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

Journal Article · · Molecular Biology and Evolution
 [1];  [2];  [3];  [4];  [5];  [6];  [6];  [7];  [8];  [9];  [2];  [2]
  1. Univ. of Cambridge (United Kingdom). Dept. of Plant Sciences; Univ. of Cambridge (United Kingdom). Sainsbury Lab.; DOE/OSTI
  2. Univ. of Cambridge (United Kingdom). Dept. of Plant Sciences
  3. Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Zoology
  4. Univ. of British Columbia, Vancouver, BC (Canada). Botanical Garden
  5. The New York Botanical Garden, Bronx, NY (United States). Molecular Systematics
  6. Donald Danforth Plant Science Center, St. Louis, MO (United States)
  7. Royal Botanic Gardens Edinburgh, Scotland (United Kingdom)
  8. Univ. of Alberta, Edmonton, AB (Canada). Dept. of Medicine; Univ. of Alberta, Edmonton, AB (Canada). Dept. of Biological Sciences; BGI-Shenzhen, Beishan Industrial Zone, Yantian District, Shenzhen (China)
  9. Univ. of Cambridge (United Kingdom). Sainsbury Lab.

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.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1625399
Journal Information:
Molecular Biology and Evolution, Journal Name: Molecular Biology and Evolution Journal Issue: 8 Vol. 31; ISSN 0737-4038
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United States
Language:
English

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Cited By (25)

Evolution and roles of cytokinin genes in angiosperms 1: Do ancient IPTs play housekeeping while non-ancient IPTs play regulatory roles? journal March 2020
Evolution of fast root gravitropism in seed plants journal August 2019
Algal ancestor of land plants was preadapted for symbiosis journal October 2015
Evolution and ecology of plant architecture: integrating insights from the fossil record, extant morphology, developmental genetics and phylogenies journal November 2017
Functionally different PIN proteins control auxin flux during bulbil development in Agave tequilana
  • Abraham Juárez, María Jazmín; Hernández Cárdenas, Rocío; Santoyo Villa, José Natzul
  • Journal of Experimental Botany, Vol. 66, Issue 13 https://doi.org/10.1093/jxb/erv191
journal April 2015
Auxin-mediated developmental control in the moss Physcomitrella patens journal August 2017
The evolution of root branching: increasing the level of plasticity journal November 2018
The early evolution of land plants, from fossils to genomics: a commentary on Lang (1937) ‘On the plant-remains from the Downtonian of England and Wales' journal April 2015
Development and genetics in the evolution of land plant body plans journal February 2017
Reassessing the evolution of strigolactone synthesis and signalling posted_content January 2017
Evolution of the YABBY gene family in seed plants journal January 2016
PIN6 auxin transporter at endoplasmic reticulum and plasma membrane mediates auxin homeostasis and organogenesis in Arabidopsis journal May 2016
Auxin guides roots to avoid obstacles during gravitropic growth journal October 2019
Analysis of Nicotiana tabacum PIN genes identifies NtPIN4 as a key regulator of axillary bud growth journal March 2017
Transcription of specific auxin efflux and influx carriers drives auxin homeostasis in tobacco cells journal August 2019
Strigolactone synthesis is ancestral in land plants, but canonical strigolactone signalling is a flowering plant innovation journal September 2019
PIN-FORMED and PIN-LIKES auxin transport facilitators journal August 2019
Connective Auxin Transport in the Shoot Facilitates Communication between Shoot Apices journal April 2016
The bHLH transcription factor SPATULA enables cytokinin signaling, and both activate auxin biosynthesis and transport genes at the medial domain of the gynoecium journal April 2017
Identification and Validation of Reference Genes for Transcript Normalization in Strawberry (Fragaria × ananassa) Defense Responses journal August 2013
A comprehensive phylogeny of auxin homeostasis genes involved in adventitious root formation in carnation stem cuttings journal April 2018
Evolutionary Conserved Cysteines Function as cis-Acting Regulators of Arabidopsis PIN-FORMED 2 Distribution journal October 2017
The PIN-FORMED Auxin Efflux Carriers in Plants journal September 2018
Advances in Understanding the Mechanism of Action of the Auxin Permease AUX1 journal October 2018
Comparative Analysis of the PIN Auxin Transporter Gene Family in Different Plant Species: A Focus on Structural and Expression Profiling of PINs in Solanum tuberosum journal July 2019

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