Abstract
Receptor for activated C kinase 1 (RACK1) is a conserved scaffold protein interacting with multiple proteins and participates in diverse cellular activities. Previous high-throughput transcriptome and proteome studies both identified RACK1 gene/protein was differentially expressed in cotton, however, the detailed function of RACK1 in this important fiber-producing plant is still unclear. In the current study, we found that GhRACK1 was preferentially expressed in fast growing tissues, such as cotton fibers and ovules. Down-regulation of GhRACK1 expression in cotton plants through virus-induced gene silencing (VIGS) and ectopic expression of GhRACK1 in Arabidopsis both revealed a positive correlation between GhRACK1 expression level and plant growth rate. Physiological index (protein and soluble sugar content) further indicated that down-regulation of GhRACK1 expression could inhibit protein synthesis and photoassimilate accumulation in cotton, whereas ectopic expression of GhRACK1 exhibited opposite effects in Arabidopsis. These data collectively suggested that GhRACK1 might play an important role in regulating the growth and development of cotton plants.
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References
Adams DR, Ron D, Kiely PA (2011) RACK1, a multifaceted scaffolding protein: structure and function. Cell Commun Signal 9:22
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Chen JG, Ullah H, Temple B, Liang J, Guo J, Alonso JM, Ecker JR, Jones AM (2006) RACK1 mediates multiple hormone responsiveness and developmental processes in Arabidopsis. J Exp Bot 57:2697–2708
Cheng D, Qian W, Wang Y, Meng M, Wei L, Li Z, Kang L, Peng J, Xia Q (2014) Nuclear import of transcription factor BR-C is mediated by its interaction with RACK1. PLoS ONE 9:e109111
Deng T, Yao H, Wang J, Wang J, Xue H, Zuo K (2016) GhLTPG1, a cotton GPI-anchored lipid transfer protein, regulates the transport of phosphatidylinositol monophosphates and cotton fiber elongation. Sci Rep 6:26829
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Feng H, Li X, Chen H, Deng J, Zhang C, Liu J, Wang T, Zhang X, Dong J (2018) GhHUB2, a ubiquitin ligase, is involved in cotton fiber development via the ubiquitin-26S proteasome pathway. J Exp Bot 69:5059–5075
Guo J, Chen JG (2008) RACK1 genes regulate plant development with unequal genetic redundancy in Arabidopsis. BMC Plant Biol 8:108
Guo J, Wang J, Xi L, Huang WD, Liang J, Chen JG (2009) RACK1 is a negative regulator of ABA responses in Arabidopsis. J Exp Bot 60:3819–3833
Guo J, Wang S, Valerius O, Hall H, Zeng Q, Li JF, Weston DJ, Ellis BE, Chen JG (2011) Involvement of Arabidopsis RACK1 in protein translation and its regulation by abscisic acid. Plant Physiol 155:370–383
Guo K, Du X, Tu L, Tang W, Wang P, Wang M, Liu Z, Zhang X (2016) Fibre elongation requires normal redox homeostasis modulated by cytosolic ascorbate peroxidase in cotton (Gossypium hirsutum). J Exp Bot 67:3289–3301
Hu G, Koh J, Yoo MJ, Grupp K, Chen S, Wendel JF (2013) Proteomic profiling of developing cotton fibers from wild and domesticated Gossypium barbadense. New Phytol 200:570–582
Ishida S, Takahashi Y, Nagata T (1993) Isolation of cDNA of an auxin-regulated gene encoding a G protein beta subunit-like protein from tobacco BY-2 cells. Proc Natl Acad Sci USA 90:11152–11156
Islas-Flores T, Guillén G, Alvarado-Affantranger X, Lara-Flores M, Sánchez F, Villanueva MA (2011) PvRACK1 loss-of-function impairs cell expansion and morphogenesis in Phaseolus vulgaris L. root nodules. Mol Plant Microb Interact 24:819–826
Islas-Flores T, Rahman A, Ullah H, Villanueva MA (2015) The receptor for activated C Kinase in plant signaling: tale of a promiscuous little molecule. Front Plant Sci 6:1090
Jannot G, Bajan S, Giguère NJ, Bouasker S, Banville IH, Piquet S, Hutvagner G, Simard MJ (2011) The ribosomal protein RACK1 is required for microRNA function in both C. elegans and humans. EMBO Rep 12:581–586
Jin F, Hu L, Yuan D, Xu J, Gao W, He L, Yang X, Zhang X (2014) Comparative transcriptome analysis between somatic embryos (SEs) and zygotic embryos in cotton: evidence for stress response functions in SE development. Plant Biotechnol J 12:161–173
Kundu N, Dozier U, Deslandes L, Somssich IE, Ullah H (2013) Arabidopsis scaffold protein RACK1A interacts with diverse environmental stress and photosynthesis related proteins. Plant Signal Behav 8:e24012
Li HB, Qin YM, Pang Y, Song WQ, Mei WQ, Zhu YX (2007) A cotton ascorbate peroxidase is involved in hydrogen peroxide homeostasis during fibre cell development. New Phytol 175:462–471
Li Y, Wang NN, Wang Y, Liu D, Gao Y, Li L, Li XB (2018) The cotton XLIM protein (GhXLIM6) is required for fiber development via maintaining dynamic F-actin cytoskeleton and modulating cellulose biosynthesis. Plant J 96:1269–1282
Liu YV, Baek JH, Zhang H, Diez R, Cole RN, Semenza GL (2007) RACK1 competes with HSP90 for binding to HIF-1α and is required for O2-independent and HSP90 inhibitor-induced degradation of HIF-1α. Mol Cell 25:207–217
Liu Y, Kang T, Cheng J, Yi Y, Han J, Chen H, Li Q, Tang N, Liang M (2020) Heterologous expression of the metallothionein PpMT2 gene from Physcomitrella patens confers enhanced tolerance to heavy metal stress on transgenic Arabidopsis plants. Plant Growth Regul 90:63–72
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆Ct method. Methods 25:402–408
Nakashima A, Chen L, Thao NP, Fujiwara M, Wong HL, Kuwano M, Umemura K, Shirasu K, Kawasaki T, Shimamoto K (2008) RACK1 functions in rice innate immunity by interacting with the Rac1 immune complex. Plant Cell 20:2265–2279
Nilsson J, Sengupta J, Frank J, Nissen P (2004) Regulation of eukaryotic translation by the RACK1 protein: a platform for signalling molecules on the ribosome. EMBO Rep 5:1137–1141
Okano K, Schnaper HW, Bomsztyk K, Hayashida T (2006) RACK1 binds to Smad3 to modulate transforming growth factor-β1-stimulated α2(I) collagen transcription in renal tubular epithelial cells. J Biol Chem 281:26196–26204
Omosigho NN, Swaminathan K, Plomann M, Müller-Taubenberger A, Noegel AA, Riyahi TY (2014) The Dictyostelium discoideum RACK1 orthologue has roles in growth and development. Cell Commun Signal 12:37
Pang CY, Wang H, Pang Y, Xu C, Jiao Y, Qin YM, Western TL, Yu SX, Zhu YX (2010) Comparative proteomics indicates that biosynthesis of pectic precursors is important for cotton fiber and Arabidopsis root hair elongation. Mol Cell Proteomics 9:2019–2033
Ron D, Chen CH, Caldwell J, Jamieson L, Orr E, Mochly-Rosen D (1994) Cloning of an intracellular receptor for protein kinase C: a homolog of the beta subunit of G proteins. Proc Natl Acad Sci USA 91:839–843
Speth C, Willing EM, Rausch S, Schneeberger K, Laubinger S (2013) RACK1 scaffold proteins influence miRNA abundance in Arabidopsis. Plant J 76:433–445
Sun W, Gao Z, Wang J, Huang Y, Chen Y, Li J, Lv M, Wang J, Luo M, Zuo K (2019) Cotton fiber elongation requires the transcription factor GhMYB212 to regulate sucrose transportation into expanding fibers. New Phytol 222:864–881
Sundaramoorthy E, Leonard M, Mak R, Liao J, Fulzele A, Bennett EJ (2017) ZNF598 and RACK1 regulate mammalian ribosome-associated quality control function by mediating regulatory 40S ribosomal ubiquitylation. Mol Cell 65:751–760
Tang W, Tu L, Yang X, Tan J, Deng F, Hao J, Guo K, Lindsey K, Zhang X (2014) The calcium sensor GhCaM7 promotes cotton fiber elongation by modulating reactive oxygen species (ROS) production. New Phytol 202:509–520
Urano D, Czarnecki O, Wang X, Jones AM, Chen JG (2015) Arabidopsis receptor of activated C kinase1 phosphorylation by with no lysine 8 kinase. Plant Physiol 167:507–516
Wamaitha MJ, Yamamoto R, Wong HL, Kawasaki T, Kawano Y, Shimamoto K (2012) OsRap2.6 transcription factor contributes to rice innate immunity through its interaction with Receptor for Activated Kinase-C 1 (RACK1). Rice 5:35
Wang B, Yu J, Zhu D, Chang Y, Zhao Q (2014) Maize ZmRACK1 is involved in the plant response to fungal phytopathogens. Int J Mol Sci 15:9343–9359
Wang XC, Li Q, Jin X, Xiao GH, Liu GJ, Liu NJ, Qin YM (2015) Quantitative proteomics and transcriptomics reveal key metabolic processes associated with cotton fiber initiation. J Proteomics 114:16–27
Wang W, Wang X, Wang X, Ahmed S, Hussain S, Zhang N, Ma Y, Wang S (2019) Integration of RACK1 and ethylene signaling regulates plant growth and development in Arabidopsis. Plant Sci 280:31–40
Wu Z, Yang Y, Huang G, Lin J, Xia Y, Zhu Y (2017) Cotton functional genomics reveals global insight into genome evolution and fiber development. J Genet Genomics 44:511–518
Wu C, Zhou B (2018) Characterization of a sterile dwarf mutant and the cloning of zeaxanthin epoxidase in Asian cotton (Gossypium arboreum L.). Plant Growth Regul 85:57–72
Wu H, Tian Y, Wan Q, Fang L, Guan X, Chen J, Hu Y, Ye W, Zhang H, Guo W, Chen X, Zhang T (2018) Genetics and evolution of MIXTA genes regulating cotton lint fiber development. New Phytol 217:883–895
Yao D, Zhang X, Zhao X, Liu C, Wang C, Zhang Z, Zhang C, Wei Q, Wang Q, Yan H, Li F, Su Z (2011) Transcriptome analysis reveals salt-stress-regulated biological processes and key pathways in roots of cotton (Gossypium hirsutum L.). Genomics 98:47–55
Yoo MJ, Wendel JF (2014) Comparative evolutionary and developmental dynamics of the cotton (Gossypium hirsutum) fiber transcriptome. PLoS Genet 10:e1004073
Zhang B, Yang YW, Zhang Y, Liu JY (2013) A high-confidence reference dataset of differentially expressed proteins in elongating cotton fiber cells. Proteomics 13:1159–1163
Zhang D, Chen L, Li D, Lv B, Chen Y, Chen J, Yan X, Liang J (2014) OsRACK1 is involved in abscisic acid- and H2O2-mediated signaling to regulate seed germination in rice (Oryza sativa L.). PLoS One 9:e97120
Zhang B, Liu JY (2016) Cotton cytosolic pyruvate kinase GhPK6 participates in fast fiber elongation regulation in a ROS-mediated manner. Planta 244:915–926
Zhang B, Du SJ, Hu J, Miao D, Liu JY (2016) Comparative proteomic analyses of Asian cotton ovules with attached fibers in the early stages of fiber elongation process. Proteome Sci 14:13
Zhang Z, Ruan YL, Zhou N, Wang F, Guan X, Fang L, Shang X, Guo W, Zhu S, Zhang T (2017) Suppressing a putative sterol carrier gene reduces plasmodesmal permeability and activates sucrose transporter genes during cotton fiber elongation. Plant Cell 29:2027–2046
Zhang D, Wang Y, Shen J, Yin J, Li D, Gao Y, Xu W, Liang J (2018) OsRACK1A, encodes a circadian clock-regulated WD40 protein, negatively affect salt tolerance in rice. Rice 11:45
Zhang J, Yang Z, Feng P, Zhong X, Ma Q, Su Q, Wang X, Li C, Yang Y (2019) Identification and the potential roles of long non-coding RNAs in cotton leaves damaged by Aphis gossypii. Plant Growth Regul 88:215–225
Zhou M, Sun G, Sun Z, Tang Y, Wu Y (2014) Cotton proteomics for deciphering the mechanism of environment stress response and fiber development. J Proteomics 105:74–84
Zhu YN, Shi DQ, Ruan MB, Zhang LL, Meng ZH, Liu J, Yang WC (2013) Transcriptome analysis reveals crosstalk of responsive genes to multiple abiotic stresses in cotton (Gossypium hirsutum L.). PLoS ONE 8:e80218
Acknowledgements
We are grateful to Professor Jin-Yuan Liu at Tsinghua University for providing constructive comments on the experiments and manuscript.
Funding
This work was supported by Grants from the China Postdoctoral Science Foundation (2014M550074) and State Key Laboratory of Cotton Biology Open Fund (CB2015A01).
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Zhang B designed the experiments and wrote the manuscript. Shu FZ and Wang BS conducted the experiments and analyzed the data. Liu DL and Wang XS participated in the experiments and help to write the manuscript. All authors read and approved the final manuscript.
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10725_2020_610_MOESM2_ESM.xlsx
Table S2. Information on the six RACK1-like genes in upland cotton (Gossypium hirsutum L.). Supplementary Material 2. (XLSX 10 kb)
10725_2020_610_MOESM5_ESM.tif
Figure S3. Phylogenetic relationship (A), gene structure (B) and protein domain (C) of six RACK1-like genes from upland cotton and three RACK1 genes from Arabidopsis. Supplementary Material 5. (TIF 2800 kb)
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Shu, F., Wang, B., Liu, D. et al. Functional characterization of a receptor for activated C kinase 1 (RACK1) gene from upland cotton (Gossypium hirsutum L.). Plant Growth Regul 91, 359–369 (2020). https://doi.org/10.1007/s10725-020-00610-7
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DOI: https://doi.org/10.1007/s10725-020-00610-7