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Research Paper

Functional characterization of C-TERMINALLY ENCODED PEPTIDE (CEP) family in Brassica rapa L

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Article: 2021365 | Received 24 Nov 2021, Accepted 16 Dec 2021, Published online: 30 Dec 2021

References

  • Tavormina P, De Coninck B, Nikonorova N, De Smet I, Cammue BP. The plant peptidome: an expanding repertoire of structural features and biological functions. Plant Cell. 2015;27(8):2095–10. doi:10.1105/tpc.15.00440.
  • Takahashi F, Hanada K, Kondo T, Shinozaki K. Hormone-like peptides and small coding genes in plant stress signaling and development. Curr Opin Plant Biol. 2019;51:88–95. doi:10.1016/j.pbi.2019.05.011.
  • Tanco S, Gevaert K, Van Damme P. C‐terminomics: targeted analysis of natural and posttranslationally modified protein and peptide C‐termini. Proteomics. 2015;15(5–6):903–914. doi:10.1002/pmic.201400301.
  • Stührwohldt N, Schaller A, Staiger D. Regulation of plant peptide hormones and growth factors by post-translational modification. Plant Biol (Stuttg). 2019;1:49–63. doi:10.1111/plb.12881.
  • Delay C, Imin N, Djordjevic MA. CEP genes regulate root and shoot development in response to environmental cues and are specific to seed plants. J Exp Bot. 2013;64(17):5383–5394. doi:10.1093/jxb/ert332.
  • Roberts I, Smith S, De Rybel B, Van Den Broeke J, Smet W, De Cokere S, Mispelaere, M, De Smet I, Beeckman T. The CEP family in land plants: evolutionary analyses, expression studies, and role in Arabidopsis shoot development. J Exp Bot. 2013;64(17):5371–5381. doi:10.1093/jxb/ert331.
  • Ogilvie HA, Imin N, Djordjevic MA. Diversification of the C-TERMINALLY ENCODED PEPTIDE (CEP) gene family in angiosperms, and evolution of plant-family specific CEP genes. BMC Genomics. 2014;15(1):870. doi:10.1186/1471-2164-15-870.
  • Ohyama K, Ogawa M, Matsubayashi Y. Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC‐MS‐based structure analysis. Plant J. 2008;55(1):152–160. doi:10.1111/j.1365-313X.2008.03464.x.
  • Sui Z, Wang T, Li H, Zhang M, Li Y, Xu R, Xing G, Ni Z, Xin M. Overexpression of peptide-encoding OsCEP6.1 results in pleiotropic effects on growth in Rice (O. sativa). Front Plant Sci. 2016;7:228. doi:10.3389/fpls.2016.00228.
  • Roberts I, Smith S, Stes E, De Rybel B, Staes A, Van De Cotte B, Njo MF, Dedeyne L, Demol H, Lavenus J, et al. CEP5 and XIP1/CEPR1 regulate lateral root initiation in Arabidopsis. J Exp Bot. 2016;67(16):4889–4899. doi:10.1093/jxb/erw231.
  • Chapman K, Taleski M, Ogilvie HA, Imin N, Djordjevic MA. CEP-CEPR1 signalling inhibits the sucrose-dependent enhancement of lateral root growth. J Exp Bot. 2019;70(15):3955–3967. doi:10.1093/jxb/erz207.
  • Delay C, Chapman K, Taleski M, Wang Y, Tyagi S, Xiong Y, Djordjevic MA. CEP3 levels affect starvation-related growth responses of the primary root. J Exp Bot. 2019;70(18):4763–4774. doi:10.1093/jxb/erz270.
  • Zhou Y, Sarker U, Neumann G, Ludewig U. The LaCEP1 peptide modulates cluster root morphology in Lupinus albus. Physiol Plant. 2019;166(2):525–537. doi:10.1111/ppl.12799.
  • Liu Y, Zuo T, Qiu Z, Zhuang K, Hu S, Han H. Genome-wide identification reveals the function of CEP peptide in cucumber root development. Plant Physiol Biochem. 2021;169:119–126. doi:10.1016/j.plaphy.2021.11.007.
  • Yu Z, Xu Y, Liu L, Guo Y, Yuan X, Man X, Liu C, Yang G, Huang J, Yan K, et al. The importance of conserved serine for C-Terminally Encoded Peptides function exertion in Apple. Int J Mol Sci. 2019;20(3):775. doi:10.3390/ijms20030775.
  • Aggarwal S, Kumar A, Jain M, Sudan J, Singh K, Kumari S, Mustafiz A. C-terminally encoded peptides (CEPs) are potential mediators of abiotic stress response in plants. Physiol Mol Biol Plants. 2020;26(10):2019–2033. doi:10.1007/s12298-020-00881-4.
  • Xu R, Li Y, Sui Z, Lan T, Song W, Zhang M, Zhang Y, Xing J, . A C-terminal encoded peptide, ZmCEP1, is essential for kernel development in maize. J Exp Bot. 2021;72(15):5390–5406. doi:10.1093/jxb/erab224.
  • Zhang L, Ren Y, Xu Q, Wan Y, Zhang S, Yang G, Huang J, Yan K, Zheng C, Wu C. SiCEP3, a C-terminally encoded peptide from Setaria italica, promotes ABA import and signaling. J Exp Bot. 2021;72(18):6260–6273. doi:10.1093/jxb/erab267.
  • Imin N, Mohd-Radzman NA, Ogilvie HA, Djordjevic MA. The peptide-encoding CEP1 gene modulates lateral root and nodule numbers in Medicago truncatula. J Exp Bot. 2013;64:5395–5409.
  • Mohd-Radzman NA, Laffont C, Ivanovici A, Patel N, Reid D, Stougaard J, Djordjevic MA. Different pathways act downstream of the CEP peptide receptor CRA2 to regulate lateral root and nodule development. Plant Physiol. 2016;171(4):2536–2548. doi:10.1104/pp.16.00113.
  • Smith S, Zhu S, Joos L, Roberts I, Nikonorova N, Vu LD, Stes E, Cho H, Larrieu A, Xuan W, et al. The CEP5 peptide promotes abiotic stress tolerance, as revealed by quantitative proteomics, and attenuates the AUX/IAA equilibrium in Arabidopsis. Mol. Cell Proteomics. 2020;19(8):1248–1262. doi:10.1074/mcp.RA119.001826.
  • Tabata R, Sumida K, Yoshii T, Ohyama K, Shinohara H, Matsubayashi Y. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science. 2014;346(6207):343–346. doi:10.1126/science.1257800.
  • Ohkubo Y, Tanaka M, Tabata R, Ogawa-Ohnishi M, Matsubayashi Y. Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition. Nat Plants. 2017;3:17029. doi:10.1038/nplants.2017.29.
  • Ota R, Ohkubo Y, Yamashita Y, Ogawa-Ohnishi M, Matsubayashi Y. Shoot-to-root mobile CEPD-like 2 integrates shoot nitrogen status to systemically regulate nitrate uptake in Arabidopsis. Nat Commun. 2020;11(1):641. doi:10.1038/s41467-020-14440-8.
  • Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009;37:W202–W208.
  • Crooks GE, Hon G, Chandonia JM, Brenner SE. Weblogo: a sequence logo generator. Genome Res. 2004;14(6):1188–1190. doi:10.1101/gr.849004.
  • Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G. GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics. 2015;31(8):1296–1297. doi:10.1093/bioinformatics/btu817.
  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002;30(1):325–327. doi:10.1093/nar/30.1.325.
  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997;25(24):4876–4882. doi:10.1093/nar/25.24.4876.
  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K, . MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547–1549. doi:10.1093/molbev/msy096.
  • Greenham K, McClung CR. Integrating circadian dynamics with physiological processes in plants. Nat Rev Genet. 2015;16(10):598–610. doi:10.1038/nrg3976.
  • Greenham K, Sartor RC, Zorich S, Lou P, Mockler TC, McClung CR. Expansion of the circadian transcriptome in Brassica rapa and genome-wide diversification of paralog expression patterns. Elife. 2020;9:e58993. doi:10.7554/eLife.58993.
  • Pan W, You Y, Weng YN, Shentu JL, Lu Q, Xu QR, Liu HJ, Du ST. Zn stress facilitates nitrate transporter 1.1-mediated nitrate uptake aggravating Zn accumulation in Arabidopsis plants. Ecotoxicol Environ Saf. 2020;190:110104. doi:10.1016/j.ecoenv.2019.110104.
  • Mench MJ. Cadmium availability to plants in relation to major long-term changes in agronomy systems. Agric Ecosyst Environ. 1998;67:174–187. doi:10.1016/S0167-8809(97)00117-5.
  • Rizwan M, Ali S, Zia Ur Rehman M, Rinklebe J, Tsang DCW, Bashir A, Maqbool A, Tack FMG, Ok YS. Cadmium phytoremediation potential of Brassica crop species: a review. Sci Total Environ. 2018;631–632:1175–1191. doi:10.1016/j.scitotenv.2018.03.104.
  • Mhamdi A, Van Breusegem F. Reactive oxygen species in plant development. Development. 2018;145(15):dev164376. doi:10.1242/dev.164376.
  • Tang RJ, Wang C, Li K, Luan S. The CBL-CIPK calcium signaling network: unified paradigm from 20 years of discoveries. Trends Plant Sci. 2020;25(6):604–617. doi:10.1016/j.tplants.2020.01.009.
  • Tabata R, Sawa S. Maturation processes and structures of small secreted peptides in plants. Front Plant Sci. 2014;5:311. doi:10.3389/fpls.2014.00311.
  • Taleski M, Imin N, Djordjevic MA. CEP peptide hormones: key players in orchestrating nitrogen-demand signalling, root nodulation, and lateral root development. J Exp Bot. 2018;69(8):1829–1836. doi:10.1093/jxb/ery037.
  • Patel N, Mohd-Radzman NA, Corcilius L, Crossett B, Connolly A, Cordwell SJ, Ivanovici A, Taylor K, Williams J, Binos S, et al. Diverse peptide hormones affecting root growth identified in the Medicago truncatula secreted peptidome. Mol Cell Proteomics. 2018;17(1):160–174. doi:10.1074/mcp.RA117.000168.
  • Song XF, Guo P, Ren SC, Xu TT, Liu CM. Antagonistic peptide technology for functional dissection of CLV3/ESR genes in Arabidopsis. Plant Physiol. 2013;161:1076–1085. doi:10.1104/pp.112.211029.
  • Czyzewicz N, Wildhagen M, Cattaneo P, Stahl Y, Pinto KG, Aalen RB, Butenko MA, Simon R, Hardtke CS, De Smet I. Antagonistic peptide technology for functional dissection of CLE peptides revisited. J Exp Bot. 2015;66:5367–5374. doi:10.1093/jxb/erv284.
  • Rameneni JJ, Lee Y, Dhandapani V, Yu X, Choi SR, Oh MH, Lim YP, . Genomic and post-translational modification analysis of Leucine-Rich-Repeat receptor-like kinases in Brassica rapa. PLoS One. 2015;10(11):e0142255. doi:10.1371/journal.pone.0142255.
  • Chen G, Wang J, Wang H, Wang C, Tang X, Li J, Zhang L, Song J, Hou J, Yuan L. Genome-wide analysis of proline-rich extension like receptor protein kinase (PERK) in Brassica rapa and its association with the pollen development. BMC Genomics. 2020;21(1):401. doi:10.1186/s12864-020-06802-9.
  • Yang H, Bayer PE, Tirnaz S, Edwards D, Batley J. Genome-Wide identification and evolution of receptor-like kinases (RLKs) and receptor like proteins (RLPs) in Brassica juncea. Biology (Basel). 2020;10(1):17. doi:10.3390/biology10010017.
  • Mase K, Tsukagoshi H. Reactive oxygen species link gene regulatory networks during Arabidopsis root development. Front Plant Sci. 2021;12:660274. doi:10.3389/fpls.2021.660274.
  • Daudi A, Cheng Z, O’Brien JA, Mammarella N, Khan S, Ausubel FM, Bolwell GP. The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity. Plant Cell. 2012;24(1):275–287. doi:10.1105/tpc.111.093039.
  • Kadota Y, Shirasu K, Zipfel C. Regulation of the NADPH oxidase RBOHD during plant immunity. Plant Cell Physiol. 2015;56(8):1472–1480. doi:10.1093/pcp/pcv063.
  • Wang Y, Branicky R, Noë A, Hekimi S. Superoxide dismutases: dual roles in controlling ROS damage and regulating ROS signaling. J Cell Biol. 2018;217(6):1915–1928. doi:10.1083/jcb.201708007.