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Current Genomics

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ISSN (Print): 1389-2029
ISSN (Online): 1875-5488

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Research Article

Study on Transcriptional Responses and Identification of Ribosomal Protein Genes for Potential Resistance against Brown Planthopper and Gall Midge Pests in Rice

Author(s): Mazahar Moin*, Anusree Saha , Achala Bakshi, Divya D., Madhav M.S. and Kirti P.B.

Volume 22, Issue 2, 2021

Published on: 19 February, 2021

Page: [98 - 110] Pages: 13

DOI: 10.2174/1389202922666210219113220

Price: $65

Abstract

Background: Our previous studies have revealed the roles of ribosomal protein (RP) genes in the abiotic stress responses of rice.

Methods: In the current investigation, we examine the possible involvement of these genes in insect stress responses. We have characterized the RP genes that included both Ribosomal Protein Large (RPL) and Ribosomal Protein Small (RPS) subunit genes in response to infestation by two economically important insect pests, the brown planthopper (BPH) and the Asian rice gall midge (GM) in rice. Differential transcript patterns of seventy selected RP genes were studied in a susceptible and a resistant genotype of indica rice: BPT5204 and RPNF05, respectively. An in silico analyses of the upstream regions of these genes also revealed the presence of cis-elements that are associated with wound signaling.

Results: We identified the genes that were up or downregulated in either one of the genotypes, or both of them after pest infestation. The transcript patterns of a majority of the genes were found to be temporally-regulated by both the pests. In the resistant RPNF05, BPH infestation activated RPL15, L51 and RPS5a genes while GM infestation induced RPL15, L18a, L22, L36.2, L38, RPS5, S9.2 and S25a at a certain point of time. These genes that were particularly upregulated in the resistant genotype, RPNF05, but not in BPT5204 suggest their potential involvement in plant resistance against either of the two pests studied.

Conclusion: Taken together, RPL15, L51, L18a, RPS5, S5a, S9.2, and S25a appear to be the genes with possible roles in insect resistance in rice.

Keywords: Ribosomal protein genes, brown planthopper, rice, gall midge pests, transcriptional response, resistance.

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[1]
Ehrlich, P.R.; Harte, J. Opinion: To feed the world in 2050 will require a global revolution. Proc. Natl. Acad. Sci. USA, 2015, 112(48), 14743-14744.
[http://dx.doi.org/10.1073/pnas.1519841112] [PMID: 26627228]
[2]
Das, G.; Patra, J.K.; Baek, K.H. Corrigendum: Insight into MAS: a molecular tool for development of stress resistant and quality of rice through gene stacking. Front. Plant Sci., 2017, 8, 1321.
[http://dx.doi.org/10.3389/fpls.2017.01321] [PMID: 28775736]
[3]
Prahalada, G.D.; Shivakumar, N.; Lohithaswa, H.C.; Sidde Gowda, D.K.; Ramkumar, G.; Kim, S.R.; Ramachandra, C.; Hittalmani, S.; Mohapatra, T.; Jena, K.K. Identification and fine mapping of a new gene, BPH31 conferring resistance to brown planthopper biotype 4 of India to improve rice, Oryza sativa L. Rice (N. Y.), 2017, 10(1), 41.
[http://dx.doi.org/10.1186/s12284-017-0178-x] [PMID: 28861736]
[4]
Bentur, J.S.; Rawat, N.; Divya, D.; Sinha, D.K.; Agarrwal, R.; Atray, I.; Nair, S. Rice–gall midge interactions: Battle for survival. J. Insect Physiol., 2016, 84, 40-49.
[http://dx.doi.org/10.1016/j.jinsphys.2015.09.008] [PMID: 26455891]
[5]
Du, B.; Chen, R.; Guo, J.; He, G. Current understanding of the genomic, genetic, and molecular control of insect resistance in rice. Mol. Breed., 2020, 40, 24.
[http://dx.doi.org/10.1007/s11032-020-1103-3]
[6]
Abdul Malik, N.A.; Kumar, I.S.; Nadarajah, K. Elicitor and Receptor Molecules: Orchestrators of Plant Defense and Immunity. Int. J. Mol. Sci., 2020, 21(3), 963.
[http://dx.doi.org/10.3390/ijms21030963] [PMID: 32024003]
[7]
Jones, J.D.; Dangl, J.L. The plant immune system. Nature, 2006, 444(7117), 323-329.
[http://dx.doi.org/10.1038/nature05286] [PMID: 17108957]
[8]
Dodds, P.N.; Rathjen, J.P. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet., 2010, 11(8), 539-548.
[http://dx.doi.org/10.1038/nrg2812] [PMID: 20585331]
[9]
Boller, T.; He, S.Y. Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science, 2009, 324(5928), 742-744.
[http://dx.doi.org/10.1126/science.1171647] [PMID: 19423812]
[10]
Tsuda, K.; Katagiri, F. Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr. Opin. Plant Biol., 2010, 13(4), 459-465.
[http://dx.doi.org/10.1016/j.pbi.2010.04.006] [PMID: 20471306]
[11]
Cui, H.; Tsuda, K.; Parker, J.E. Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol., 2015, 66, 487-511.
[http://dx.doi.org/10.1146/annurev-arplant-050213-040012] [PMID: 25494461]
[12]
Hatsugai, N.; Igarashi, D.; Mase, K.; Lu, Y.; Tsuda, Y.; Chakravarthy, S.; Wei, H.L.; Foley, J.W.; Collmer, A.; Glazebrook, J.; Katagiri, F. A plant effector-triggered immunity signaling sector is inhibited by pattern-triggered immunity. EMBO J., 2017, 36(18), 2758-2769.
[http://dx.doi.org/10.15252/embj.201796529] [PMID: 28811287]
[13]
Cartier, J.J.; Painter, R.H. Differential reactions of two biotypes of the corn leaf aphid to resistant and susceptible varieties, hybrids and selections of sorghums. J. Econ. Entomol., 1956, 49, 498-508.
[http://dx.doi.org/10.1093/jee/49.4.498]
[14]
Moss, T.; Langlois, F.; Gagnon-Kugler, T.; Stefanovsky, V. A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis. Cell. Mol. Life Sci., 2007, 64(1), 29-49.
[http://dx.doi.org/10.1007/s00018-006-6278-1] [PMID: 17171232]
[15]
Tschochner, H.; Hurt, E. Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol., 2003, 13(5), 255-263.
[http://dx.doi.org/10.1016/S0962-8924(03)00054-0] [PMID: 12742169 ]
[16]
Grummt, I. The nucleolus—guardian of cellular homeostasis and genome integrity. Chromosoma, 2013, 122(6), 487-497.
[http://dx.doi.org/10.1007/s00412-013-0430-0] [PMID: 24022641]
[17]
Sáez-Vásquez, J.; Delseny, M. Ribosome biogenesis in plants: from functional 45S ribosomal DNA organization to ribosome assembly factors. Plant Cell, 2019, 31(9), 1945-1967.
[http://dx.doi.org/10.1105/tpc.18.00874] [PMID: 31239391]
[18]
Ferreira-Cerca, S.; Hurt, E. Cell biology: Arrest by ribosome. Nature, 2009, 459(7243), 46-47.
[http://dx.doi.org/10.1038/459046a] [PMID: 19424147]
[19]
Kressler, D.; Hurt, E.; Baßler, J. Driving ribosome assembly. Biochimica Et Biophysica Acta (BBA)-. Molecular Cell Research, 1803, 2010, 673-683.
[20]
Ito, T.; Kim, G.T.; Shinozaki, K. Disruption of an Arabidopsis cytoplasmic ribosomal protein S13- homologous gene by transposon-mediated mutagenesis causes aberrant growth and development. Plant J., 2000, 22(3), 257-264.
[http://dx.doi.org/10.1046/j.1365-313x.2000.00728.x] [PMID: 10849343]
[21]
Yao, Y.; Ling, Q.; Wang, H.; Huang, H. Ribosomal proteins promote leaf adaxial identity. Development, 2008, 135(7), 1325-1334.
[http://dx.doi.org/10.1242/dev.017913] [PMID: 18305007]
[22]
Szakonyi, D.; Byrne, M.E. Ribosomal protein L27a is required for growth and patterning in Arabidopsis thaliana. Plant J., 2011, 65(2), 269-281.
[http://dx.doi.org/10.1111/j.1365-313X.2010.04422.x] [PMID: 21223391]
[23]
Falcone Ferreyra, M.L.F.; Pezza, A.; Biarc, J.; Burlingame, A.L.; Casati, P. Plant L10 ribosomal proteins have different roles during development and translation under ultraviolet-B stress. Plant Physiol., 2010, 153(4), 1878-1894.
[http://dx.doi.org/10.1104/pp.110.157057] [PMID: 20516338]
[24]
Kakehi, J.I.; Kawano, E.; Yoshimoto, K.; Cai, Q.; Imai, A.; Takahashi, T. Mutations in ribosomal proteins, RPL4 and RACK1, suppress the phenotype of a thermospermine-deficient mutant of Arabidopsis thaliana. PLoS One, 2015, 10(1)e0117309
[http://dx.doi.org/10.1371/journal.pone.0117309] [PMID: 25625317]
[25]
Zheng, M.; Wang, Y.; Liu, X.; Sun, J.; Wang, Y.; Xu, Y. Lv, J.; Long, W.; Zhu, X.; Guo, X.; Jiang, L.; Wang, C.; Wan, J. The RICE MINUTE-LIKE1 (RML1) gene, encoding a ribosomal large subunit protein L3B, regulates leaf morphology and plant architecture in rice. J. Exp. Bot., 2016, 67(11), 3457-3469.
[http://dx.doi.org/10.1093/jxb/erw167] [PMID: 27241493 ]
[26]
Byrne, M.E. A role for the ribosome in development. Trends Plant Sci., 2009, 14(9), 512-519.
[http://dx.doi.org/10.1016/j.tplants.2009.06.009] [PMID: 19716746]
[27]
Degenhardt, R.F.; Bonham-Smith, P.C. Arabidopsis ribosomal proteins RPL23aA and RPL23aB are differentially targeted to the nucleolus and are disparately required for normal development. Plant Physiol., 2008, 147(1), 128-142.
[http://dx.doi.org/10.1104/pp.107.111799] [PMID: 18322146]
[28]
Degenhardt, R.F.; Bonham-Smith, P.C. Evolutionary divergence of ribosomal protein paralogs in Arabidopsis. Plant Signal. Behav., 2008, 3(7), 493-495.
[http://dx.doi.org/10.4161/psb.3.7.5991]
[29]
Xiong, W.; Chen, X.; Zhu, C.; Zhang, J.; Lan, T. Arabidopsis ribosomal proteins RPL23aA and RPL23aB are functionally equivalent. BMC Plant Biol., 2020.
[30]
Giavalisco, P.; Wilson, D.; Kreitler, T.; Lehrach, H.; Klose, J.; Gobom, J.; Fucini, P. High heterogeneity within the ribosomal proteins of the Arabidopsis thaliana 80S ribosome. Plant Mol. Biol., 2005, 57(4), 577-591.
[http://dx.doi.org/10.1007/s11103-005-0699-3] [PMID: 15821981 ]
[31]
Carroll, A.J.; Heazlewood, J.L.; Ito, J.; Millar, A.H. Analysis of the Arabidopsis cytosolic ribosome proteome provides detailed insights into its components and their post-translational modification. Mol. Cell. Proteomics, 2008, 7(2), 347-369.
[http://dx.doi.org/10.1074/mcp.M700052-MCP200] [PMID: 17934214 ]
[32]
Sugihara, Y.; Honda, H.; Iida, T.; Morinaga, T.; Hino, S.; Okajima, T. Matsuda, T.; Nadano, D. Proteomic analysis of rodent ribosomes revealed heterogeneity including ribosomal proteins L10-like, L22-like 1, and L39-like. J. Proteome Res., 2010, 9(3), 1351-1366.
[http://dx.doi.org/10.1021/pr9008964] [PMID: 20063902 ]
[33]
Xue, S.; Barna, M. Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat. Rev. Mol. Cell Biol., 2012, 13(6), 355-369.
[http://dx.doi.org/10.1038/nrm3359] [PMID: 22617470 ]
[34]
Hummel, M.; Cordewener, J.H.; de Groot, J.C.; Smeekens, S.; America, A.H.; Hanson, J. Dynamic protein composition of Arabidopsis thaliana cytosolic ribosomes in response to sucrose feeding as revealed by label free MS E proteomics. Proteomics, 2012, 12(7), 1024-1038.
[http://dx.doi.org/10.1002/pmic.201100413] [PMID: 22522809]
[35]
Carroll, A.J. The Arabidopsis cytosolic ribosomal proteome: from form to function. Front. Plant Sci., 2013, 4, 32.
[http://dx.doi.org/10.3389/fpls.2013.00032] [PMID: 23459595 ]
[36]
Martinez-Seidel, F.; Beine-Golovchuk, O.; Hsieh, Y.C.; Kopka, J. Systematic review of plant ribosome heterogeneity and specialization. Front. Plant Sci., 2020, 11, 948.
[http://dx.doi.org/10.3389/fpls.2020.00948] [PMID: 32670337 ]
[37]
Komili, S.; Farny, N.G.; Roth, F.P.; Silver, P.A. Functional specificity among ribosomal proteins regulates gene expression. Cell, 2007, 131(3), 557-571.
[http://dx.doi.org/10.1016/j.cell.2007.08.037] [PMID: 17981122 ]
[38]
Moin, M.; Bakshi, A.; Saha, A.; Udaya Kumar, M.; Reddy, A.R.; Rao, K.V.; Siddiq, E.A.; Kirti, P.B. Activation tagging in indica rice identifies ribosomal proteins as potential targets for manipulation of water-use efficiency and abiotic stress tolerance in plants. Plant Cell Environ., 2016, 39(11), 2440-2459.
[http://dx.doi.org/10.1111/pce.12796] [PMID: 27411514]
[39]
Moin, M.; Bakshi, A.; Saha, A.; Dutta, M.; Madhav, S.M.; Kirti, P.B. Rice ribosomal protein large subunit genes and their spatio-temporal and stress regulation. Front. Plant Sci., 2016, 7, 1284.
[http://dx.doi.org/10.3389/fpls.2016.01284] [PMID: 27605933 ]
[40]
Saha, A.; Das, S.; Moin, M.; Dutta, M.; Bakshi, A.; Madhav, M.S.; Kirti, P.B. Genome-wide identification and comprehensive expression profiling of Ribosomal Protein Small Subunit (RPS) genes and their comparative analysis with the Large Subunit (RPL) genes in rice. Front. Plant Sci., 2017, 8, 1553.
[http://dx.doi.org/10.3389/fpls.2017.01553] [PMID: 28966624 ]
[41]
Sama, V.S.A.K.; Rawat, N.; Sundaram, R.M.; Himabindu, K.; Naik, B.S.; Viratamath, B.C.; Bentur, J.S. A putative candidate for the recessive gall midge resistance gene gm3 in rice identified and validated. Theor. Appl. Genet., 2014, 127(1), 113-124.
[http://dx.doi.org/10.1007/s00122-013-2205-7] [PMID: 24145853 ]
[42]
Divya, D.; Madhavi, K.R.; Dass, M.A.; Maku, R.V.; Mallikarjuna, G.; Sundaram, R.M.; Laha, G.S.; Padmakumari, A.P.; Patel, H.K.; Prasad, M.S.; Sonti, R.V.; Bentur, J.S. Expression profile of defense genes in rice lines pyramided with resistance genes against bacterial blight, fungal blast and insect gall midge. Rice (N.Y.), 2018, 11(1), 40.
[http://dx.doi.org/10.1186/s12284-018-0231-4] [PMID: 30006850]
[43]
Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Δ Δ C(T)) Method. Methods, 2001, 25((4)), 402-408.
[http://dx.doi.org/10.1006/meth.2001.1262] [PMID: 11846609]
[44]
Claeys, H.; Inzé, D. The agony of choice: how plants balance growth and survival under water-limiting conditions. Plant Physiol., 2013, 162(4), 1768-1779.
[http://dx.doi.org/10.1104/pp.113.220921] [PMID: 23766368 ]
[45]
Mazzucotelli, E.; Mastrangelo, A.M.; Crosatti, C.; Guerra, D.; Stanca, A.M.; Cattivelli, L. Abiotic stress response in plants: when post-transcriptional and post-translational regulations control transcription. Plant Sci., 2008, 174, 420-431.
[http://dx.doi.org/10.1016/j.plantsci.2008.02.005 ]
[46]
Nelson, C.J.; Millar, A.H. Protein turnover in plant biology. Nat. Plants, 2015, 1, 15017.
[http://dx.doi.org/10.1038/nplants.2015.1] [PMID: 27246884 ]
[47]
Pieterse, C.M.; Van der Does, D.; Zamioudis, C.; Leon-Reyes, A.; Van Wees, S.C. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol., 2012, 28, 489-521.
[http://dx.doi.org/10.1146/annurev-cellbio-092910-154055] [PMID: 22559264]
[48]
Cohen, S.P.; Leach, J.E. Abiotic and biotic stresses induce a core transcriptome response in rice. Sci. Rep., 2019, 9(1)6273
[http://dx.doi.org/10.1038/s41598-019-42731-8] [PMID: 31000746 ]
[49]
Bari, R.; Jones, J.D. Role of plant hormones in plant defence responses. Plant Mol. Biol., 2009, 69(4), 473-488.
[http://dx.doi.org/10.1007/s11103-008-9435-0] [PMID: 19083153 ]
[50]
Li, N.; Han, X.; Feng, D.; Yuan, D.; Huang, L.J. Signaling crosstalk between salicylic acid and ethylene/jasmonate in plant defense: do we understand what they are whispering? Int. J. Mol. Sci., 2019, 20(3), 671.
[http://dx.doi.org/10.3390/ijms20030671] [PMID: 30720746]
[51]
Smith, C.M.; Boyko, E.V. The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomol. Exp. Appl., 2007, 122, 1-6.
[http://dx.doi.org/10.1111/j.1570-7458.2006.00503.x]
[52]
Klessig, D.F.; Choi, H.W.; Dempsey, D.A. Systemic acquired resistance and salicylic acid: past, present and future. Mol. Plant Microbe Interact., 2018, 31(9), 871-888.
[http://dx.doi.org/10.1094/MPMI-03-18-0067-CR] [PMID: 29781762 ]
[53]
Deng, Y.; Zhu, X.; Shen, Y.; He, Z. Genetic characterization and fine mapping of the blast resistance locus Pigm (t) tightly linked to Pi2 and Pi9 in a broad-spectrum resistant Chinese variety. Theor. Appl. Genet., 2006, 113(4), 705-713.
[http://dx.doi.org/10.1007/s00122-006-0338-7] [PMID: 16832648]
[54]
Liu, C.; Hao, F.; Hu, J.; Zhang, W.; Wan, L.; Zhu, L. Tang, H.; He, G. Revealing different systems responses to brown planthopper infestation for pest susceptible and resistant rice plants with the combined metabonomic and gene-expression analysis. J. Proteome Res., 2010, 9(12), 6774-6785.
[http://dx.doi.org/10.1021/pr100970q] [PMID: 20936879 ]
[55]
Du, B.; Wei, Z.; Wang, Z.; Wang, X.; Peng, X.; Du, B. Chen, R.; Zhu, L.; He, G. Phloem-exudate proteome analysis of response to insect brown plant-hopper in rice. J. Plant Physiol., 2015, 183, 13-22.
[http://dx.doi.org/10.1016/j.jplph.2015.03.020] [PMID: 26072143]
[56]
Wang, H.; Ye, S.; Mou, T. Molecular breeding of rice restorer lines and hybrids for brown planthopper (BPH) resistance using the Bph14 and Bph15 genes. Rice (N.Y.), 2016, 9(1), 53.
[http://dx.doi.org/10.1186/s12284-016-0126-1] [PMID: 27704482 ]
[57]
Tong, X.; Qi, J.; Zhu, X.; Mao, B.; Zeng, L.; Wang, B.; Li, Q.; Zhou, G.; Xu, X.; Lou, Y.; He, Z. The rice hydroperoxide lyase OsHPL3 functions in defense responses by modulating the oxylipin pathway. Plant J., 2012, 71(5), 763-775.
[http://dx.doi.org/10.1111/j.1365-313X.2012.05027.x] [PMID: 22519706 ]
[58]
Pathak, M.D.; Saxena, R.C. Insect resistance in crop plants. Commentaries Plant Sci., 2013, 2, 2-61.
[59]
Wei, Z.; Hu, W.; Lin, Q.; Cheng, X.; Tong, M.; Zhu, L. Chen, R.; He, G. Understanding rice plant resistance to the Brown Planthopper (Nilaparvata lugens): A proteomic approach. Proteomics, 2009, 9(10), 2798-2808.
[http://dx.doi.org/10.1002/pmic.200800840] [PMID: 19405033]
[60]
Douglas, A.E. Strategies for enhanced crop resistance to insect pests. Annu. Rev. Plant Biol., 2018, 69, 637-660.
[http://dx.doi.org/10.1146/annurev-arplant-042817-040248] [PMID: 29144774]
[61]
Wang, J.; Lan, P.; Gao, H.; Zheng, L.; Li, W.; Schmidt, W. Expression changes of ribosomal proteins in phosphate-and iron-deficient Arabidopsis roots predict stress-specific alterations in ribosome composition. BMC Genomics, 2013, 14(1), 783.
[http://dx.doi.org/10.1186/1471-2164-14-783] [PMID: 24225185 ]
[62]
Falcone Ferreyra, M.L.F.; Casadevall, R.; Luciani, M.D.; Pezza, A.; Casati, P. New evidence for differential roles of l10 ribosomal proteins from Arabidopsis. Plant Physiol., 2013, 163(1), 378-391.
[http://dx.doi.org/10.1104/pp.113.223222] [PMID: 23886624 ]
[63]
Kim, K.Y.; Park, S.W.; Chung, Y.S.; Chung, C.H.; Kim, J.I.; Lee, J.H. Molecular cloning of low-temperature-inducible ribosomal proteins from soybean. J. Exp. Bot., 2004, 55(399), 1153-1155.
[http://dx.doi.org/10.1093/jxb/erh125] [PMID: 15020631 ]
[64]
Genuth, N.R.; Barna, M. The discovery of ribosome heterogeneity and its implications for gene regulation and organismal life. Mol. Cell, 2018, 71(3), 364-374.
[http://dx.doi.org/10.1016/j.molcel.2018.07.018] [PMID: 30075139]
[65]
Whittle, C.A.; Krochko, J.E. Transcript profiling provides evidence of functional divergence and expression networks among ribosomal protein gene paralogs in Brassica napus. Plant Cell, 2009, 21(8), 2203-2219.
[http://dx.doi.org/10.1105/tpc.109.068411] [PMID: 19706795 ]
[66]
Sormani, R.; Masclaux-Daubresse, C.; Daniele-Vedele, F.; Chardon, F. Transcriptional regulation of ribosome components are determined by stress according to cellular compartments in Arabidopsis thaliana. PLoS One, 2011, , 6.(12)e28070
[http://dx.doi.org/10.1371/journal.pone.0028070] [PMID: 22164228 ]
[67]
Ghulam, M.M.; Catala, M.; Abou Elela, S. Differential expression of duplicated ribosomal protein genes modifies ribosome composition in response to stress. Nucleic Acids Res., 2020, 48(4), 1954-1968.
[http://dx.doi.org/10.1093/nar/gkz1183 ] [PMID: 31863578 ]
[68]
Moin, M.; Bakshi, A.; Madhav, M.S.; Kirti, P.B. Expression profiling of ribosomal protein gene family in dehydration stress responses and characterization of transgenic rice plants overexpressing RPL23A for water-use efficiency and tolerance to drought and salt stresses. Front Chem., 2017, 5, 97.
[http://dx.doi.org/10.3389/fchem.2017.00097] [PMID: 29184886 ]
[69]
León, J.; Rojo, E.; Sánchez-Serrano, J.J. Wound signalling in plants. J. Exp. Bot., 2001, 52(354), 1-9.
[http://dx.doi.org/10.1093/jxb/52.354.1] [PMID: 11181708 ]
[70]
Gerst, J.E. Pimp my ribosome: ribosomal protein paralogs specify translational control. Trends Genet., 2018, 34(11), 832-845.
[http://dx.doi.org/10.1016/j.tig.2018.08.004] [PMID: 30195580 ]
[71]
Yang, C.; Zang, W.; Ji, Y.; Li, T.; Yang, Y.; Zheng, X. Ribosomal protein L6 (RPL6) is recruited to DNA damage sites in a poly (ADP-ribose) polymerase–dependent manner and regulates the DNA damage response. J. Biol. Chem., 2019, 294(8), 2827-2838.
[http://dx.doi.org/10.1074/jbc.RA118.007009] [PMID: 30598506]
[72]
Yu, J.; Hu, S.; Ma, K.; Sun, L.; Hu, H.; Zou, F. ; Guo, Q.; Lei, Z.; Zhou, D.; Sun, Y.; Zhang, D.; Ma, L.; Shen, B.; Zhu, C. Ribosomal protein S29 regulates metabolic insecticide resistance through binding and degradation of CYP6N3. PLoS One, 2014, 9(4)e94611
[http://dx.doi.org/10.1371/journal.pone.0094611] [PMID: 24728095 ]
[73]
Liu, X.D.; Xie, L.; Wei, Y.; Zhou, X.; Jia, B.; Liu, J.; Zhang, S. Abiotic stress resistance, a novel moonlighting function of ribosomal protein RPL44 in the halophilic fungus Aspergillus glaucus. Appl. Environ. Microbiol., 2014, 80(14), 4294-4300.
[http://dx.doi.org/10.1128/AEM.00292-14] [PMID: 24814782 ]
[74]
Zhu, F.; Zhou, Y.K.; Ji, Z.L.; Chen, X.R. The plant ribosome-inactivating proteins play important roles in defense against pathogens and insect pest attacks. Front. Plant Sci., 2018, 9, 146.
[http://dx.doi.org/10.3389/fpls.2018.00146] [PMID: 29479367 ]
[75]
Panda, N.; Heinrichs, E.A. Levels of tolerance and antibiosis in rice varieties having moderate resistance to the brown planthopper, Nilaparvata lugens (Stål)(Hemiptera: Delphacidae). Environ. Entomol., 1983, 12, 1204-1214.
[http://dx.doi.org/10.1093/ee/12.4.1204]

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