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An In-Silico Study: Interaction of BOR1-type Boron (B) Transporters with A Small Group of Functionally Unidentified Proteins Under Various Stresses in Potato (Solanum tuberosum)

Year 2020, , 134 - 139, 31.12.2020
https://doi.org/10.31594/commagene.798805

Abstract

Boron (B) is an important micro element for plant metabolism. There are several transporters having a role in B transport in plants. In this study, BOR1-type B transporters in potato (Solanum tuberosum) was identified and characterized through bioinformatical approaches. The five out of 10 identified BOR1 transporters (StBOR1-2,4,5, and 10) were found in the transcriptomic data. The expression heat map and co-expression networks were constructed with these identified proteins. Results showed that these identified five transporters were expressed more under Benzothiadiazole (BTH) compared to other treatments. The co-expression networks of five B transporters, constructed using 24,950 genes at 0.99 correlation coefficient with expression threshold above one fold change, showed that three B transporters were co-expressed with three functionally unknown proteins and Heparanase 1, a defense protein against pathogens. Also, StBOR1-4 and StBOR1-8 were found to crosstalk with Heparanase 1, PGSC0003DMT400010798, and PGSC0003DMT400030256 proteins. Generally, StBOR1-8 appears to be a key player regulating B and plant signal and on the defense mechanism. The Gene Ontology (GO) analysis, conducted for prediction of molecular functions of B transporters, resulted in three different clusters. Similarity Network analysis showed that StBOR1-10 may be involved in more different biological processes compared to the rest of the studied StBOR1 transporters. The identified three unknown proteins interacting with BOR1-type transporters can be further investigated under biotic stress. Particularly, PGSC0003DMT400025924 gen may be a component of plant immunity system. Moreover, roles of three mentioned proteins in B uptake and accumulation mechanism can be considered for future research.

References

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  • Consortium EUC 3 AGS, Research TI for G, Institute KDNAR (2000). Sequence and analysis of chromosome 3 of the plant Arabidopsis thaliana. Nature, 408, 820–823. https://doi.org/10.1038/35048706
  • Consortium, T.U. (2019). UniProt: A worldwide hub of protein knowledge. Nucleic Acids Research, 47, D506–D515. https://doi.org/10.1093/nar/gky1049
  • Delaunois, B., Colby, T., Belloy, N., Conreux, A., Harzen, A., Baillieul, F.,... & Cordelier, S. (2013). Large-scale proteomic analysis of the grapevine leaf apoplastic fluid reveals mainly stress-related proteins and cell wall modifying enzymes. BMC Plant Biology, 13, 24. https://doi.org/10.1186/1471-2229-13-24
  • Draffehn, A.M., Li, L., Krezdorn, N., Ding, J., Lübeck, J., Strahwald, J.,....& Gebhardt, C. (2013). Comparative transcript profiling by SuperSAGE identifies novel candidate genes for controlling potato quantitative resistance to late blight not compromised by late maturity. Front Plant Science, 4, 1–21. https://doi.org/10.3389/fpls.2013.00423
  • Edgar, R., Domrachev, M., & Lash, A.E. (2002). Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Research, 30, 207–210. https://doi.org/10.1093/nar/30.1.207
  • Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M.r., Appel, R.D. & Bairoch, A. (2005). Protein Identification and Analysis Tools on the ExPASy Server. In: Walker J.M. (eds) The Proteomics Protocols Handbook. Springer Protocols Handbooks. Humana Press. https://doi.org/10.1385/1-59259-890-0:571
  • Goodstein, D.M., Shu, S., Howson, R., Neupane, R., Hayes, R.D., Fazo, J., Mitros, T., Dirks, W., Hellsten, U., Putnam, N., & Rokhsar, D.S. (2012). Phytozome: a comparative platform for green plant genomics. Nucleic Acids Research, 40(D1), D1178-D1186. https://doi.org/10.1093/nar/gkr944
  • Guerra-Guimarães, L., Pinheiro, C., Chaves, I., Barros, D.R., & Ricardo, C.P. (2016). Protein dynamics in the plant extracellular space. Proteomes, 4(22), 1-19. https://doi.org/10.3390/proteomes4030022
  • Kinsella, R.J., Kähäri, A., Haider, S., Zamora, J., Proctor, G., Spudich, G., Almeida-King, J., Staines, D., Derwent, P., Kerhornou, A., Kersey, P., & Flicek, P. (2011). Ensembl BioMarts: A hub for data retrieval across taxonomic space. Database, 2011(bar030), 1-9. https://doi.org/10.1093/database/bar030
  • Liu, Q., Liu, H., Gong, Y., Tao, Y., Jiang, L., Zuo, W.,...& Xu, M. (2017). An Atypical Thioredoxin Imparts Early Resistance to Sugarcane Mosaic Virus in Maize. Molecular Plant, 10, 483–497. https://doi.org/10.1016/j.molp.2017.02.002
  • Mata-Pérez, C., & Spoel, S.H. (2019). Thioredoxin-mediated redox signalling in plant immunity. Plant Science, 279, 27–33. https://doi.org/10.1016/j.plantsci.2018.05.001
  • Mortaji, Z. (2011). Cellulose Biosynthesis Inhibitors Modulate Defense Transcripts and Regulate Genes that are Implicated in Cell Wall Re-Structuring in Arabidopsis (M.Sc. Thesis), University of Ontario Institute of Technology, Canada.
  • Noguchi, K., Ishii, T., Matsunaga, T., Kakegawa, K., Hayashi, H., & Fujiwara, T. (2003). Biochemical properties of the cell wall in the Arabidopsis mutant bor1-1 in relation to boron nutrition. Journal of Plant Nutrition and Soil Science, 166, 175–178. https://doi.org/10.1002/jpln.200390025
  • Ozyigit, I.I., Filiz, E., Saracoglu, I.A., & Karadeniz, S. (2020). Exploration of two major boron transport genes BOR1 and NIP5;1 in the genomes of different plants. Biotechnology & Biotechnological Equipment, 34(1), 455-468. https://doi.org/10.1080/13102818.2020.1773311
  • Reid, R. (2014). Understanding the boron transport network in plants. Plant Soil, 385, 1-13. https://doi.org/10.1007/s11104-014-2149-y
  • Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B., & Ideker, T. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome research, 13(11), 2498–2504. https://doi.org/10.1101/gr.1239303
  • Supek, F., Bošnjak, M., Škunca, N., & Šmuc, T. (2011). Revigo summarizes and visualizes long lists of gene ontology terms. PLoS ONE, 6(7), e21800. https://doi.org/10.1371/journal.pone.0021800
  • Takano, J., Noguchi, K., Yasumori, M., Kobayashi, M., Gajdos, Z., Miwa, K., Hayashi, H., Yoneyama, T., & Fujiwara, T. (2002). Arabidopsis boron transporter for xylem loading. Nature, 420(6913), 337–340. https://doi.org/10.1038/nature01139
  • Tanaka, M., & Fujiwara, T. (2008). Physiological roles and transport mechanisms of boron: Perspectives from plants. Pflügers Archiv - European Journal of Physiology, 456, 671–677. https://doi.org/10.1007/s00424-007-0370-8
  • Tian, T., Liu, Y., Yan, H., You, Q., Yi, X., Du, Z., Xu, W., & Su, Z. (2017). AgriGO v2.0: A GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Research, 45(W1), W122–W129. https://doi.org/10.1093/nar/gkx382
  • Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D.R..... & Pachter, L. (2012). Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protocols, 7, 562–578. https://doi.org/10.1038/nprot.2012.016
  • van Rossum, G., & Drake, F.L. (2009). Python 3 Reference Manual. CreateSpace, Scotts Valley, CA
  • Welter, L.J., Tisch, C., Kortekamp, A., Töpfer, R., & Zyprian, E. (2017). Powdery mildew responsive genes of resistant grapevine cultivar “regent.” Vitis – Journal of Grapevine Research, 56, 181–188. https://doi.org/10.5073/vitis.2017.56.181-188
  • Xu, X., Pan, S., Cheng, S., Zhang, B., Mu, D., Ni, P., ..... & Visser, R.G.F. (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195. https://doi.org/10.1038/nature10158
  • Yoshinari, A., & Takano, J. (2017). Insights into the mechanisms underlying boron homeostasis in plants. Frontiers in Plant Science, 8(1951), 1-8. https://doi.org/10.3389/fpls.2017.01951
  • Yoshinari, A., Hosokawa, T., Amano, T., Beier, M.P., Kunieda, T., Shimada, T…. & Takano, J. (2019). Polar localization of the borate exporter bor1 requires AP2-dependent endocytosis. Plant Physiol, 179, 1569–1580. https://doi.org/10.1104/pp.18.01017
  • Yu, C.S., Cheng, C.W., Su, W.C., Chang, K.C., Huang, S.W., Hwang, J.K., & Lu, C.H. (2014). CELLO2GO: A web server for protein subCELlular LOcalization prediction with functional gene ontology annotation. PLOS ONE, 9(6), e99368. https://doi.org/10.1371/journal.pone.0099368
  • Yu, Q., Baluška, F., Jasper, F., Menzel, D., & Goldbach, H.E. (2003). Short-term boron deprivation enhances levels of cytoskeletal proteins in maize, but not zucchini, root apices. Physiol Plant, 117(2), 270-278. https://doi.org/10.1034/j.1399-3054.2003.00029
  • Zallot, R., Oberg, N., & Gerlt, J.A. (2019). The EFI Web Resource for Genomic Enzymology Tools: Leveraging Protein, Genome, and Metagenome Databases to Discover Novel Enzymes and Metabolic Pathways. Biochemistry, 58(41), 4169-4182. https://doi.org/10.1021/acs.biochem.9b00735
  • Yoshinari, A., Kasai, K., Fujiwara, T., Naito, S., & Takano, J. (2012). Polar localization and endocytic degradation of a boron transporter, BOR1, is dependent on specific tyrosine residues. Plant Signaling Behavior, 7, 46–49. https://doi.org/10.4161/psb.7.1.18527

Bilgisayar Ortamında Bir Çalışma: BOR1-tipi Bor (B) Taşıyıcılarının Patateste (S. tuberosum) Çeşitli Stresler Altında İşlevsel Olarak Tanımlanmamış Küçük Bir Protein Grubuyla Etkileşimi

Year 2020, , 134 - 139, 31.12.2020
https://doi.org/10.31594/commagene.798805

Abstract

Bor (B) bitki metabolizması için önemli bir mikroelementtir. Bitkilerde B taşınımında rol oynayan farklı taşıyıcılar bulunmaktadır. Bu çalışmada patates (Solanum tuberosum) bitkisindeki BOR1 tipi B taşıyıcıları biyoinformatiksel yaklaşımlarla belirlenmiş ve karakterize edilmiştirler. On BOR1 taşıyıcısından beş tanesi (StBOR1-2,4,5, ve 10) transkriptomik veri seti içerisinde bulunmuştur. Ekspresyon ısı haritası ve ko-ekspresyon veri ağları belirlenen beş proteine göre yapılmıştır. Sonuç olarak, BOR1 transporter olarak belirlenen beş transporterın en fazla Benzothiadiazole (BTH) uygulamasında eksprese edildiği bulunmuştur. 24950 genin 0.99 korelasyon katsayısı ve bir kat ve üzeri eşik değeri dikkate alınarak oluşturulan beş BOR1 geninin, patojenlere karşı bir savunma proteini olan Heparanase 1 ve fonksiyonel olarak tanımı yapılmamış üç farklı genle ko-eksprese edildiği saptanmıştır. Aynı zamanda StBOR1-4 ve StBOR1-8’nin Heparanase 1, PGSC0003DMT400010798, ve PGSC0003DMT400030256 proteinleri ile çapraz iletişimi bulunmuştur. Genel olarak, StBOR1-8 B alımın, bitki sinyal ve savunma mekanizmasının düzenlenmesinde anahtar bir rol oynadığı görülmektedir. StBOR1 genlerinin moleküler fonksiyonlarına ışık tutmak için yapılan Gen Ontolojisi (GO) analizine göre üç farklı demet meydana gelmiştir. Benzerlik ağı analizine göre StBOR1-10’un, bu çalışmada incelenen diğer StBOR1 genelerine göre çok daha farklı biyolojik proseslerde yer alabileceği görülmüştür. Bu çalışmada StBOR1 taşıyıcıları ile etkileşen ve fonksiyonu bilinmeyen üç proteinin biyotik stres altında incelenmesi ileriki çalışmalarda yapılabilir. Özellikle, PGSC0003DMT400025924 geni bitki bağışıklık sisteminin bir parçası olabilir. Ayrıca, bu proteinlerinin B alınımı ve depolanma mekanizmasındaki rolleri gelecek araştırmalarda ele alınabilir.

References

  • Afgan, E., Baker, D., van den Beek, M., Blankenberg, D., Bouvier, D., Čech, M.,...& Goecks, J. (2016). The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2016 update. Nucleic Acids Research, 44, W3–W10. https://doi.org/10.1093/nar/gkw343
  • Consortium EUC 3 AGS, Research TI for G, Institute KDNAR (2000). Sequence and analysis of chromosome 3 of the plant Arabidopsis thaliana. Nature, 408, 820–823. https://doi.org/10.1038/35048706
  • Consortium, T.U. (2019). UniProt: A worldwide hub of protein knowledge. Nucleic Acids Research, 47, D506–D515. https://doi.org/10.1093/nar/gky1049
  • Delaunois, B., Colby, T., Belloy, N., Conreux, A., Harzen, A., Baillieul, F.,... & Cordelier, S. (2013). Large-scale proteomic analysis of the grapevine leaf apoplastic fluid reveals mainly stress-related proteins and cell wall modifying enzymes. BMC Plant Biology, 13, 24. https://doi.org/10.1186/1471-2229-13-24
  • Draffehn, A.M., Li, L., Krezdorn, N., Ding, J., Lübeck, J., Strahwald, J.,....& Gebhardt, C. (2013). Comparative transcript profiling by SuperSAGE identifies novel candidate genes for controlling potato quantitative resistance to late blight not compromised by late maturity. Front Plant Science, 4, 1–21. https://doi.org/10.3389/fpls.2013.00423
  • Edgar, R., Domrachev, M., & Lash, A.E. (2002). Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Research, 30, 207–210. https://doi.org/10.1093/nar/30.1.207
  • Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M.r., Appel, R.D. & Bairoch, A. (2005). Protein Identification and Analysis Tools on the ExPASy Server. In: Walker J.M. (eds) The Proteomics Protocols Handbook. Springer Protocols Handbooks. Humana Press. https://doi.org/10.1385/1-59259-890-0:571
  • Goodstein, D.M., Shu, S., Howson, R., Neupane, R., Hayes, R.D., Fazo, J., Mitros, T., Dirks, W., Hellsten, U., Putnam, N., & Rokhsar, D.S. (2012). Phytozome: a comparative platform for green plant genomics. Nucleic Acids Research, 40(D1), D1178-D1186. https://doi.org/10.1093/nar/gkr944
  • Guerra-Guimarães, L., Pinheiro, C., Chaves, I., Barros, D.R., & Ricardo, C.P. (2016). Protein dynamics in the plant extracellular space. Proteomes, 4(22), 1-19. https://doi.org/10.3390/proteomes4030022
  • Kinsella, R.J., Kähäri, A., Haider, S., Zamora, J., Proctor, G., Spudich, G., Almeida-King, J., Staines, D., Derwent, P., Kerhornou, A., Kersey, P., & Flicek, P. (2011). Ensembl BioMarts: A hub for data retrieval across taxonomic space. Database, 2011(bar030), 1-9. https://doi.org/10.1093/database/bar030
  • Liu, Q., Liu, H., Gong, Y., Tao, Y., Jiang, L., Zuo, W.,...& Xu, M. (2017). An Atypical Thioredoxin Imparts Early Resistance to Sugarcane Mosaic Virus in Maize. Molecular Plant, 10, 483–497. https://doi.org/10.1016/j.molp.2017.02.002
  • Mata-Pérez, C., & Spoel, S.H. (2019). Thioredoxin-mediated redox signalling in plant immunity. Plant Science, 279, 27–33. https://doi.org/10.1016/j.plantsci.2018.05.001
  • Mortaji, Z. (2011). Cellulose Biosynthesis Inhibitors Modulate Defense Transcripts and Regulate Genes that are Implicated in Cell Wall Re-Structuring in Arabidopsis (M.Sc. Thesis), University of Ontario Institute of Technology, Canada.
  • Noguchi, K., Ishii, T., Matsunaga, T., Kakegawa, K., Hayashi, H., & Fujiwara, T. (2003). Biochemical properties of the cell wall in the Arabidopsis mutant bor1-1 in relation to boron nutrition. Journal of Plant Nutrition and Soil Science, 166, 175–178. https://doi.org/10.1002/jpln.200390025
  • Ozyigit, I.I., Filiz, E., Saracoglu, I.A., & Karadeniz, S. (2020). Exploration of two major boron transport genes BOR1 and NIP5;1 in the genomes of different plants. Biotechnology & Biotechnological Equipment, 34(1), 455-468. https://doi.org/10.1080/13102818.2020.1773311
  • Reid, R. (2014). Understanding the boron transport network in plants. Plant Soil, 385, 1-13. https://doi.org/10.1007/s11104-014-2149-y
  • Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B., & Ideker, T. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome research, 13(11), 2498–2504. https://doi.org/10.1101/gr.1239303
  • Supek, F., Bošnjak, M., Škunca, N., & Šmuc, T. (2011). Revigo summarizes and visualizes long lists of gene ontology terms. PLoS ONE, 6(7), e21800. https://doi.org/10.1371/journal.pone.0021800
  • Takano, J., Noguchi, K., Yasumori, M., Kobayashi, M., Gajdos, Z., Miwa, K., Hayashi, H., Yoneyama, T., & Fujiwara, T. (2002). Arabidopsis boron transporter for xylem loading. Nature, 420(6913), 337–340. https://doi.org/10.1038/nature01139
  • Tanaka, M., & Fujiwara, T. (2008). Physiological roles and transport mechanisms of boron: Perspectives from plants. Pflügers Archiv - European Journal of Physiology, 456, 671–677. https://doi.org/10.1007/s00424-007-0370-8
  • Tian, T., Liu, Y., Yan, H., You, Q., Yi, X., Du, Z., Xu, W., & Su, Z. (2017). AgriGO v2.0: A GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Research, 45(W1), W122–W129. https://doi.org/10.1093/nar/gkx382
  • Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D.R..... & Pachter, L. (2012). Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protocols, 7, 562–578. https://doi.org/10.1038/nprot.2012.016
  • van Rossum, G., & Drake, F.L. (2009). Python 3 Reference Manual. CreateSpace, Scotts Valley, CA
  • Welter, L.J., Tisch, C., Kortekamp, A., Töpfer, R., & Zyprian, E. (2017). Powdery mildew responsive genes of resistant grapevine cultivar “regent.” Vitis – Journal of Grapevine Research, 56, 181–188. https://doi.org/10.5073/vitis.2017.56.181-188
  • Xu, X., Pan, S., Cheng, S., Zhang, B., Mu, D., Ni, P., ..... & Visser, R.G.F. (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195. https://doi.org/10.1038/nature10158
  • Yoshinari, A., & Takano, J. (2017). Insights into the mechanisms underlying boron homeostasis in plants. Frontiers in Plant Science, 8(1951), 1-8. https://doi.org/10.3389/fpls.2017.01951
  • Yoshinari, A., Hosokawa, T., Amano, T., Beier, M.P., Kunieda, T., Shimada, T…. & Takano, J. (2019). Polar localization of the borate exporter bor1 requires AP2-dependent endocytosis. Plant Physiol, 179, 1569–1580. https://doi.org/10.1104/pp.18.01017
  • Yu, C.S., Cheng, C.W., Su, W.C., Chang, K.C., Huang, S.W., Hwang, J.K., & Lu, C.H. (2014). CELLO2GO: A web server for protein subCELlular LOcalization prediction with functional gene ontology annotation. PLOS ONE, 9(6), e99368. https://doi.org/10.1371/journal.pone.0099368
  • Yu, Q., Baluška, F., Jasper, F., Menzel, D., & Goldbach, H.E. (2003). Short-term boron deprivation enhances levels of cytoskeletal proteins in maize, but not zucchini, root apices. Physiol Plant, 117(2), 270-278. https://doi.org/10.1034/j.1399-3054.2003.00029
  • Zallot, R., Oberg, N., & Gerlt, J.A. (2019). The EFI Web Resource for Genomic Enzymology Tools: Leveraging Protein, Genome, and Metagenome Databases to Discover Novel Enzymes and Metabolic Pathways. Biochemistry, 58(41), 4169-4182. https://doi.org/10.1021/acs.biochem.9b00735
  • Yoshinari, A., Kasai, K., Fujiwara, T., Naito, S., & Takano, J. (2012). Polar localization and endocytic degradation of a boron transporter, BOR1, is dependent on specific tyrosine residues. Plant Signaling Behavior, 7, 46–49. https://doi.org/10.4161/psb.7.1.18527
There are 31 citations in total.

Details

Primary Language English
Subjects Structural Biology
Journal Section Research Articles
Authors

Firat Kurt 0000-0003-0172-1953

Adnan Aydın 0000-0002-8284-3751

Publication Date December 31, 2020
Submission Date September 27, 2020
Acceptance Date December 3, 2020
Published in Issue Year 2020

Cite

APA Kurt, F., & Aydın, A. (2020). An In-Silico Study: Interaction of BOR1-type Boron (B) Transporters with A Small Group of Functionally Unidentified Proteins Under Various Stresses in Potato (Solanum tuberosum). Commagene Journal of Biology, 4(2), 134-139. https://doi.org/10.31594/commagene.798805
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