Genome-Wide Analysis and Expression Profiling of the SUC and SWEET Gene Families of Sucrose Transporters in Oilseed Rape (Brassica napus L.)

Sucrose is the principal transported product of photosynthesis from source leaves to sink organs. SUTs/SUCs (sucrose transporters or sucrose carriers) and SWEETs (Sugars Will Eventually be Exported Transporters) play significant central roles in phloem loading and unloading. SUTs/SUCs and SWEETs are key players in sucrose translocation and are associated with crop yields. The SUT/SUC and SWEET genes have been characterized in several plant species, but a comprehensive analysis of these two gene families in oilseed rape has not yet been reported. In our study, 22 and 68 members of the SUT/SUCs and SWEET gene families, respectively, were identified in the oilseed rape (Brassica napus) genome through homology searches. An analysis of the chromosomal distribution, phylogenetic relationships, gene structures, motifs and the cis-acting regulatory elements in the promoters of BnSUC and BnSWEET genes were analyzed. Furthermore, we examined the expression of the 18 BnSUC and 16 BnSWEET genes in different tissues of “ZS11” and the expression of 9 BnSUC and 7 BnSWEET genes in “ZS11” under various conditions, including biotic stress (Sclerotinia sclerotiorum), abiotic stresses (drought, salt and heat), and hormone treatments (abscisic acid, auxin, cytokinin, brassinolide, gibberellin, and salicylic acid). In conclusion, our study provides the first comprehensive analysis of the oilseed rape SUC and SWEET gene families. Information regarding the phylogenetic relationships, gene structure and expression profiles of the SUC and SWEET genes in the different tissues of oilseed rape helps to identify candidates with potential roles in specific developmental processes. Our study advances our understanding of the important roles of sucrose transport in oilseed rape.

[1]  C. A. Thomas,et al.  Molecular cloning. , 1977, Advances in pathobiology.

[2]  Corinne Da Silva,et al.  Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome , 2014, Science.

[3]  Kaining Hu,et al.  Unravelling the complex trait of harvest index in rapeseed (Brassica napus L.) with association mapping , 2015, BMC Genomics.

[4]  M. R. Thorpe,et al.  AtSUC2 has a role for sucrose retrieval along the phloem pathway: evidence from carbon-11 tracer studies. , 2012, Plant science : an international journal of experimental plant biology.

[5]  H. Kong,et al.  Divergence of duplicate genes in exon–intron structure , 2012, Proceedings of the National Academy of Sciences.

[6]  R. Hedrich,et al.  Vacuoles release sucrose via tonoplast-localised SUC4-type transporters. , 2012, Plant biology.

[7]  D. G. Brown,et al.  The origins of genomic duplications in Arabidopsis. , 2000, Science.

[8]  R. Hedrich,et al.  Proton-driven sucrose symport and antiport are provided by the vacuolar transporters SUC4 and TMT1/2. , 2011, The Plant journal : for cell and molecular biology.

[9]  Maoying Zhang,et al.  ZmLEA3, a multifunctional group 3 LEA protein from maize (Zea mays L.), is involved in biotic and abiotic stresses. , 2013, Plant & cell physiology.

[10]  D. Merdinoglu,et al.  The SWEET family of sugar transporters in grapevine: VvSWEET4 is involved in the interaction with Botrytis cinerea. , 2014, Journal of experimental botany.

[11]  W. Frommer,et al.  Sugar transporters for intercellular exchange and nutrition of pathogens , 2010, Nature.

[12]  A. Srivastava,et al.  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 Transport1[OA] , 2008, Plant Physiology.

[13]  J. Ward,et al.  Arabidopsis Sucrose Transporter AtSUC1 Is Important for Pollen Germination and Sucrose-Induced Anthocyanin Accumulation1[OA] , 2008, Plant Physiology.

[14]  Kathleen Marchal,et al.  PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences , 2002, Nucleic Acids Res..

[15]  Kirandeep K. Deol,et al.  Transcriptional coordination and abscisic acid mediated regulation of sucrose transport and sucrose-to-starch metabolism related genes during grain filling in wheat (Triticum aestivum L.). , 2015, Plant science : an international journal of experimental plant biology.

[16]  N. Sauer,et al.  Wounding Enhances Expression of AtSUC3, a Sucrose Transporter from Arabidopsis Sieve Elements and Sink Tissues1 , 2004, Plant Physiology.

[17]  R. Furbank,et al.  Expression and localisation analysis of the wheat sucrose transporter TaSUT1 in vegetative tissues , 2004, Planta.

[18]  Kun Lu,et al.  Genome-wide association analysis and differential expression analysis of resistance to Sclerotinia stem rot in Brassica napus. , 2016, Plant biotechnology journal.

[19]  M. Koch,et al.  Chromosome triplication found across the tribe Brassiceae. , 2005, Genome research.

[20]  Yihua Zhou,et al.  The sucrose transporter HbSUT3 plays an active role in sucrose loading to laticifer and rubber productivity in exploited trees of Hevea brasiliensis (para rubber tree). , 2010, Plant, cell & environment.

[21]  Yasuko Takahashi,et al.  Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events , 2022 .

[22]  F. Klebl,et al.  AtSUC8 and AtSUC9 encode functional sucrose transporters, but the closely related AtSUC6 and AtSUC7 genes encode aberrant proteins in different Arabidopsis ecotypes. , 2004, The Plant journal : for cell and molecular biology.

[23]  Daniel C. Ducat,et al.  Functional role of oligomerization for bacterial and plant SWEET sugar transporter family , 2013, Proceedings of the National Academy of Sciences.

[24]  W. Frommer,et al.  SUT2, a Putative Sucrose Sensor in Sieve Elements , 2000, Plant Cell.

[25]  W. Frommer,et al.  Evidence for an essential role of the sucrose transporter in phloem loading and assimilate partitioning. , 1994, The EMBO journal.

[26]  Chaozhi Ma,et al.  Molecular cloning and mRNA expression profile of sucrose transporter gene BnSUT1C from Brassica napus L. , 2013, Indian journal of experimental biology.

[27]  A. Schulz,et al.  Dimerization and endocytosis of the sucrose transporter StSUT1 in mature sieve elements , 2008, Plant Signalling & Behavior.

[28]  Koichiro Tamura,et al.  MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. , 2013, Molecular biology and evolution.

[29]  M. Deyholos,et al.  Identification and expression analysis of WRKY transcription factor genes in canola (Brassica napus L.) in response to fungal pathogens and hormone treatments , 2009, BMC Plant Biology.

[30]  R. Furbank,et al.  Three sucrose transporter genes are expressed in the developing grain of hexaploid wheat , 2002, Plant Molecular Biology.

[31]  Jinxiong Shen,et al.  Genetic analysis of rapeseed self‐incompatibility lines reveals significant heterosis of different patterns for yield and oil content traits , 2005 .

[32]  Xiaoling Dun,et al.  Neofunctionalization of Duplicated Tic40 Genes Caused a Gain-of-Function Variation Related to Male Fertility in Brassica oleracea Lineages1[W][OPEN] , 2014, Plant Physiology.

[33]  W. Frommer,et al.  Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9 , 2014, Nature.

[34]  Qian Gao,et al.  Comprehensive Analysis of NAC Domain Transcription Factor Gene Family in Populus trichocarpa , 2010, BMC Plant Biology.

[35]  A. Krapp,et al.  Overexpression of the Vacuolar Sugar Carrier AtSWEET16 Modifies Germination, Growth, and Stress Tolerance in Arabidopsis1[W] , 2013, Plant Physiology.

[36]  Yangkai Cai.  Sucrose Transporters in Higher Plants , 2006 .

[37]  R. Meeley,et al.  Sucrose transporter1 functions in phloem loading in maize leaves , 2009 .

[38]  N. Sauer,et al.  SUC1 and SUC2: two sucrose transporters from Arabidopsis thaliana; expression and characterization in baker's yeast and identification of the histidine-tagged protein. , 1994, The Plant journal : for cell and molecular biology.

[39]  F. Carrari,et al.  Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways. , 2006, The Plant journal : for cell and molecular biology.

[40]  Kun Lu,et al.  The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes , 2014, Nature Communications.

[41]  J. Leebens-Mack,et al.  Bayesian phylogeny of sucrose transporters: ancient origins, differential expansion and convergent evolution in monocots and dicots , 2014, Front. Plant Sci..

[42]  S. Baginsky,et al.  Identification of a Vacuolar Sucrose Transporter in Barley and Arabidopsis Mesophyll Cells by a Tonoplast Proteomic Approach1 , 2006, Plant Physiology.

[43]  A. Hayward,et al.  Integration analysis of quantitative trait loci for resistance to Sclerotinia sclerotiorum in Brassica napus , 2015, Euphytica.

[44]  W. Frommer,et al.  A New Subfamily of Sucrose Transporters, SUT4, with Low Affinity/High Capacity Localized in Enucleate Sieve Elements of Plants , 2000, Plant Cell.

[45]  P. Jameson,et al.  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 , 2015, Journal of experimental botany.

[46]  W. Frommer,et al.  SWEETs, transporters for intracellular and intercellular sugar translocation. , 2015, Current opinion in plant biology.

[47]  Xiyan Yang,et al.  Transcript profiling reveals complex auxin signalling pathway and transcription regulation involved in dedifferentiation and redifferentiation during somatic embryogenesis in cotton , 2012, BMC Plant Biology.

[48]  J. Poulain,et al.  The genome of the mesopolyploid crop species Brassica rapa , 2011, Nature Genetics.

[49]  Colby G Starker,et al.  Functional analysis of LjSUT4, a vacuolar sucrose transporter from Lotus japonicus , 2008, Plant Molecular Biology.

[50]  R. Furbank,et al.  The sucrose transporter gene family in rice. , 2003, Plant & cell physiology.

[51]  M. Sussman,et al.  Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[52]  J. Ward,et al.  Analysis of the transport activity of barley sucrose transporter HvSUT1. , 2005, Plant & cell physiology.

[53]  Igor B. Rogozin,et al.  Analysis of evolution of exon-intron structure of eukaryotic genes , 2005, Briefings Bioinform..

[54]  P. Bureš,et al.  Ancestral Chromosomal Blocks Are Triplicated in Brassiceae Species with Varying Chromosome Number and Genome Size1 , 2007, Plant Physiology.

[55]  P. Geigenberger,et al.  Sucrose Transporter StSUT 4 from Potato Affects Flowering , Tuberization , and Shade Avoidance Response 1 [ W ] , 2008 .

[56]  W. Frommer,et al.  Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. , 1992, The EMBO journal.

[57]  Stephane Rombauts,et al.  PlantCARE, a plant cis-acting regulatory element database , 1999, Nucleic Acids Res..

[58]  P. Bhalla,et al.  miRNAs in the crosstalk between phytohormone signalling pathways. , 2014, Journal of experimental botany.

[59]  Alisdair R Fernie,et al.  Sucrose Efflux Mediated by SWEET Proteins as a Key Step for Phloem Transport , 2012, Science.

[60]  P. Geigenberger,et al.  Sucrose Transporter StSUT4 from Potato Affects Flowering, Tuberization, and Shade Avoidance Response1[W] , 2007, Plant Physiology.

[61]  Damien Afoufa-Bastien,et al.  The Vitis vinifera sugar transporter gene family: phylogenetic overview and macroarray expression profiling , 2010, BMC Plant Biology.

[62]  Jung Sun Kim,et al.  Genome-wide comparative analysis of the Brassica rapa gene space reveals genome shrinkage and differential loss of duplicated genes after whole genome triplication , 2009, Genome Biology.

[63]  Xiaowu Wang,et al.  Deciphering the Diploid Ancestral Genome of the Mesohexaploid Brassica rapa[C][W] , 2013, Plant Cell.

[64]  D. Braun,et al.  SWEET as Sugar: New Sucrose Effluxers in Plants. , 2012, Molecular plant.

[65]  J. Ward,et al.  Evolution of Plant Sucrose Uptake Transporters , 2012, Front. Plant Sci..

[66]  Yun Zhao,et al.  Isolation and characterization of gene encoding G protein α subunit protein responsive to plant hormones and abiotic stresses in Brassica napus , 2010, Molecular Biology Reports.

[67]  A. Srivastava,et al.  Arabidopsis plants harbouring a mutation in AtSUC2, encoding the predominant sucrose/proton symporter necessary for efficient phloem transport, are able to complete their life cycle and produce viable seed. , 2009, Annals of botany.

[68]  Xiaowu Wang,et al.  Genome triplication drove the diversification of Brassica plants , 2014, Horticulture Research.