Paralogous radiations of PIN proteins with multiple origins of noncanonical PIN structure.
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.
Department of Plant Sciences, University of Cambridge, Cambridge, United KingdomSainsbury Laboratory, University of Cambridge, Cambridge, United Kingdom.
Tom
T
Bennett
Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom.
Samuel F
SF
Brockington
Department of Zoology, University of British Columbia, Vancouver, British Colombia, Canada.
Carl
C
Rothfels
UBC Botanical Garden Campbell Building, Vancouver, British Colombia, Canada.
Sean W
SW
Graham
Molecular Systematics, The New York Botanical Garden, Bronx, NY.
Dennis
D
Stevenson
Danforth Center, St. Louis, MO.
Toni
T
Kutchan
Danforth Center, St. Louis, MO.
Megan
M
Rolf
Royal Botanic Gardens Edinburgh, 20A Inverleith Row, Edinburgh, United Kingdom.
Philip
P
Thomas
Department of Medicine, University of Alberta, Edmonton, Alberta, CanadaDepartment of Biological Sciences, University of Alberta, Edmonton, Alberta, CanadaBGI-Shenzhen, Beishan Industrial Zone, Yantian District, Shenzhen, China.
Gane Ka-Shu
GK
Wong
Sainsbury Laboratory, University of Cambridge, Cambridge, United Kingdom.
Ottoline
O
Leyser
Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom.
Beverley J
BJ
Glover
Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom cjh97@cam.ac.uk.
C Jill
CJ
Harrison
D000595:Amino Acid Sequence; D017124:Conserved Sequence; D019143:Evolution, Molecular; D020440:Gene Duplication; D007210:Indoleacetic Acids / Q000378:metabolism*; D008958:Models, Molecular; D005810:Multigene Family; D010802:Phylogeny; D010940:Plant Proteins / Q000737:chemistry* / Q000235:genetics*; D010944:Plants / Q000145:classification* / Q000235:genetics*
D007210:Indoleacetic Acids; D010940:Plant Proteins
PIN protein; auxin; auxin transport; phylogeny; plant evolution; protein structure