN proteins predate the origin of land plants.…”

“…Similar to that of the angiosperm Arabidopsis, the P. patens genome encodes two different types of PIN proteins, characterized by either a short or a long hydrophylic loop between the transmembrane regions ( Figure 1A), the latter designated as the canonical PIN protein [12,13]. We assessed the auxin transport capabilities of these different PIN proteins by several means.…”

Auxin Produced by the Indole-3-Pyruvic Acid Pathway Regulates Development and Gemmae Dormancy in the Liverwort Marchantia polymorpha

“…This transport was later supported by the findings of Gaal et al (1982) and Maravolo (1976), who showed that 14 C-IAA is transported in an apical-basal and dorsal-ventral manner in the M. polymorpha thallus. Considering M. polymorpha has at least four PIN-FORMED (PIN) genes (Bennett et al, 2014a), these findings suggest PIN-mediated polar auxin transport is an important mechanism for gametophytic M. polymorpha development, as recently shown in the moss P. patens (Bennett et al, 2014b;Viaene et al, 2014). Our IAA measurements of different thallus tissues suggested IAA levels correlate well with pro YUC2:GUS expression but less well with pro TAA: GUS, as Mp-TAA is highly expressed only in the meristematic region and the base of gemma cups, with much weaker signal in the midrib and no signal in thallus margins.…”