Russian Journal of GeneticsRussian Journal of GeneticsГенетика0016-67583034-5103The Russian Academy of Sciences66717610.31857/S0016675824100034wgdmziГЕНЕТИКА РАСТЕНИЙResearch ArticleGenome-Wide Identification and Characterization of Sugar Transporter Genes in Silver BirchПолногеномная идентификация и характеристика генов, кодирующих транспортеры сахаров у березы повислойKorzhenevskyiM. A.КорженевскийМ. А.
Russian Federation
tselishcheva.yulia@mail.ruMoshchenskayaYu. L.МощенскаяЮ. Л.
Russian Federation
tselishcheva.yulia@mail.ruTarelkinaT. V.ТарелкинаТ. В.
Russian Federation
tselishcheva.yulia@mail.ruGalibinaN. A.ГалибинаН. А.
Russian Federation
tselishcheva.yulia@mail.ruForest Research Institute of the Karelian Research Centre Russian Academy of SciencesИнститут леса – обособленное подразделение Федерального исследовательского центра “Карельский научный центр Российской академии наук”161020246010314626022025Copyright ©; 2024, Russian Academy of SciencesCopyright ©; 2024, Российская академия наук2024Russian Academy of SciencesРоссийская академия наукhttps://transsyst.ru/0016-6758/article/view/667176

Sugar transporters play an important role in regulating the long-distance sucrose transport from source to sink organs. The main sucrose absorber in woody plants is developing wood. Thus, sucrose transport, regulated by SUT, SWEET, and MST gene families, will determine the formation of woody biomass. Based on silver birch (Betula pendula var. pendula Roth) genomic data, we identified and analyze encoding sugar transporters in Betula pendula. We conducted BLAST-search, phylogenetic, structural analysis and analysis of cis-acting elements of sugar transporter genes and determined their chromosomal localization. We were able to identify and characterize 3 genes of the SUT family, 10 SWEET genes and 36 MST genes, which have a typical number of functional and transmembrane domains for the family. It was shown that silver birch contains a smaller number of sugar transporters genes compared to A. thaliana, which is probably because of the apoplastic type of terminal phloem loading in Arabidopsis, while in silver birch phloem loading is carried out predominantly symplastically. The results obtained may be useful for further study of the participation of sucrose transporters in various biosynthetic processes in woody plants and provide a basis for various biotechnological manipulations.

Транспортеры сахаров играют важную роль в регуляции дальнего транспорта сахарозы в растениях. Основным поглотителем сахарозы у древесных растений является формирующаяся древесина. Таким образом, транспорт сахарозы, регулируемый семействами генов SUT, SWEET и MST, будет определять формирование древесной биомассы. На основании данных генома березы повислой (Betula pendula var. pendula Roth) мы идентифицировали и проанализировали кодирующие транспортеры сахаров у Betula pendula. Мы провели BLAST-поиск, филогенетический, структурный анализы и анализ цис-действующих элементов генов-переносчиков сахаров и определили их хромосомную локализацию. Нам удалось идентифицировать и охарактеризовать три гена семейства SUT, 10 генов SWEET и 36 генов MST, которые имеют типичное для семейства количество функциональных и трансмембранных доменов. Показано, что береза повислая содержит меньшее количество генов-переносчиков сахаров по сравнению с A. thaliana, что, вероятно, связано с апопластным типом загрузки терминальной флоэмы у Arabidopsis, тогда как у березы повислой загрузка флоэмы осуществляется преимущественно симпластически. Полученные результаты могут быть полезны для дальнейшего изучения участия транспортеров сахарозы в различных биосинтетических процессах древесных растений и служить основой для различных биотехнологических манипуляций.

Betulapendula Rothsugar transportSUTSWEETMSTgene structureBetula pendula Rothтранспорт сахаровSUTSWEETMSTструктура генаРоссийский научный фонд (проект)Russian Science Foundation (project)22-74-00096Salojärvi J., Smolander O.P., Nieminen K. et al. Genome sequencing and population genomic analyses provide insights into the adaptive landscape of silver birch // Nat. Genet. 2017. V. 49. P. 904–912. https://doi.org/10.1038/ng.3862Koski V., Rousi M. A review of the promises and constraints of breeding silver birch (Betula pendula Roth) in Finland // Forestry: An Intern. J. Forest Research. 2005. V. 78. P. 187–198. doi:10.1093/forestry/cpi017Любавская А.Я. Карельская береза. М.: Лесная пром-ть., 1978. 158 с.Новицкая Л.Л. Карельская береза: механизмы роста и развития структурных аномалий. Петрозаводск: Verso, 2008. 143 с.Novitskaya L., Nikolaeva N., Tarelkina T. Endogenous variability of the figured wood of Karelian birch // Wulfenia. 2016. V. 23. P. 175–188.Galibina N.A., Novitskaya L.L., Nikerova K.M. et al. Labile nitrogen availability in soil influences the expression of wood pattern in Karelian birch // Botanicheskii Zhurnal. 2019.V. 104. № 10. P. 1598–1609. doi: 10.1134/S0006813619100053Galibina N.A., Novitskaya L.L., Moshchenskaya Y.L., Krasavina M.S. Activity of sucrose synthase in trunk tissues of Karelian birch during cambial growth// Russ. J. Plant Physiol. 2015. V. 62. P. 381–389. doi:10.1134/S102144371503005XGalibina N.A., Novitskaya L.L., Krasavina M.S., Moshchenskaya J.L. Invertase activity in trunk tissues of Karelian birch // Russ. J. Plant Physiol. 2015. V. 62. P. 753–760. doi:10.1134/S1021443715060060Moshchenskaya Y.L., Galibina N.A., Topchieva L.V., Novitskaya L.L. Expression of genes encoding sucrose synthase isoforms during anomalous xylogenesis in Karelian birch // Russ. J. Plant Physiol. 2017. V. 64. P. 616–624. doi:10.1134/S1021443717030104Novitskaya L.L., Nikolaeva N.N., Galibina N.A. et al. The greatest density of parenchyma inclusions in Karelian birch wood occurs at confluences of phloem flows // Silva Fenn. 2016. V. 50. P. 1461–1478. doi:10.14214/sf.1461Galibina N.A., Novitskaya L.L., Nikerova K.M. Source-sink relations in the organs and tissues of silver birch during different scenarios of xylogenesis // Russ. J. Plant Physiol. 2019. V. 66. P. 308–315. doi:10.1134/S1021443719020067Mahboubi A., Niittyla T. Sucrose transport and carbon fluxes during wood formation // Physiologia plantarum. 2018. V. 164. P. 67–81. doi:10.1111/ppl.12729Van Bel A.J.E. Xylem-phloem exchange via the rays: The undervalued route of transport // J. Exp. Bot. 1990. V. 41. P. 631–644. doi:10.1093/jxb/41.6.631Sauter J.J. The strasburger cells – equivalents of companion cells //Berichte der Deutschen Botan. Gesellschaft. 1980. Bd. 93. S. 29–42.Sauter J.J., Kloth S. Plasmodesmatal frequency and radial translocation rates in ray cells of poplar (Populus x Canadensis Moench ‘robusta’) // Planta. 1986. V. 168. P. 377–380. doi: 10.1007/BF00392363Roach M., Arrivault S., Mahboubi A. et al. Spatially resolved metabolic analysis reveals a central role for transcriptional control in carbon allocation to wood // J. Exp. Bot. 2017. V. 68. P. 3529–3539. doi:10.1093/jxb/erx200Uggla C., Magel E., Moritz T., Sundberg B. Function and dynamics of auxin and carbohydrates during earlywood/latewood transition in scots pine // Plant Physiol. 2001. V. 125. P. 2029–2039. doi:10.1104/pp.125.4.2029Sokołowska K., Zagórska-Marek B. Symplasmic, long-distance transport in xylem and cambial regions in branches of Acer pseudoplatanus (Aceraceae) and Populus tremula × P. Tremuloides (Salicaceae) // Am. J. Bot. 2012. V. 99. P. 1745–1755. doi: 10.3732/ajb.1200349Weise A., Barker L., Kühn C. et al. A new subfamily of sucrose transporters, SUT4, with low affinity/high capacity localized in enucleate sieve elements of plants // The Plant Cell. 2000. V. 12. P. 1345–1355. doi:10.1105/tpc.12.8.1345Stadler R., Brandner J., Schulz A. et al. Phloem loading by the PmSUC2 sucrose carrier from Plantago major occurs into companion cells // The Plant Cell. 1995. V. 7. P. 1545–1554. doi:10.1105/tpc.7.10.1545Baker R.F., Leach K.A., Boyer N.R. et al. Sucrose transporter ZmSut1 expression and localization uncover new insights into sucrose phloem loading // Plant Physiol. 2016. V. 172. P. 1876–1898. doi:10.1104/pp.16.00884Wang Y., Chen Y., Wei Q. et al. Phylogenetic relationships of sucrose transporters (SUTs) in plants and genome-wide characterization of SUT genes in Orchidaceae reveal roles in floral organ development // Peer J. 2021. V. 9. doi:10.7717/peerj.11961Aoki N., Hirose T., Scofield G.N. et al. The sucrose transporter gene family in rice // Plant Cell Physiol. 2003. V. 44. P. 223–232. doi: 10.1093/pcp/pcg030Barth I., Meyer S., Sauer N. PmSUC3: Characterization of a SUT2/SUC3-type sucrose transporter from Plantago major // Plant Cell. 2003. V. 15. P. 1375–1385. doi: 10.1105/tpc.010967Meyer S., Lauterbach C., Niedermeier M. et al. Wounding enhances expression of AtSUC3, a sucrose transporter from Arabidopsis sieve elements and sink tissues // Plant Physiol. 2004. V. 134. P. 684–693. doi: 10.1104/pp.103.033399Hackel A., Schauer N., Carrari F. et al. Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways // Plant J. 2004. V. 45. P. 180–192. doi: 10.1111/j.1365- 313X.2005.02572.xPeng D., Gu X., Xue L.-J. et al. Bayesian phylogeny of sucrose transporters: Ancient origins, differential expansion and convergent evolution in monocots and dicots // Frontiers in Plant Science. 2014. V. 5(615). P. 1–12. doi:10.3389/fpls.2014.00615Chen H.Y., Huh J.H., Yu Y.C. et al. The Arabidopsis vacuolar sugar transporter SWEET2 limits carbon sequestration from roots and restricts Pythium infection // Plant J. 2015. V. 83. P. 1046–1058. doi: 10.1111/tpj.12948Bock K.W., Honys D., Ward J.M. et al. Integrating membrane transport with male gametophyte development and function through transcriptomics // Plant Physiol. 2006. V. 140. P. 1151–1168. doi: 10.1104/pp.105.074708.Guan Y.F., Huang X.Y., Zhu J. et al. RUPTURED POLLEN GRAIN1, a member of the MtN3/saliva gene family, is crucial for exine pattern formation and cell integrity of microspores in Arabidopsis // Plant Physiol. 2008. V. 147. P. 852–863. doi:10.1104/pp.108.118026Zhang L., Wang L., Zhang J. et al. Expression and localization of SWEETs in Populus and the effect of SWEET7 overexpression in secondary growth // Tree Physiology. 2020. V. 41. P. 882–899. doi:10.1093/treephys/tpaa145.Slewinski T.L. Diverse functional roles of monosaccharide transporters and their homologs in vascular plants: A physiological perspective // Mol. Plant. 2011. V. 4. P. 641–662. doi:10.1093/mp/ssr051LiAfoufa-Bastien D., Medici A., Jeauffre J. et al. The Vitis vinifera sugar transporter gene family: Phylogenetic overview and macroarray expression profiling // Plant Biology. 2010. V. 10(245). P. 1–22. doi:10.1186/1471-2229-10-245Edgar R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput // Nucl. Acids Res. 2004. V. 32. № 5. P. 1792–1797. doi: 10.1093/nar/gkh340Hu B., Jin J., Guo A.Y. et al. GSDS 2.0: An upgraded gene feature visualization server // Bioinformatics. 2015. V. 31. № 8. P. 1296–1297. doi: 10.1093/bioinformatics/btu817Chen Ch., Chen H., Zhang Y. et al. TBtools: An integrative toolkit developed for interactive analyses of big biological data // Mol. Plant. 2020. V. 13. P. 1194–1202. doi:10.1016/j.molp.2020.06.009Doidy J., Vidal U., Lemoine R. Sugar transporters in Fabaceae, featuring SUT MST and SWEET families of the model plant Medicago truncatula and the agricultural crop Pisumsativum // PLoS One. 2019. V. 14. № 9. P. 1–19. https://doi.org/10.1371/journal.pone.0223173