Asparagine-rich protein (NRP) mediates stress response by regulating biosynthesis of plant secondary metabolites in Arabidopsis

References

• Gong Z, Xiong L, Shi H, Yang S, Herrera-Estrella LR, Xu G, Chao D-Y, Li J, Wang P-Y, Qin F, et al. Plant abiotic stress response and nutrient use efficiency. Sci China Life Sci. 2020;63(5):635–8. doi:10.1007/s11427-020-1683-x.
   PubMed Web of Science ®Google Scholar
• Takahashi F, Kuromori T, Sato H, Shinozaki K. Regulatory gene networks in drought stress responses and resistance in plants. Adv Exp Med Biol. 2018;1081:189–214.
   PubMed Web of Science ®Google Scholar
• Ludwig AA, Tenhaken R. A new cell wall located N-rich protein is strongly induced during the hypersensitive response in Glycine max L. Eur J Plant Pathol. 2001;107(3):323–336. doi:10.1023/A:1011202225323.
   Web of Science ®Google Scholar
• Tenhaken R, Doerks T, Bork P. DCD – a novel plant specific domain in proteins involved in development and programmed cell death. BMC Bioinform. 2005;6(1):169. doi:10.1186/1471-2105-6-169.
   PubMedGoogle Scholar
• Yang Y, Liu X, Zhang W, Qian Q, Zhou L, Liu S, Li Y, Hou, X. Stress response proteins NRP1 and NRP2 are pro-survival factors that inhibit cell death during ER stress. Plant Physiol. 2021;187(3):1414–1427. doi:10.1093/plphys/kiab335.
   PubMed Web of Science ®Google Scholar
• Hoepflinger MC, Pieslinger AM, Tenhaken R. Investigations on N-rich protein (NRP) of Arabidopsis thaliana under different stress conditions. Plant Physiol Biochem. 2011;49(3):293–302. doi:10.1016/j.plaphy.2011.01.005.
   PubMed Web of Science ®Google Scholar
• Hetz C, Zhang K, Kaufman RJ. Mechanisms, regulation and functions of the unfolded protein response. Nat Rev Mol Cell Biol. 2020;21(8):421–438. doi:10.1038/s41580-020-0250-z.
   PubMed Web of Science ®Google Scholar
• Li Z, Tang J, Srivastava R, Bassham DC, Howell SH. The transcription factor bZIP60 links the unfolded protein response to the heat stress response in maize. Plant Cell. 2020;32(11):3559–3575. doi:10.1105/tpc.20.00260.
   PubMed Web of Science ®Google Scholar
• Locato V, De Gara L. Programmed cell death in plants: an overview. Methods Mol Biol. 2018;1743:1–8.
   PubMedGoogle Scholar
• Reis PA, Carpinetti PA, Freitas PP, Santos EGD, Camargos LF, Oliveira IHT, Silva JCF, Carvalho HH, Dal-Bianco M, Soares-Ramos JRL, et al. Functional and regulatory conservation of the soybean ER stress-induced DCD/NRP-mediated cell death signaling in plants. BMC Plant Biol. 2016;16(1):156. doi:10.1186/s12870-016-0843-z.
   PubMedGoogle Scholar
• Zhou R, Zhu T, Han L, Liu M, Xu M, Liu Y, Han D, Qiu D, Gong Q, Liu X, et al. The asparagine-rich protein NRP interacts with the Verticillium effector PevD1 and regulates the subcellular localization of cryptochrome 2. J Exp Bot. 2017;68(13):3427–3440. doi:10.1093/jxb/erx192.
   PubMed Web of Science ®Google Scholar
• Costa MD, Reis PA, Valente MA, Irsigler AST, Carvalho CM, Loureiro ME, Aragão FJL, Boston RS, Fietto LG, Fontes EPB, et al. A new branch of endoplasmic reticulum stress signaling and the osmotic signal converge on plant-specific asparagine-rich proteins to promote cell death. J Biol Chem. 2008;283(29):20209–20219. doi:10.1074/jbc.M802654200.
   PubMed Web of Science ®Google Scholar
• Genoud T, Buchala AJ, Chua NH, Métraux J-P. Phytochrome signalling modulates the SA-perceptive pathway in Arabidopsis. Plant J. 2002;31(1):87–95. doi:10.1046/j.1365-313X.2002.01338.x.
   PubMed Web of Science ®Google Scholar
• Griebel T, Zeier J. Light regulation and daytime dependency of inducible plant defenses in Arabidopsis: phytochrome signaling controls systemic acquired resistance rather than local defense. Plant Physiol. 2008;147(2):790–801. doi:10.1104/pp.108.119503.
   PubMed Web of Science ®Google Scholar
• Guo H, Yang H, Mockler TC, Lin C. Regulation of flowering time by Arabidopsis photoreceptors. Science. 1998;279(5355):1360–1363. doi:10.1126/science.279.5355.1360.
   PubMed Web of Science ®Google Scholar
• Hirayama T, Shinozaki K. Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J. 2010;61(6):1041–1052. doi:10.1111/j.1365-313X.2010.04124.x.
   PubMed Web of Science ®Google Scholar
• Zhu T, Wu Y, Yang X, Chen W, Gong Q, Liu X. The asparagine-rich protein NRP facilitates the degradation of the PP6-type phosphatase FyPP3 to promote ABA response in Arabidopsis. Mol Plant. 2018;11(2):257–268. doi:10.1016/j.molp.2017.11.006.
   PubMed Web of Science ®Google Scholar
• Reis PA, Fontes EP. N-rich protein (NRP)-mediated cell death signaling: a new branch of the ER stress response with implications for plant biotechnology. Plant Signal Behav. 2012;7(6):628–632. doi:10.4161/psb.20111.
   PubMed Web of Science ®Google Scholar
• Albertos P, Romero-Puertas MC, Tatematsu K, Mateos I, Sánchez-Vicente I, Nambara E, Lorenzo O. S-nitrosylation triggers ABI5 degradation to promote seed germination and seedling growth. Nat Commun. 2015;6(1):8669. doi:10.1038/ncomms9669.
   PubMedGoogle Scholar
• Belda-Palazon B, Rodriguez L, Fernandez MA, Castillo M-C, Anderson EM, Gao C, Gonzalez-Guzman M, Peirats-Llobet M, Zhao Q, De Winne N, et al. FYVE1/FREE1 interacts with the PYL4 ABA receptor and mediates its delivery to the vacuolar degradation pathway. Plant Cell. 2016;28(9):2291–2311. doi:10.1105/tpc.16.00178.
   PubMed Web of Science ®Google Scholar
• Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16(6):735–743. doi:10.1046/j.1365-313x.1998.00343.x.
   PubMed Web of Science ®Google Scholar
• Jiang Y, Duan Y, Yin J, Ye S, Zhu J, Zhang F, Lu W, Fan D, Luo K. Genome-wide identification and characterization of the Populus WRKY transcription factor family and analysis of their expression in response to biotic and abiotic stresses. J Exp Bot. 2014;65(22):6629–6644. doi:10.1093/jxb/eru381.
   PubMed Web of Science ®Google Scholar
• Chen C, Yao Y, Zhang L, Xu M, Jiang J, Dou T, Lin W, Zhao G, Huang M, Zhou Y, et al. A comprehensive analysis of the transcriptomes of marssonina brunnea and infected poplar leaves to capture vital events in host-pathogen interactions. PLoS One. 2015;10(7):e0134246. doi:10.1371/journal.pone.0134246.
   PubMed Web of Science ®Google Scholar
• Du Z, Zhou X, Ling Y, Zhang Z, Su Z. agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 2010;38(Web Server issue):W64–70. doi:10.1093/nar/gkq310.
   PubMedGoogle Scholar
• Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550. doi:10.1186/s13059-014-0550-8.
   PubMed Web of Science ®Google Scholar
• Tian T, Liu Y, Yan H, You Q, Yi X, Du Z, Xu W, Su Z. agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res. 2017;45(W1):W122–W129. doi:10.1093/nar/gkx382.
   PubMed Web of Science ®Google Scholar
• Nakashima K, Yamaguchi-Shinozaki K. ABA signaling in stress-response and seed development. Plant Cell Rep. 2013;32(7):959–970. doi:10.1007/s00299-013-1418-1.
   PubMed Web of Science ®Google Scholar
• Deschamps C, Simon JE. Phenylpropanoid biosynthesis in leaves and glandular trichomes of basil (Ocimum basilicum L.). Methods Mol Biol. 2010;643:263–273.
   PubMedGoogle Scholar
• Farag MA, Huhman DV, Dixon RA, Sumner LW. Metabolomics reveals novel pathways and differential mechanistic and elicitor-specific responses in phenylpropanoid and isoflavonoid biosynthesis in Medicago truncatula cell cultures. Plant Physiol. 2008;146(2):387–402. doi:10.1104/pp.107.108431.
   PubMed Web of Science ®Google Scholar
• Lee SH, Park YJ, Park SU, Lee S-W, Kim S-C, Jung C-S, Jang J-K, Hur Y, Kim YB. Expression of genes related to phenylpropanoid biosynthesis in different organs of ixeris dentata var. albiflora. Molecules. 2017;22(6):901. doi:10.3390/molecules22060901.
   PubMed Web of Science ®Google Scholar
• Mc CD, Neish AC. Metabolism of phenylpropanoid compounds in Salvia. II. Biosynthesis of phenolic cinnamic acids. Can J Biochem Physiol. 1959;37(4):537–547. doi:10.1139/y59-057.
   PubMedGoogle Scholar
• Wink M. Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry. 2003;64(1):3–19. doi:10.1016/S0031-9422(03)00300-5.
   PubMed Web of Science ®Google Scholar
• Yang L, Wen KS, Ruan X, Zhao Y-X, Wei F, Wang Q. Response of plant secondary metabolites to environmental factors. Molecules. 2018;23(4):762. doi:10.3390/molecules23040762.
   PubMed Web of Science ®Google Scholar
• Vogt T. Phenylpropanoid biosynthesis. Mol Plant. 2010;3(1):2–20. doi:10.1093/mp/ssp106.
   PubMed Web of Science ®Google Scholar
• Jin M, Zhang X, Zhao M, Deng M, Du Y, Zhou Y, Wang S, Tohge T, Fernie AR, Willmitzer L, et al. Integrated genomics-based mapping reveals the genetics underlying maize flavonoid biosynthesis. BMC Plant Biol. 2017;17(1):17. doi:10.1186/s12870-017-0972-z.
   PubMedGoogle Scholar
• War AR, Paulraj MG, War MY, Ignacimuthu S. Role of salicylic acid in induction of plant defense system in chickpea (Cicer arietinum L.). Plant Signal Behav. 2011;6(11):1787–1792. doi:10.4161/psb.6.11.17685.
   PubMedGoogle Scholar
• Higuchi T, Brown SA. Studies of lignin biosynthesis using isotopic carbon. XIII. The phenylpropanoid system in lignification. Can J Biochem Physiol. 1963;41(1):621–628. doi:10.1139/y63-074.
   PubMedGoogle Scholar
• Zhang H, Zhu J, Gong Z, Zhu J-K. Abiotic stress responses in plants. Nat Rev Genet. 2022;23(2):104–119. doi:10.1038/s41576-021-00413-0.
   PubMed Web of Science ®Google Scholar
• Saijo Y, Loo EP. Plant immunity in signal integration between biotic and abiotic stress responses. New Phytol. 2020;225(1):87–104. doi:10.1111/nph.15989.
   PubMed Web of Science ®Google Scholar
• Secic E, Kogel KH, Ladera-Carmona MJ. Biotic stress-associated microRNA families in plants. J Plant Physiol. 2021;263:153451. doi:10.1016/j.jplph.2021.153451.
   PubMed Web of Science ®Google Scholar
• Hartmann T. From waste products to ecochemicals: fifty years research of plant secondary metabolism. Phytochemistry. 2007;68(22–24):2831–2846. doi:10.1016/j.phytochem.2007.09.017.
   PubMed Web of Science ®Google Scholar
• Ramakrishna A, Ravishankar GA. Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav. 2011;6(11):1720–1731. doi:10.4161/psb.6.11.17613.
   PubMedGoogle Scholar
• Berini JL, Brockman SA, Hegeman AD, Reich PB, Muthukrishnan R, Montgomery RA, Forester JD. Combinations of abiotic factors differentially alter production of plant secondary metabolites in five woody plant species in the boreal-temperate transition zone. Front Plant Sci. 2018;9:1257. doi:10.3389/fpls.2018.01257.
   PubMed Web of Science ®Google Scholar
• Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM. Glucosinolate metabolites required for an Arabidopsis innate immune response. Science. 2009;323(5910):95–101. doi:10.1126/science.1164627.
   PubMed Web of Science ®Google Scholar
• Meihls LN, Handrick V, Glauser G, Barbier H, Kaur H, Haribal MM, Lipka AE, Gershenzon J, Buckler ES, Erb M, et al. Natural variation in maize aphid resistance is associated with 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one glucoside methyltransferase activity. Plant Cell. 2013;25(6):2341–2355. doi:10.1105/tpc.113.112409.
   PubMed Web of Science ®Google Scholar
• Mackenzie SA, Mullineaux PM, Teige M. Plant environmental sensing relies on specialized plastids. J Exp Bot. 2022;73(21):7155–7164. doi:10.1093/jxb/erac334.
   PubMed Web of Science ®Google Scholar
• Nicolas-Espinosa J, Garcia-Ibanez P, Lopez-Zaplana A, Yepes-Molina L, Albaladejo-Marico L, Carvajal M. Confronting secondary metabolites with water uptake and transport in plants under abiotic stress. Int J Mol Sci. 2023;24(3):2826. doi:10.3390/ijms24032826.
   PubMed Web of Science ®Google Scholar
• Wang JW, Wu JY. Effective elicitors and process strategies for enhancement of secondary metabolite production in hairy root cultures. Adv Biochem Eng Biotechnol. 2013;134:55–89.
   PubMed Web of Science ®Google Scholar
• Hartmann T. Plant-derived secondary metabolites as defensive chemicals in herbivorous insects: a case study in chemical ecology. Planta. 2004;219(1):1–4. doi:10.1007/s00425-004-1249-y.
   PubMed Web of Science ®Google Scholar
• Chinnusamy V, Schumaker K, Zhu JK. Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot. 2004;55(395):225–236. doi:10.1093/jxb/erh005.
   PubMed Web of Science ®Google Scholar
• Rejeb IB, Pastor V, Mauch-Mani B. Plant responses to simultaneous biotic and abiotic stress: molecular mechanisms. Plants (Basel). 2014;3(4):458–475. doi:10.3390/plants3040458.
   PubMedGoogle Scholar
• Wu Y, Chang Y, Luo L, Tian W, Gong Q, Liu, X. Abscisic acid employs NRP-dependent PIN2 vacuolar degradation to suppress auxin-mediated primary root elongation in Arabidopsis. New Phytol. 2022;233(1):297–312. doi:10.1111/nph.17783.
   PubMed Web of Science ®Google Scholar
• Yao T, Feng K, Xie M, Barros J, Tschaplinski TJ, Tuskan GA, Muchero W, Chen J-G. Phylogenetic occurrence of the phenylpropanoid pathway and lignin biosynthesis in plants. Front Plant Sci. 2021;12:704697. doi:10.3389/fpls.2021.704697.
   PubMed Web of Science ®Google Scholar
• Niklas KJ, Cobb ED, Matas AJ. The evolution of hydrophobic cell wall biopolymers: from algae to angiosperms. J Exp Bot. 2017;68(19):5261–5269. doi:10.1093/jxb/erx215.
   PubMed Web of Science ®Google Scholar
• Sharma A, Shahzad B, Rehman A, Bhardwaj R, Landi M, Zheng B. Response oF phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress. Molecules. 2019;24(13):2452. doi:10.3390/molecules24132452.
   PubMed Web of Science ®Google Scholar