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

Journal Article · · Frontiers in Plant Science
 [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

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.

Research Organization:
Univ. of Georgia, Athens, GA (United States). Warnell School of Forestry and Natural Resources
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
SC0005140
OSTI ID:
1457460
Journal Information:
Frontiers in Plant Science, Vol. 5; ISSN 1664-462X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 35 works
Citation information provided by
Web of Science

References (84)

Pattern formation in the vascular system of monocot and dicot plant species: Tansley review journal September 2004
AtSUC3, a gene encoding a new Arabidopsis sucrose transporter, is expressed in cells adjacent to the vascular tissue and in a carpel cell layer journal December 2000
SolexaQA: At-a-glance quality assessment of Illumina second-generation sequencing data journal September 2010
Arabidopsis SUC1 loads the phloem in suc2 mutants when expressed from the SUC2 promoter journal October 2011
Sucrose transporter1 functions in phloem loading in maize leaves journal January 2009
Impaired Function of the Tonoplast-Localized Sucrose Transporter in Rice, OsSUT2 , Limits the Transport of Vacuolar Reserve Sucrose and Affects Plant Growth journal July 2011
Transport Mechanisms for Organic Forms of Carbon and Nitrogen Between Source and sink journal June 2004
The Medicago truncatula Sucrose Transporter Family: Characterization and Implication of Key Members in Carbon Partitioning towards Arbuscular Mycorrhizal Fungi journal November 2012
Sucrose Transport in Higher Plants: From Source to Sink book August 2011
Long branch attraction, taxon sampling, and the earliest angiosperms: Amborella or monocots? journal January 2004
Functional Characterization of the Arabidopsis AtSUC2 Sucrose/H + Symporter by Tissue-Specific Complementation Reveals an Essential Role in Phloem Loading But Not in Long-Distance Transport journal July 2008
The Sucrose Transporter Gene Family in Rice journal March 2003
Penetration of the Stigma and Style Elicits a Novel Transcriptome in Pollen Tubes, Pointing to Genes Critical for Growth in a Pistil journal August 2009
Bayes Empirical Bayes Inference of Amino Acid Sites Under Positive Selection journal January 2005
Transcript profiling reveals expression differences in wild-type and glabrous soybean lines journal January 2011
The Amborella Genome and the Evolution of Flowering Plants journal December 2013
Membrane-Transport Systems for Sucrose in Relation to Whole-Plant Carbon Partitioning journal May 2011
Identification of a pollen‐specific sucrose transporter‐like proteinNtSUT3 from tobacco journal July 1999
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks journal March 2012
Phloem Loading by the PmSUC2 Sucrose Carrier from Plantago major Occurs into Companion Cells. journal October 1995
Photoperiodic regulation of the sucrose transporter StSUT4 affects the expression of circadian-regulated genes and ethylene production journal January 2013
The Mitochondrial Genome of Soybean Reveals Complex Genome Structures and Gene Evolution at Intercellular and Phylogenetic Levels journal February 2013
The banana (Musa acuminata) genome and the evolution of monocotyledonous plants journal July 2012
Phylogeny.fr: robust phylogenetic analysis for the non-specialist journal May 2008
Genome sequence of the palaeopolyploid soybean journal January 2010
Evolution, polymorphology and multifunctionality of the phloem system journal January 1999
Sucrose transporters of higher plants journal June 2010
Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters journal November 2000
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability journal January 2013
A Comparison of the Sucrose Transporter Systems of Different Plant Species journal May 2003
Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events journal March 2003
Angiosperm genome comparisons reveal early polyploidy in the monocot lineage journal December 2009
A dynamic gene expression atlas covering the entire life cycle of rice journal March 2010
RNA-Seq Analysis of a Soybean Near-Isogenic Line Carrying Bacterial Leaf Pustule-Resistant and -Susceptible Alleles journal October 2011
The Physcomitrella Genome Reveals Evolutionary Insights into the Conquest of Land by Plants journal December 2007
KaKs_Calculator: Calculating Ka and Ks Through Model Selection and Model Averaging journal January 2006
Rfam 11.0: 10 years of RNA families journal November 2012
Understanding and manipulating sucrose phloem loading, unloading, metabolism, and signalling to enhance crop yield and food security journal December 2013
affy--analysis of Affymetrix GeneChip data at the probe level journal February 2004
Aquilegia : A New Model for Plant Development, Ecology, and Evolution journal June 2009
SUT Sucrose and MST Monosaccharide Transporter Inventory of the Selaginella Genome journal January 2012
Complete Chloroplast Genome Sequence of Glycine max and Comparative Analyses with other Legume Genomes journal September 2005
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools journal November 2012
Evolution of plant sucrose uptake transporters journal January 2012
Antisense suppression of the rice transporter gene, OsSUT1, leads to impaired grain filling and germination but does not affect photosynthesis journal January 2002
A suite of sucrose transporters expressed in coats of developing legume seeds includes novel pH-independent facilitators: Novel sucrose transporters expressed in legume seed coats journal January 2007
The role of the sucrose transporter, OsSUT1, in germination and early seedling growth and development of rice plants journal December 2006
PLncDB: plant long non-coding RNA database journal March 2013
Vacuoles release sucrose via tonoplast-localised SUC4-type transporters: SUC4-type sucrose transporters in the tonoplast journal September 2011
Potato sucrose transporter expression in minor veins indicates a role in phloem loading. journal November 1993
MACSE: Multiple Alignment of Coding SEquences Accounting for Frameshifts and Stop Codons journal September 2011
The sucrose transporter family in Populus: the importance of a tonoplast PtaSUT4 to biomass and carbon partitioning: Tonoplast-localized sucrose transporter in Populus journal January 2011
Creating the CIPRES Science Gateway for inference of large phylogenetic trees conference November 2010
Genetic Control of Carbon Partitioning in Grasses: Roles of Sucrose Transporters and Tie-dyed Loci in Phloem Loading journal January 2009
UniVIO: A Multiple Omics Database with Hormonome and Transcriptome Data from Rice journal January 2013
Molecular physiology of higher plant sucrose transporters journal March 2007
JrSUT1, a putative xylem sucrose transporter, could mediate sucrose influx into xylem parenchyma cells and be up-regulated by freeze-thaw cycles over the autumn-winter period in walnut tree (Juglans regia L.) journal January 2006
MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods journal May 2011
PmSUC3: Characterization of a SUT2/SUC3-Type Sucrose Transporter from Plantago major journal May 2003
AtSUC8 and AtSUC9 encode functional sucrose transporters, but the closely related AtSUC6 and AtSUC7 genes encode aberrant proteins in different Arabidopsis ecotypes: AtSUC genes and pseudogenes journal August 2004
The Tonoplast-Localized Sucrose Transporter in Populus (PtaSUT4) Regulates Whole-Plant Water Relations, Responses to Water Stress, and Photosynthesis journal August 2012
Evolution of development of vascular cambia and secondary growth: Tansley review journal April 2010
SUT2, a Putative Sucrose Sensor in Sieve Elements journal July 2000
MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space journal February 2012
Evaluation of an Improved Branch-Site Likelihood Method for Detecting Positive Selection at the Molecular Level journal August 2005
MicroRNA profiles and their control of male gametophyte development in rice journal March 2012
Involvement of the sucrose transporter, OsSUT1, in the long-distance pathway for assimilate transport in rice journal July 2007
De novo genome sequencing and comparative genomics of date palm (Phoenix dactylifera) journal May 2011
A sucrose transporter, LjSUT4, is up-regulated during Lotus japonicus nodule development journal May 2003
Phylogeny estimation: traditional and Bayesian approaches journal April 2003
A gene expression map of Arabidopsis thaliana development journal April 2005
Evolution of developmental mechanisms in plants journal August 2008
PAML 4: Phylogenetic Analysis by Maximum Likelihood journal April 2007
Rice Expression Atlas In Reproductive Development journal November 2010
Wounding Enhances Expression of AtSUC3, a Sucrose Transporter from Arabidopsis Sieve Elements and Sink Tissues journal January 2004
PGDD: a database of gene and genome duplication in plants journal November 2012
The promoter of the Arabidopsis thaliana SUC2 sucrose-H+ symporter gene directs expression of ?-glucuronidase to the phloem: Evidence for phloem loading and unloading by SUC2 journal June 1995
Genome-wide identification, structural analysis and expression profiles of GRAS gene family in orchardgrass journal February 2020
Analysis of Microarray Data Using Z Score Transformation journal May 2003
The CLASSY family controls tissue-specific DNA methylation patterns in Arabidopsis journal January 2022
Full-length transcriptome analysis of multiple organs and identification of adaptive genes and pathways in Mikania micrantha journal February 2022
The AtSUC1 sucrose carrier may represent the osmotic driving force for anther dehiscence and pollen tube growth in Arabidopsis journal August 1999
Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways journal January 2006
SUT2, a Putative Sucrose Sensor in Sieve Elements journal July 2000

Cited By (11)

Expression patterns of Brassica napus genes implicate IPT, CKX , sucrose transporter, cell wall invertase, and amino acid permease gene family members in leaf, flower, silique, and seed development journal April 2015
Sucrose transporter2 contributes to maize growth, development, and crop yield: ZmSUT2 contributes to plant growth and yield journal April 2017
Genome-wide identification, phylogeny, and expression profile of the sucrose transporter multigene family in tobacco journal June 2019
A novel sucrose transporter gene IbSUT4 involves in plant growth and response to abiotic stress through the ABF-dependent ABA signaling pathway in Sweetpotato journal April 2020
Genome-Wide Analysis and Expression Profiling of the SUC and SWEET Gene Families of Sucrose Transporters in Oilseed Rape (Brassica napus L.) journal September 2016
Protoplast-Esculin Assay as a New Method to Assay Plant Sucrose Transporters: Characterization of AtSUC6 and AtSUC7 Sucrose Uptake Activity in Arabidopsis Col-0 Ecotype journal April 2018
Drought response transcriptomes are altered in poplar with reduced tonoplast sucrose transporter expression journal September 2016
Evolution of the Apicomplexan Sugar Transporter Gene Family Repertoire journal January 2017
Genome-wide identification of MST, SUT and SWEET family sugar transporters in root parasitic angiosperms and analysis of their expression during host parasitism journal May 2019
Differential Signaling and Sugar Exchanges in Response to Avirulent Pathogen- and Symbiont-Derived Molecules in Tobacco Cells journal November 2017
Cytokinins and Expression of SWEET, SUT, CWINV and AAP Genes Increase as Pea Seeds Germinate journal December 2016

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