Genome-wide analysis indicates diverse physiological roles of the turnip (Brassica rapa var. rapa) oligopeptide transporters gene family

doi:10.1016/j.pld.2018.03.001

Abstract

Abstract:

Oligopeptide transporters (OPTs) encode integral membrane-localized proteins and have a broad range of substrate transport capabilities.Here,28 BrrOPT genes were identified in the turnip.Phylogenetic analyses revealed two well-supported clades in the OPT family,containing 15 BrrOPTs and 13 BrrYSLs. The exon/intron structure of OPT clade are conserved but the yellow stripe-like (YSL) clade was different. The exon/intron of the YSL clade possesses structural differences,whereas the YSL class motifs structure are conserved.The OPT genes are distributed unevenly among the chromosomes of the turnip genome. Phylogenetic and chromosomal distribution analyses revealed that the expansion of the OPT gene family is mainly attributable to segmental duplication.For the expression profiles at different developmental stages,a comprehensive analysis provided insights into the possible functional divergence among members of the paralog OPT gene family.Different expression levels under a variety of ion deficiencies also indicated that the OPT family underwent functional divergence during long-term evolution. Furthermore,BrrOPT8.1,BrrYSL1.2,BrrYSL1.3,BrrYSL6 and BrrYSL9 responded to Fe (Ⅱ) treatments and BrrYSL7 responded to calcium treatments,BrrYSL6 responded to multiple treatments in root,suggesting that turnip OPTs may be involved in mediating cross-talk among different ion deficiencies.Our data provide important information for further functional dissection of BrrOPTs,especially in transporting metal ions and nutrient deficiency stress adaptation.

Key words: BrrOPTs, Segmental duplication, Functional differentiation, Turnip

Yanan Pu, Danni Yang, Xin Yin, Qiuli Wang, Qian Chen, Yunqiang Yang, Yongping Yang. Genome-wide analysis indicates diverse physiological roles of the turnip (Brassica rapa var. rapa) oligopeptide transporters gene family[J]. Plant Diversity, 2018, 40(02): 57-67.

References

Aoyama, T., Kobayashi, T., Takahashi, M., Nagasaka, S., Usuda, K., Kakei, Y., Ishimaru, Y., Nakanishi, H., Mori, S., Nishizawa, N.K., 2009. OsYSL18 is a rice iron(Ⅲ)edeoxymugineic acid transporter specifically expressed in reproductive organs and phloem of lamina joints. Plant Mol. Biol. 70, 681-692.
Bailey, T.L., Williams, N., Misleh, C., Li, W.W., 2006. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 34, W369eW373.
Buckhout, T.J., Yang, T.J., Schmidt, W., 2009. Early iron-deficiency-induced transcriptional changes in Arabidopsis roots as revealed by microarray analyses.BMC Genomics 10, 147.
Cagnac, O., Bourbouloux, A., Chakrabarty, D., Zhang, M.Y., Delrot, S., 2004. AtOPT6 transports glutathione derivatives and is induced by primisulfuron. Plant Physiol. 135, 1378-1387.
Cao, J., Huang, J., Yang, Y., Hu, X., 2011. Analyses of the oligopeptide transporter gene family in poplar and grape. BMC Genomics 12, 465.
Cheng, F., Sun, R., Hou, X., Zheng, H., Zhang, F., Zhang, Y., Liu, B., Liang, J., Zhuang, M., Liu, Y., Liu, D., Wang, X., Li, P., Liu, Y., Lin, K., Bucher, J., Zhang, N., Wang, Y., Wang, H., Deng, J., Liao, Y., Wei, K., Zhang, X., Fu, L., Hu, Y., Liu, J., Cai, C., Zhang, S., Zhang, S., Li, F., Zhang, H., Zhang, J., Guo, N., Liu, Z., Liu, J., Sun, C., Ma, Y., Zhang, H., Cui, Y., Freeling, M.R., Borm, T., Bonnema, G., Wu, J., Wang, X., 2016. Subgenome parallel selection is associated with morphotype diversification and convergent crop domestication in Brassica rapa and Brassica oleracea. Nat. Genet. 48, 1218-1224.
Curie, C., Panaviene, Z., Loulergue, C., Dellaporta, S.L., Briat, J.F., Walker, E.L., 2001.Maize yellow stripe1 encodes a membrane protein directly involved in Fe(Ⅲ) uptake. Nature 409, 346-349.
DiDonato Jr., R.J., Roberts, L.A., Sanderson, T., Eisley, R.B., Walker, E.L., 2004. Arabidopsis Yellow Stripe-Like2 (YSL2): a metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes. Plant J. 39, 403-414.
Doyle, D.A., Morais Cabral, J., Pfuetzner, R.A., Kuo, A., Gulbis, J.M., Cohen, S.L., Chait, B.T., MacKinnon, R., 1998. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280, 69-77.
Fernandes, F., Valentao, P., Sousa, C., Pereira, J., Seabra, R., Andrade, P., 2007.Chemical and antioxidative assessment of dietary turnip (Brassica rapa var. rapa L.). Food Chem. 105, 1003-1010.
Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S.E., Wilkins, M.R., Appel, R.D., Bairoch, A., 2005. Protein Identification and Analysis Tools on the ExPASy Server. Springer.
Gomolplitinant, K.M., Saier Jr., M.H., 2011. Evolution of the oligopeptide transporter family. J. Membr. Biol. 240, 89-110.
Gruber, B.D., Giehl, R.F., Friedel, S., von Wiren, N., 2013. Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol. 163, 161-179.
Hell, R., Stephan, U.W., 2003. Iron uptake, trafficking and homeostasis in plants.Planta 216, 541-551.
Hepler, P.K., 2005. Calcium: a central regulator of plant growth and development.Plant Cell 17, 2142-2155.
Hirsch, R.E., Lewis, B.D., Spalding, E.P., Sussman, M.R., 1998. A role for the AKT1 potassium channel in plant nutrition. Science 280, 918-921.
Horton, P., Park, K.J., Obayashi, T., Fujita, N., Harada, H., Adams-Collier, C.J., Nakai, K., 2007. WoLF PSORT: protein localization predictor. Nucleic Acids Res. 35, W585eW587.
Hu, B., Jin, J., Guo, A.Y., Zhang, H., Luo, J., Gao, G., 2015. GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31, 1296-1297.
Ishimaru, Y., Masuda, H., Bashir, K., Inoue, H., Tsukamoto, T., Takahashi, M., Nakanishi, H., Aoki, N., Hirose, T., Ohsugi, R., Nishizawa, N.K., 2010. Rice metalnicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. Plant J. 62, 379-390.
Jackson, L.A., Dyer, D.W., 2012. Protocol for gene expression profiling using DNA microarrays in Neisseria gonorrhoeae. Methods Mol. Biol. 903, 343-357.
Kent, W.J., Baertsch, R., Hinrichs, A., Miller, W., Haussler, D., 2003. Evolution's cauldron: duplication, deletion, and rearrangement in the mouse and human genomes. Proc. Natl. Acad. Sci. U. S. A. 100, 11484-11489.
Koh, S., Wiles, A.M., Sharp, J.S., Naider, F.R., Becker, J.M., Stacey, G., 2002. An oligopeptide transporter gene family in Arabidopsis. Plant Physiol. 128, 21-29.
Koike, S., Inoue, H., Mizuno, D., Takahashi, M., Nakanishi, H., Mori, S., Nishizawa, N.K., 2004. OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. Plant J. 39, 415-424.
Kumar, S., Stecher, G., Tamura, K., 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870-1874.
Lee, S., Chiecko, J.C., Kim, S.A., Walker, E.L., Lee, Y., Guerinot, M.L., An, G., 2009.Disruption of OsYSL15 leads to iron inefficiency in rice plants. Plant Physiol. 150, 786-800.
Li, J., Ding, Q., Wang, F., Zhang, Y., Li, H., Gao, J., 2015. Integrative analysis of mRNA and miRNA expression profiles of the tuberous root development at seedling stages in turnips. PLoS One 10, e0137983.
Liang, Y.S., Kim, H.K., Lefeber, A.W., Erkelens, C., Choi, Y.H., Verpoorte, R., 2006.Identification of phenylpropanoids in methyl jasmonate treated Brassica rapa leaves using two-dimensional nuclear magnetic resonance spectroscopy.J. Chromatogr. A 1112, 148-155.
Lubkowitz, M., 2006. The OPT family functions in long-distance peptide and metal transport in plants. Genet. Eng. (N. Y.) 27, 35-55.
Lubkowitz, M., 2011. The oligopeptide transporters: a small gene family with a diverse group of substrates and functions? Mol. Plant 4, 407-415.Maguire, M.E., 2006. Magnesium transporters: properties, regulation and structure.Front. Biosci. 11, 3149-3163.
Mehan, M.R., Freimer, N.B., Ophoff, R.A., 2004. A genome-wide survey of segmental duplications that mediate common human genetic variation of chromosomal architecture. Hum Genomics 1, 335-344.
Murata, Y., Ma, J.F., Yamaji, N., Ueno, D., Nomoto, K., Iwashita, T., 2006. A specific transporter for iron(Ⅲ)-phytosiderophore in barley roots. Plant J. 46, 563-572.
Osawa, H., Stacey, G., Gassmann, W., 2006. ScOPT1 and AtOPT4 function as protoncoupled oligopeptide transporters with broad but distinct substrate specificities. Biochem. J. 393, 267-275.
Perea-Garcia, A., Garcia-Molina, A., Andres-Colas, N., Vera-Sirera, F., PerezAmador, M.A., Puig, S., Penarrubia, L., 2013. Arabidopsis copper transport protein COPT2 participates in the cross talk between iron deficiency responses and low-phosphate signaling. Plant Physiol. 162, 180-194.
Pike, S., Patel, A., Stacey, G., Gassmann, W., 2009. Arabidopsis OPT6 is an oligopeptide transporter with exceptionally broad substrate specificity. Plant Cell Physiol. 50, 1923-1932.
Prince, V.E., Pickett, F.B., 2002. Splitting pairs: the diverging fates of duplicated genes. Nat. Rev. Genet. 3, 827-837.
Roberts, L.A., Pierson, A.J., Panaviene, Z., Walker, E.L., 2004. Yellow stripe1.Expanded roles for the maize iron-phytosiderophore transporter. Plant Physiol. 135, 112-120.
Schranz, M.E., Lysak, M.A., Mitchell-Olds, T., 2006. The ABC's of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci. 11, 535-542.
Shen, Y., Liu, M., Wang, L., Li, Z., Taylor, D.C., Li, Z., Zhang, M., 2016. Identification, duplication, evolution and expression analyses of caleosins in Brassica plants and Arabidopsis subspecies. Mol. Genet. Genomics 291, 971-988.
Stacey, M.G., Osawa, H., Patel, A., Gassmann, W., Stacey, G., 2006. Expression analyses of Arabidopsis oligopeptide transporters during seed germination, vegetative growth and reproduction. Planta 223, 291-305.
Stacey, M.G., Patel, A., McClain, W.E., Mathieu, M., Remley, M., Rogers, E.E., Gassmann, W., Blevins, D.G., Stacey, G., 2008. The Arabidopsis AtOPT3 protein functions in metal homeostasis and movement of iron to developing seeds.Plant Physiol. 146, 589-601.
Sturn, A., Quackenbush, J., Trajanoski, Z., 2002. Genesis: cluster analysis of microarray data. Bioinformatics 18, 207-208.
Vasconcelos, M.W., Li, G.W., Lubkowitz, M.A., Grusak, M.A., 2008. Characterization of the PT clade of oligopeptide transporters in rice. Plant Genome J. 1, 77.
Wintz, H., Fox, T., Wu, Y.Y., Feng, V., Chen, W., Chang, H.S., Zhu, T., Vulpe, C., 2003.Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. J. Biol. Chem. 278, 47644-47653.
Yang, T., Poovaiah, B.W., 2003. Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci. 8, 505-512.
Yang, Y.-W., Lai, K.-N., Tai, P.-Y., Li, W.-H., 1999. Rates of nucleotide substitution in angiosperm mitochondrial DNA sequences and dates of divergence between Brassica and other angiosperm lineages. J. Mol. Evol. 48, 597-604.
Yang, Z., 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol.Evol. 24, 1586-1591.
Zhai, Z., Gayomba, S.R., Jung, H.I., Vimalakumari, N.K., Pineros, M., Craft, E., Rutzke, M.A., Danku, J., Lahner, B., Punshon, T., Guerinot, M.L., Salt, D.E., Kochian, L.V., Vatamaniuk, O.K., 2014. OPT3 is a phloem-specific iron transporter that is essential for systemic iron signaling and redistribution of iron and cadmium in Arabidopsis. Plant Cell 26, 2249-2264.
Zhang, B., Yang, L., Wang, W., Li, Y., Li, H., 2011. Environmental selenium in the Kaschin-Beck disease area, Tibetan Plateau, China. Environ. Geochem. Health 33, 495-501.
Zhang, M.Y., Bourbouloux, A., Cagnac, O., Srikanth, C.V., Rentsch, D., Bachhawat, A.K., Delrot, S., 2004. A novel family of transporters mediating the transport of glutathione derivatives in plants. Plant Physiol. 134, 482-491.
Zheng, L., Huang, F., Narsai, R., Wu, J., Giraud, E., He, F., Cheng, L., Wang, F., Wu, P., Whelan, J., Shou, H., 2009. Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings. Plant Physiol. 151, 262-274.

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