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Title: Bayesian phylogeny of sucrose transporters: ancient origins, differential expansion and convergent evolution in monocots and dicots

Sucrose transporters (SUTs) are essential for the export and efficient movement of sucrose from source leaves to sink organs in plants. The angiosperm SUT family was previously classified into three or four distinct groups, Types I, II (subgroup IIB), and III, with dicot-specific Type I and monocot-specific Type IIB functioning in phloem loading. To shed light on the underlying drivers of SUT evolution, Bayesian phylogenetic inference was undertaken using 41 sequenced plant genomes, including seven basal lineages at key evolutionary junctures. Our analysis supports four phylogenetically and structurally distinct SUT subfamilies, originating from two ancient groups (AG1 and AG2) that diverged early during terrestrial colonization. In both AG1 and AG2, multiple intron acquisition events in the progenitor vascular plant established the gene structures of modern SUTs. Tonoplastic Type III and plasmalemmal Type II represent evolutionarily conserved descendants of AG1 and AG2, respectively. Type I and Type IIB were previously thought to evolve after the dicot-monocot split. We show, however, that divergence of Type I from Type III SUT predated basal angiosperms, likely associated with evolution of vascular cambium and phloem transport. Type I SUT was subsequently lost in monocots along with vascular cambium, and independent evolution of Type IIB coincidedmore » with modified monocot vasculature. Both Type I and Type IIB underwent lineage-specific expansion. In multiple unrelated taxa, the newly-derived SUTs exhibit biased expression in reproductive tissues, suggesting a functional link between phloem loading and reproductive fitness. Convergent evolution of Type land Type IIB for SUT function in phloem loading and reproductive organs supports the idea that differential vascular development in dicots and monocots is a strong driver for SUT family evolution in angiosperms.« less
Authors:
 [1] ;  [1] ;  [2] ;  [3] ;  [2]
  1. Univ. of Georgia, Athens, GA (United States). Institute of Bioinformatics
  2. Univ. of Georgia, Athens, GA (United States). Institute of Bioinformatics, Warnell School of Forestry and Natural Resources, and Department of Genetics
  3. Univ. of Georgia, Athens, GA (United States). Institute of Bioinformatics and Department of Plant Biology
Publication Date:
Grant/Contract Number:
SC0005140
Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 5; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Research Org:
Univ. of Georgia, Athens, GA (United States). Warnell School of Forestry and Natural Resources
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; transporters; phloem; vascular evolution; angiosperms; molecular evolution; expression partitioning
OSTI Identifier:
1457460

Peng, Duo, Gu, Xi, Xue, Liang-Jiao, Leebens-Mack, James H., and Tsai, Chung-Jui. Bayesian phylogeny of sucrose transporters: ancient origins, differential expansion and convergent evolution in monocots and dicots. United States: N. p., Web. doi:10.3389/fpls.2014.00615.
Peng, Duo, Gu, Xi, Xue, Liang-Jiao, Leebens-Mack, James H., & Tsai, Chung-Jui. Bayesian phylogeny of sucrose transporters: ancient origins, differential expansion and convergent evolution in monocots and dicots. United States. doi:10.3389/fpls.2014.00615.
Peng, Duo, Gu, Xi, Xue, Liang-Jiao, Leebens-Mack, James H., and Tsai, Chung-Jui. 2014. "Bayesian phylogeny of sucrose transporters: ancient origins, differential expansion and convergent evolution in monocots and dicots". United States. doi:10.3389/fpls.2014.00615. https://www.osti.gov/servlets/purl/1457460.
@article{osti_1457460,
title = {Bayesian phylogeny of sucrose transporters: ancient origins, differential expansion and convergent evolution in monocots and dicots},
author = {Peng, Duo and Gu, Xi and Xue, Liang-Jiao and Leebens-Mack, James H. and Tsai, Chung-Jui},
abstractNote = {Sucrose transporters (SUTs) are essential for the export and efficient movement of sucrose from source leaves to sink organs in plants. The angiosperm SUT family was previously classified into three or four distinct groups, Types I, II (subgroup IIB), and III, with dicot-specific Type I and monocot-specific Type IIB functioning in phloem loading. To shed light on the underlying drivers of SUT evolution, Bayesian phylogenetic inference was undertaken using 41 sequenced plant genomes, including seven basal lineages at key evolutionary junctures. Our analysis supports four phylogenetically and structurally distinct SUT subfamilies, originating from two ancient groups (AG1 and AG2) that diverged early during terrestrial colonization. In both AG1 and AG2, multiple intron acquisition events in the progenitor vascular plant established the gene structures of modern SUTs. Tonoplastic Type III and plasmalemmal Type II represent evolutionarily conserved descendants of AG1 and AG2, respectively. Type I and Type IIB were previously thought to evolve after the dicot-monocot split. We show, however, that divergence of Type I from Type III SUT predated basal angiosperms, likely associated with evolution of vascular cambium and phloem transport. Type I SUT was subsequently lost in monocots along with vascular cambium, and independent evolution of Type IIB coincided with modified monocot vasculature. Both Type I and Type IIB underwent lineage-specific expansion. In multiple unrelated taxa, the newly-derived SUTs exhibit biased expression in reproductive tissues, suggesting a functional link between phloem loading and reproductive fitness. Convergent evolution of Type land Type IIB for SUT function in phloem loading and reproductive organs supports the idea that differential vascular development in dicots and monocots is a strong driver for SUT family evolution in angiosperms.},
doi = {10.3389/fpls.2014.00615},
journal = {Frontiers in Plant Science},
number = ,
volume = 5,
place = {United States},
year = {2014},
month = {11}
}