Abstract
The developing seed of soybean is susceptible to high temperature and humidity (HTH) stress, resulting in pre-harvest seed deterioration in the field. Many genes are found to respond to the stress. Based on our previous proteomics study, an HTH-responsive gene, GmCDPKSK5, was isolated from soybean seed. GmCDPKSK5 encodes a cytoplasm- and membrane-associated protein, which belongs to Group I of the CDPK family. By yeast two-hybrid (Y2H) from soybean seed cDNA library, GmTCTP was screened as a GmCDPKSK5-interacting protein. The interaction between GmCDPKSK5 and GmTCTP was further verified using bimolecular fluorescence complementation and GST pull down assays. Expression levels of both GmCDPKSK5 and GmTCTP were induced by HTH stress in soybean seed. Our results indicated that GmCDPKSK5 and GmTCTP interact with each other and may function in responses to HTH stress in soybean developing seed.
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Abbreviations
- BiFC:
-
Bimolecular fluorescence complementation
- CDPK:
-
Calcium dependent protein kinases
- CV:
-
Cultivar
- GFP:
-
Green fluorescent protein
- GST:
-
Glutathione S-transferase
- HTH:
-
High temperature and humidity
- ORF:
-
Open reading frame
- PCR:
-
Polymerase chain reaction
- qRT-PCR:
-
Quantitative reverse transcription PCR
- TCTP:
-
Translationally controlled tumor protein
- Y2H:
-
Yeast two-hybrid
- YFP:
-
Yellow fluorescent protein
References
Anil VS, Harmon AC, Rao KS (2003) Temporal association of Ca2+-dependent protein kinase with oil bodies during seed development in Santalum album L.: its biochemical characterization and significance. Plant Cell Physiol 44:367–376
Asano T, Hakata M, Nakamura H, Aoki N, Komatsu S, Ichikawa H, Hirochika H, Ohsugi R (2011) Functional characterization of OsCPK21, a calcium-dependent protein kinase that confers salt tolerance in rice. Plant Mol Biol 75:179–191
Asano T, Hayashi N, Kobayashi M, Aoki N, Miyao A, Mitsuhara I, Ichikawa H, Komatsu S, Hirochika H, Kikuchi S, Ohsugi R (2012) A rice calcium-dependent protein kinase OsCPK12 oppositely modulates salt-stress tolerance and blast disease resistance. Plant J 69:26–36
Bommer UA, Thiele BJ (2004) The translationally controlled tumour protein (TCTP). Int J Biochem Cell Biol 36:379–385
Bommer UA, Lazaris-Karatzas A, de Benedetti A, Nürnberg P, Benndorf R, Bielka H, Sonenberg N (1994) Translational regulation of the mammalian growth-related protein P23: involvement of eIF-4E. Cell Mol Biol Res 40:633–641
Boudsocq M, Sheen J (2013) CDPKs in immune and stress signaling. Trends Plant Sci 18:30–40
Brioudes F, Thierry AM, Chambrier P, Mollereau B, Bendahmane M (2010) Translationally controlled tumor protein is a conserved mitotic growth integrator in animals and plants. Proc Natl Acad Sci USA 107:16384–16389
Campo S, Baldrich P, Messeguer J, Lalanne E, Coca M, San Segundo B (2014) Overexpression of a calcium-dependent protein kinase confers salt and drought tolerance in rice by preventing membrane lipid peroxidation. Plant Physiol 165:688–704
Cao BH, Lei JJ, Chen GJ, Zeng GP, Meng CM (2006) Isolation and expression analysis of the gene encoding translationally controlled tumor protein (TCTP) in Cabbage. J Agric Biotechnol 14:996–997 (Chinese)
Chang WJ, Su HS, Li WJ, Zhang ZL (2009) Expression profiling of a novel calcium-dependent protein kinase gene, LeCPK2, from tomato (Solanum lycopersicum) under heat and pathogen-related hormones. Biosci Biotechnol Biochem 73:2427–2431
Chen S, Liu GS, Wang YY, Sun YH, Chen J (2011) Cloning of a calcium-dependent protein kinase gene NtCDPK12, and its induced expression by high-salt and drought in Nicotiana tabacum. Agric Sci China 10: 1851–1860
Cheng SH, Willmann MR, Chen HC, Sheen J (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469–485
Choi HI, Park HJ, Park JH, Kim S, Im MY, Seo HH, Kim YW, Hwang I, Kim SY (2005) Arabidopsis calcium-dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity. Plant Physiol 139:1750–1761
Citovsky V, Lee LY, Vyas S, Glick E, Chen MH, Vainstein A, Gafni Y, Gelvin SB, Tzfira T (2006) Subcellular localization of interacting proteins by bimolecular fluorescence complementation in Planta. J Mol Biol 362:1120–1131
Davletova S, Mészáros T, Miskolczi P, Oberschall A, Török K, Magyar Z, Dudits D, Deák M (2001) Auxin and heat shock activation of a novel member of the calmodulin like domain protein kinase gene family in cultured alfalfa cells. J Exp Bot 52:215–221
Dornbos DLJ, Mullen RE (1991) Influence of stress during soybean seed fill on seed weight, germination and seedling growth rate. Can J Plant Sci 71:373–383
Egli DB, TeKrony DM, Heitholt JJ, Rupe J (2005) Air temperature during seed filling and soybean seed germination and vigor. Crop Sci 45:1329–1335
Ermolayev V, Weschke W, Manteuffel R (2003) Comparison of Al-induced gene expression in sensitive and tolerant soybean cultivars. J Exp Bot 54:2745–2756
Franz S, Ehlert B, Liese A, Kurth J, Cazalé AC, Romeis T (2011) Calcium-dependent protein kinase CPK21 functions in abiotic stress response in Arabidopsis thaliana. Mol Plant 4: 83–96.
Frattini M, Morello L, Breviario D (1999) Rice calcium-dependent protein kinase isoforms OsCDPK2 and OsCDPK11 show different responses to light and different expression patterns during seed development. Plant Mol Biol 41:753–764
Geiger D, Scherzer S, Mumm P, Marten I, Ache P, Matschi S, Liese A, Wellmann C, Al-Rasheid KA, Grill E, Romeis T, Hedrich R (2010) Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proc Natl Acad Sci USA 107:8023–8028
Geng S, Zhao Y, Tang L, Zhang R, Sun M, Guo H, Kong X, Li A, Mao L (2011) Molecular evolution of two duplicated CDPK genes CPK7 and CPK12 in grass species: A case study in wheat (Triticum aestivum L.). Gene 475:94–103
Gibson LR, Mullen RE (1999) Soybean seed quality reductions by high day and night temperature. Crop Sci 36:1615–1619
Gnanasekar M, Thirugnanam S, Zheng G, Chen A, Ramaswamy K (2009) Gene silencing of translationally controlled tumor protein (TCTP) by siRNA inhibitscell growth and induces apoptosis of human prostate cancer cells. Int J Oncol 34:1241–1246
Gross B, Gaestel M, Böhm H, Bielka H (1989) cDNA sequence coding for a translationally controlled human tumor protein. Nucleic Acids Res 17:8367
Harmon AC, Putnam-Evans C, Cormier MJ (1987) A calcium-dependent but calmodulin-independent protein kinase from soybean. Plant Physiol 83:830–837
Harper JF, Sussman MR, Schaller GE, Putnam-Evans C, Charbonneau H, Harmon AC (1991) A calcium-dependent protein kinase with a regulatory domain similar to calmodulin. Science 252:951–954
Hettenhausen C, Sun G, He Y, Zhuang H, Sun, Qi J, Wu J (2016) Genome-wide identification of calcium-dependent protein kinases in soybean and analyses of their transcriptional responses to insect herbivory and drought stress. Sci Rep 06: 1–14
Jaworski K, Szmidt-Jaworska A, Kopcewicz J (2011) Two calcium dependent protein kinases are differently regulated by light and have different activity patterns during seedling growth in Pharbitis nil. Plant Growth Regul 65:369–379
Jiang S, Zhang D, Wang L, Pan J, Liu Y, Kong X, Zhou Y, Li D (2013) A maize calcium-dependent protein kinase gene, ZmCPK4, positively regulated abscisic acid signaling and enhanced drought stress tolerance in transgenic Arabidopsis. Plant Physiol Biochem 71:112–120
Keigley PJ, Mullen RE (1986) Changes in soybean seed quality from high temperature during seed fill and maturation. Crop Sci 26:1212–1216
Kong X, Lv W, Jiang S, Zhang D, Cai G, Pan J, Li D (2013) Genome-wide identification and expression analysis of calcium-dependent protein kinase in maize. BMC Genomics 14:433
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
Lee JH, Rho SB, Park SY, Chun T (2008) Interaction between fortil in and transforming growth factor-beta stimulated clone-22 (TSC-22) prevents apoptosis via the destabilization of TSC-22. FEBS Lett 582:1210–1218
Lei P, He Q, He F, Wu Q, Pan G (2015) Cloning of mulberry translationally controlled tumor protein (TCTP) gene and expressional variation under temperature stress. Sci Seric 41: 0405–0409 (in Chinese)
Li AL, Zhu YF, Tan XM, Wang X, Wei B, Guo HZ, Zhang ZL, Chen XB, Zhao GY, Kong XY, Jia JZ, Mao L (2008) Evolutionary and functional study of the CDPK gene family in wheat (Triticum aestivum L.). Plant Mol Biol 66:429–443
Liu H, Peng HW, Cheng YS, Yuan HS, Yang-Yen HF (2005) Stabilization and enhancement of the antiapoptotic activity of Mcl-1 by TCTP. Mol Cell Biol 25:3117–3126
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
Ma SY, Wu WH (2007) AtCPK23 functions in Arabidopsis responses to drought and salt stresses. Plant Mol Biol 65:511–518
Mak CH, Su KW, Ko RC (2001) Identification of some heat-induced genes of Trichinella spiralis. Parasitology 123:293–300
Morello L, Frattini M, Gianì S, Christou P, Breviario D (2000) Overexpression of the calcium-dependent protein kinase OsCDPK2 in transgenic rice is repressed by light in leaves and disrupts seed development. Transgenic Res 9:453–462
Ndimande BN, Wien HC, Kueneman EA (1981) Soybean seed deterioration in the tropics. I. The role of physiological factors and fungal pathogens. Field Crops Res 4:113–121
Nelson BK, Cai X, Nebenführ A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51:1126–1136
Patharkar OR,·Cushman JC (2006) A novel coiled-coil protein co-localizes and interacts with a calcium-dependent protein kinase in the common ice plant during low-humidity stress. Planta 225:57–73
Patharkar OR,·Cushman JC (2000) A stress-induced calcium-dependent protein kinase from Mesembryanthemum crystallinum phosphorylates a two component pseudo-response regulator. Plant J 24:679–691
Pay A, Heberle-Bors E, Hirt H (1992) An alfalfa cDNA encodes a protein with homology to translationally controlled human tumor protein. Plant Mol Biol 19:501–503
Ray S, Agarwal P, Arora R, Kapoor S, Tyagi AK (2007) Expression analysis of calcium-dependent protein kinase gene family during reproductive development and abiotic stress conditions in rice (Oryza sativa L. ssp. indica). Mol Genet Genomics 278:493–505
Rho SB, Lee JH, Park MS, Byun HJ, Kang S, Seo SS, Kim JY, Park SY (2011) Anti-apoptotic protein TCTP controls the stability of the tumor suppressor p53. FEBS Lett 585:29–35
Rieping M, Schöffl F (1992) Synergistic effect of upstream sequences, CCAAT box elements, and HSE sequences for enhanced expression of chimaeric heat shock genes in transgenic tobacco. Mol Gen Genet 231:226–232
Romeis T, Ludwig AA, Martin R, Jones JD (2001) Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J 20:5556–5567
Sage-Ono K, Ono M, Harada H, Kamada H (1998) Dark-induced accumulation of mRNA for a homolog of translationally controlled tumor protein (TCTP) in Pharbitis. Plant Cell Physiol 39:357–360
Saha RR, Sultana W (2008) Influence of seed ageing on growth and yield of soybean. Bangladesh J Bot 37:21–26
Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K (2000) Over-expression of a single Ca2+-dependent protein kinase cofers both cold and salt/drought tolerance on rice plant. Plant J 23:319–327
Saijo Y, Kinoshita N, Ishiyama K, Hata S, Kyozuka J, Hayakawa T, Nakamura T, Shimamoto K, Yamaya T, Izui K (2001) A Ca2+-dependent protein kinase that endows rice plants with cold- and salt-stress tolerance functions in vascular bundles. Plant Cell Physiol 42:1228–1233
Shi J, Kim KN, Ritz O, Albrecht V, Gupta R, Harter K, Luan S, Kudla J (1999) Novel protein kinases associated with calcineurin B-like calcium sensors in Arabidopsis. Plant Cell 11:2393–2405
Shu Y, Tao Y, Wang S, Huang L, Yu X, Wang Z, Chen M, Gu W, Ma H (2015) GmSBH1, a homeobox transcription factor gene, related to growth and development and involves in response to high temperature and humidity stress in soybean. Plant Cell Rep 34:1927–1937
Susini L, Besse S, Duflaut D, Lespagnol A, Beekman C, Fiucci G, Atkinson AR, Busso D, Poussin P, Marine JC, Martinou JC, Cavarelli J, Moras D, Amson R, Telerman A (2008) TCTP protects from apoptotic cell death by antagonizing bax function. Cell Death Differ 15:1211–1220
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis Version 6.0. Mol Biol Evol 30:2725–2729
Thomas G, Thomas G, Luther H (1981) Transcriptional and translational control of cytoplasmic proteins after serum stimulation of quiescent Swiss 3T3 cells. Proc Natl Acad Sci USA 78:5712–5716
Urao T, Katagiri T, Mizoguchi T, Yamaguchi-Shinozaki K, Hayashida N, Shinozaki K (1994) Two genes that encode Ca2+-dependent protein kinases are induced by drought and high-salt stresses in Arabidopsis thaliana. Mol Gen Genet 244:331–340
Vincent D, Ergül A, Bohlman MC, Tattersall EA, Tillett RL, Wheatley MD, Woolsey R, Quilici DR, Joets J, Schlauch K, Schooley DA, Cushman JC, Cramer GR (2007) Proteomic analysis reveals differences between Vitis vinifera L. cv. Chardonnay and cv. Cabernet Sauvignon and their responses to water deficit and salinity. J Exp Bot 58:1873–1892
Wan B, Lin Y, Mou T (2007) Expression of rice Ca2+-dependent protein kinases (CDPKs) genes under different environmental stresses. FEBS Lett 581:1179–1189
Wang F, Wang LQ, Tian X, Gu WH, Ma H (2007) Pre-harvest and post-harvest seed deterioration resistance of spring soybean germplasm in south China. Scientia Agri Sinica 40: 2637–2647 (in Chinese)
Wang LQ, Ma H, Song LR, Shu Y, Gu W (2012) Comparative proteomics analysis reveals the mechanism of pre-harvest seed deterioration of soybean under high temperature and humidity stress. J Proteom 75:2109–2127
Weckwerth P, Ehlert B, Romeis T (2015) ZmCPK1, a calciumin-independent kinase member of the Zea mays CDPK gene family, functions as a negative regulator in cold stress signalling. Plant Cell Environ 38:544–558
Wei S, Hu W, Deng X, Zhang Y, Liu X, Zhao X, Luo Q, Jin Z, Li Y, Zhou S, Sun T, Wang L, Yang G, He G (2014) A rice calcium-dependent protein kinase OsCPK9 positively regulates drought stress tolerance and spikelet fertility. BMC Plant Biol 14:133
Xu J, Tian YS, Peng RH, Xiong AS, Zhu B, Jin XF, Gao F, Fu XY, Hou XL, Yao QH (2010) AtCPK6, a functionally redundant and positive regulator involved in salt/drought stress tolerance in Arabidopsis. Planta 231:1251–1260
Yang Y, Yang F, Xiong Z, Yan Y, Wang X, Nishino M, Mirkovic D, Nguyen J, Wang H, Yang XF (2005) An N-terminal region of translationally controlled tumor protein is required for its antiapoptotic activity. Oncogene 24:4778–4788
Yenofsky R, Bergmann I, Brawerman G (1982) Messenger RNA species partially in a repressed state in mouse sarcoma ascites cells. Proc Natl Acad Sci USA 79:5876–5880
Yenofsky R, Cereghini S, Krowczynska A, Brawerman G (1983) Regulation of mRNA utilization in mouse erythroleukemia cells induced to differentiate by exposure to dimethyl sulfoxide. Mol Cell Biol 3:1197–1203
Yoon GM, Cho HS, Ha HJ, Liu JR, Lee HS (1999) Characterization of NtCDPK1, a calcium-dependent protein kinase gene in Nicotiana tabacum, and the activity of its encoded protein. Plant Mol Biol 39:991–1001
Zanakis GN, Ellis RH, Summerfield RJ (1994) A comparison of changes in vigour among three genotypes of soybean (Glycine max) during seed development and maturation in three temperature regimes. Exp Agric 30: 157–170
Zarkadas CG, Gagnon C, Gleddie S, Khanizadeh S, Cober ER, Guillemette RJD (2007) Assessment of the protein quality of fourteen soybean [Glycine max (L.) Merr.] cultivars using amino acid analysis and two-dimensional electrophoresis. Food Res Int 40:129–146
Zhang M, Liang S, Lu YT (2005) Cloning and functional characterization of NtCPK4, a new tobacco calcium-dependent protein kinase. Biochim Biophys Acta 1729: 174–185
Zhao R, Sun HL, Mei C, Wang XJ, Yan L, Liu R, Zhang XF, Wang XF, Zhang DP (2001a) The Arabidopsis Ca2+-dependent protein kinase CPK12 negatively regulates abscisic acid signaling in seed germination and post-germination growth. New Phytol 192:61–73
Zhao R, Wang XF, Zhang DP (2011b) CPK12: a Ca2+-dependent protein kinase balancer in abscisic acid signaling. Plant Signal Behav 6:1687–1690
Zhao R, Sun HL, Zhao N, Jing X, Shen X, Chen S (2015) The Arabidopsis Ca2+-dependent protein kinase CPK27 is required for plant response to salt-stress. Gene 563:203–214
Zheng M, Wang Y, Wang Y, Wang C, Ren Y, Lv J, Peng C, Wu T, Liu K, Zhao S, Liu X, Guo X, Jiang L, Terzaghi W, Wan J (2015) DEFORMED FLORAL ORGAN1 (DFO1) regulates floral organ identity by epigenetically repressing the expression of OsMADS58 in rice (Oryza sativa). New Phytol 206:1476–1490
Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, Du SY, Wang XF, Wu FQ, Xu YH, Zhang XY, Zhang DP (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019–3036
Zou JJ, Wei FJ, Wang C, Wu JJ, Ratnasekera D, Liu WX, Wu WH (2010) Arabidopsis calcium-dependent protein kinase CPK10 functions in abscisic acid- and Ca2+-mediated stomatal regulation in response to drought stress. Plant Physiol 154:1232–1243
Zou JJ, Li XD, Ratnasekera D, Wang C, Liu WX, Song LF, Zhang WZ, Wu WH (2015) Arabidopsis CALCIUM-DEPENDENT PROTEIN KINASE8 and CATALASE3 function in abscisic acid-mediated signaling and H2O2 homeostasis in stomatal guard cells under drought stress. Plant Cell 27:1445–1460
Acknowledgements
We gratefully acknowledge the partial financial support from the projects supported by the Shanghai Committee of Agriculture, China [Hu (2013), No. 1–2], The National Natural Science Foundation of China (30971840, 31171572, 31371711, 31671772), the Specialized Research Fund for the Doctoral Program of Higher Education of China (20100097110030, 20120097110025), and the Agriculture Science and Technology Fund of the Ministry of Science and Technology, China (02EFN216901241, 04EFN213100094) for this research.
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Wang, S., Tao, Y., Zhou, Y. et al. Translationally controlled tumor protein GmTCTP interacts with GmCDPKSK5 in response to high temperature and humidity stress during soybean seed development. Plant Growth Regul 82, 187–200 (2017). https://doi.org/10.1007/s10725-017-0250-y
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DOI: https://doi.org/10.1007/s10725-017-0250-y