Abstract
FK506-binding proteins (FKBPs), which belong to the peptidyl-prolyl cis/trans isomerase superfamily, are involved in plant response to abiotic stresses. A number of FKBP family genes have been isolated in plants, but little has been reported of FKBP genes in maize. In this study, a drought-induced FKBP gene, ZmFKBP20-1, was isolated from maize and was characterized for its role in stress responses using gene expression, protein subcellular localization, transformation in Arabidopsis, expression patterns of the stress-responsive genes, and physiological parameter analysis. During drought and salt stresses, ZmFKBP20-1 transgenic Arabidopsis plants exhibited enhanced tolerance, which was concomitant with the altered expression of stress/ABA-responsive genes, such as COR15a, COR47, ERD10, RD22, KIN1, ABI1, and ABI2. The resistance characteristics of ZmFKBP20-1 overexpression were associated with a significant increase in survival rate. These results suggested that ZmFKBP20-1 plays a positive role in drought and salt stress responses in Arabidopsis and provided new insights into the mechanisms of FKBP in response to abiotic stresses in plants.
Similar content being viewed by others
Abbreviations
- COR15a:
-
(cold-regulated gene 15a)
- COR47:
-
(cold-regulated gene 47)
- ERD10:
-
(early responsive to dehydration 10)
- RD22:
-
(responsive to dehydration 22)
- KIN1:
-
(kinase 1)
- BI1:
-
(ABA-insensitive 1)
- ABI2:
-
(ABA-insensitive 2)
- RAB18:
-
(ABA-responsive gene 18)
- Murashigeand Skoog:
-
(MS)
References
Aghdasi B, Ye K, Resnick A, Huang A, Ha HC, Guo X, Dawson TM, Dawson VL, Snyder SH (2001) FKBP12, the 12-kDa FK506- binding protein, is a physiologic regulator of the cell cycle. Proc Natl Acad Sci U S A 98:2425–2430
Agredano-Moreno LT, Reyes de la Cruz H, Martinez-Castilla LP, Sanchez de Jimenez E (2007) Distinctive expression and functional regulation of the maize (Zea mays L.) TOR kinase ortholog. Molecular bioSystems 3:794–802
Ahn JC, Kim DW, You YN, Seok MS, Park JM, Hwang H, Kim BG, Luan S, Park HS, Cho HS (2010) Classification of rice (Oryza sativa L. Japonica nipponbare) immunophilins (FKBPs, CYPs) and expression patterns under water stress. BMC Plant Biology 10:253
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Aviezer-Hagai K, Skovorodnikova J, Galigniana M, Farchi-Pisanty O, Maayan E, Bocovza S, Efrat Y, von Koskull-Doring P et al. (2007) Arabidopsis immunophilins ROF1 (AtFKBP62) and ROF2 (AtFKBP65) exhibit tissue specificity, are heat-stress induced, and bind HSP90. Plant Mol Biol 63:237–255
Bailly A, Sovero V, Vincenzetti V, Santelia D, Bartnik D, Koenig BW, Mancuso S, Martinoia E, Geisler M (2008) Modulation of P-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins. J Biol Chem 283:21817–21826
Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24:701–713
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39:205–207
Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signaling. J Exp Bot 65:1229–1240
Bierer BE, Somers PK, Wandless TJ, Burakoff SJ, Schreiber SL (1990) Probing immunosuppressant action with a nonnatural immunophilin ligand. Science 250:556–559
Blecher O, Erel N, Callebaut I, Aviezer K, Breiman A (1996) A novel plant peptidyl-prolyl-cis-trans-isomerase (PPIase): cDNA cloning, structural analysis, enzymatic activity and expression. Plant Mol Biol 32:493–504
Bouchard R, Bailly A, Blakeslee JJ, Oehring SC, Vincenzetti V, Lee OR, Paponov I, Palme K, Mancuso S, Murphy AS, Schulz B, Geisler M (2006) Immunophilin-like TWISTED DWARF1 modulates auxin efflux activities of Arabidopsis P-glycoproteins. J Biol Chem 281:30603–30612
Breiman A, Camus I (2002) The involvement of mammalian and plant FK506-binding proteins (FKBPs) in development. Transgenic Res 11:321–335
Choi HW, Kim YJ, Lee SC, Hong JK, Hwang BK (2007) Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defense response to bacterial pathogens. Plant Physiol 145:890–904
Crespo JL, Diaz-Troya S, Florencio FJ (2005) Inhibition of target of rapamycin signaling by rapamycin in the unicellular green alga Chlamydomonas reinhardtii. Plant Physiol 139:1736–1749
Dwivedi RS, Breiman A, Herman EM (2003) Differential distribution of the cognate and heat-stress-induced isoforms of high Mr cistrans prolyl peptidyl isomerase (FKBP) in the cytoplasm and nucleoplasm. J Exp Bot 54:2679–2689
Galat A (2000) Sequence diversification of the FK506-binding proteins in several different genomes. Eur J Biochem 267:4945–4959
Gao Y, Jiang W, Dai Y, Xiao N, Zhang C, Li H, Lu Y, Wu M, Tao X, Deng D, Chen J (2015) A maize phytochrome-interacting factor 3 improves drought and salt stress tolerance in rice. Plant Mol Biol 87:413–428
Geisler M, Bailly A (2007) Tete-a-tete: the function of FKBPs in plant development. Trends in Plant Science 12:465–473
Gollan PJ, Bhave M (2010) Genome-wide analysis of genes encoding FK506-binding proteins in rice. Plant Mol Biol 72:1–16
Gollan PJ, Bhave M, Aro EM (2012) The FKBP families of higher plants: Exploring the structures and functions of protein interaction specialists. FEBS Letters 586:3539–3547
Gopalan G, He Z, Balmer Y, Romano P, Gupta R, Heroux A, Buchanan BB, Swaminathan K, Luan S (2004) Structural analysis uncovers a role for redox in regulating FKBP13, an immunophilin of the chloroplast thylakoid lumen. Proc Natl Acad Sci U S A 101:13945–13950
Harding MW, Galat A, Uehling DE, Schreiber SL (1989) A receptor for the immunosuppressant FK506 is a cis-trans peptidyl-prolyl isomerase. Nature 341:758–760
He Z, Li L, Luan S (2004) Immunophilins and parvulins. Superfamily of peptidyl prolyl isomerases in Arabidopsis. Plant Physiol 134:1248–1267
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125:189–198
Heitman J, Movva NR, Hall MN (1992) Proline isomerases at the crossroads of protein folding, signal transduction, and immunosuppression. The New Biologist 4:448–460
Hueros G, Rahfeld J, Salamini F, Thompson R (1998) A maize FK506-sensitive immunophilin, mzFKBP-66, is a peptidylproline cis-trans-isomerase that interacts with calmodulin and a 36-kDa cytoplasmic protein. Planta 205:121–131
Ingram J, Bartels D (1996) The Molecular Basis of Dehydration Tolerance in Plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403
Kamphausen T, Fanghanel J, Neumann D, Schulz B, Rahfeld JU (2002) Characterization of Arabidopsis thaliana AtFKBP42 that is membrane-bound and interacts with Hsp90. Plant J 32:263–276
Kang CB, Hong Y, Dhe-Paganon S, Yoon HS (2008) FKBP family proteins: immunophilins with versatile biological functions. Neuro-Signals 16:318–325
Kurek I, Aviezer K, Erel N, Herman E, Breiman A (1999) The wheat peptidyl prolyl cis-trans-isomerase FKBP77 is heat induced and developmentally regulated. Plant Physiol 119:693–704
Kurek I, Dulberger R, Azem A, Tzvi BB, Sudhakar D, Christou P, Breiman A (2002a) Deletion of the C-terminal 138 amino acids of the wheat FKBP73 abrogates calmodulin binding, dimerization and male fertility in transgenic rice. Plant Mol Biol 48:369–381
Kurek I, Stöger E, Dulberger R, Christou P, Breiman A (2002b) Overexpression of the wheat FK506-binding protein 73 (FKBP73) and the heat-induced wheat FKBP77 in transgenic wheat reveals different functions of the two isoforms. Transgenic Research 11:373–379
Kurkela S, Franck M (1990) Cloning and characterization of a coldand ABA-inducible Arabidopsis gene. Plant Mol Biol 15:137–144
Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2DNA binding domain separate two cellular signal transduction pathways in drought- and lowtemperature- responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406
Luan S, Albers MW, Schreiber SL (1994) Light-regulated, tissuespecific immunophilins in a higher plant. Proc Natl Acad Sci U S A 91:984–988
Meiri D, Breiman A (2009) Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90.1 and affecting the accumulation of HsfA2-regulated sHSPs. Plant J 59:387–399
Meiri D, Tazat K, Cohen-Peer R, Farchi-Pisanty O, Aviezer-Hagai K, Avni A, Breiman A (2010) Involvement of Arabidopsis ROF2 (FKBP65) in thermotolerance. Plant Mol Biol 72:1912203
Menand B, Desnos T, Nussaume L, Berger F, Bouchez D, Meyer C, Robaglia C (2002) Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. Proc Natl Acad Sci U S A 99:642226427
Mercado D, Renard ME, Maraite H, Duveiller E, Rasmussen JB, Friesen TL, Ali S Chlorophyll content and chlorophyll fluorescence as indicators of resilience to temperature stress in wheat and its relationship with resistance to Bipolaris sorokiniana. In: Proceedings of Fourth International Wheat Tan Spot and Spot Blotch Workshop, Bemidji, Minnesota, USA, 21–24 July, 2002, 2003
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7:405–410
Nakashima K, Fujita Y, Kanamori N, Katagiri T, Umezawa T, Kidokoro S, Maruyama K, Yoshida T, Ishiyama K, Kobayashi M, Shinozaki K, Yamaguchi-Shinozaki K (2009) Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol 50:1345–1363
Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148
Nigam N, Singh A, Sahi C, Chandramouli A, Grover A (2008) SUMO-conjugating enzyme (Sce) and FK506-binding protein (FKBP) encoding rice (Oryza sativa L.) genes: genome-wide analysis, expression studies and evidence for their involvement in abiotic stress response. Mol Gen Genet 279:371–383
Perez-Perez JM, Ponce MR, Micol JL (2004) The ULTRACURVATA2 gene of Arabidopsis encodes an FK506-binding protein involved in auxin and brassinosteroid signaling. Plant Physiol 134:101–117
Reddy RK, Kurek I, Silverstein AM, Chinkers M, Breiman A, Krishna P (1998) High-molecular-weight FK506-binding proteins are components of heat-shock protein 90 heterocomplexes in wheat germ lysate. Plant Physiol 118:1395–1401
Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stressresponsive gene expression. Proc Natl Acad Sci U S A 103: 18822–18827
Seki M, Ishida J, Narusaka M, Fujita M, Nanjo T, Umezawa T, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Shinozaki K (2002a) Monitoring the expression pattern of around 7,000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Funct Integr Genomics 2:282–291
Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002b) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292
Seok MS, You YN, Park HJ, Lee SS, Aigen F, Luan S, Ahn JC, Cho HS (2014) AtFKBP16-1, a chloroplast lumenal immunophilin, mediates response to photosynthetic stress by regulating PsaL stability. Physiol Plant 150:620–631
Shinozaki K, Yamaguchi-Shinozaki K (1996) Molecular responses to drought and cold stress. Curr Opin Biotechnol 7:161–167
Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227
Siekierka JJ, Staruch MJ, Hung SH, Sigal NH (1989) FK-506, a potent novel immunosuppressive agent, binds to a cytosolic protein which is distinct from the cyclosporin A-binding protein, cyclophilin. J Immunol 143:1580–1583
Smyczynski C, Roudier F, Gissot L, Vaillant E, Grandjean O, Morin H, Masson T, Bellec Y, Geelen D, Faure JD (2006) The C terminus of the immunophilin PASTICCINO1 is required for plant development and for interaction with a NAC-like transcription factor. J Biol Chem 281:25475–25484
Somarelli JA, Herrera RJ (2007) Evolution of the 12 kDa FK506- binding protein gene. Biol Cell 99:311–321
Sun J, Jiang H, Xu Y, Li H, Wu X, Xie Q, Li C (2007) The CCCHtype zinc finger proteins AtSZF1 and AtSZF2 regulate salt stress responses in Arabidopsis. Plant Cell Physiol 48:1148–1158
Szekely G, Abraham E, Cseplo A, Rigo G, Zsigmond L, Csiszar J, Ayaydin F, Strizhov N, Jasik J, Schmelzer E, Koncz C, Szabados L (2008) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J 53:11–28
Vespa L, Vachon G, Berger F, Perazza D, Faure JD, Herzog M (2004) The immunophilin-interacting protein AtFIP37 from Arabidopsis is essential for plant development and is involved in trichome endoreduplication. Plant Physiol 134:1283–1292
Vucich VA, Gasser CS (1996) Novel structure of a high molecular weight FK506 binding protein from Arabidopsis thaliana. Mol Gen Genet 252:510–517
Wang B, Bailly A, Zwiewka M, Henrichs S, Azzarello E, Mancuso S, Maeshima M, Friml J, Schulz A, Geisler M (2013) Arabidopsis TWISTED DWARF1 functionally interacts with auxin exporter ABCB1 on the root plasma membrane. Plant Cell 25:202–214
Wang C, Jing R, Mao X, Chang X, Li A (2011) TaABC1, a member of the activity of bc1 complex protein kinase family from common wheat, confers enhanced tolerance to abiotic stresses in Arabidopsis. J Exp Bot 62:1299–1311
Weber H, Chetelat A, Reymond P, Farmer EE (2004) Selective and powerful stress gene expression in Arabidopsis in response to malondialdehyde. Plant J 37:877–888
Wu L, Zu X, Zhang H, Wu L, Xi Z, Chen Y (2015) Overexpression of ZmMAPK1 enhances drought and heat stress in transgenic Arabidopsis thaliana. Plant Mol Biol 88:429–443
Xu DB, Gao SQ, Ma YZ, Xu ZS, Zhao CP, Tang YM, Li XY, Li LC, Chen YF, Chen M (2014) ABI-like transcription factor gene TaABL1 from wheat improves multiple abiotic stress tolerances in transgenic plants. Funct Integr Genomics 14:717–730
Yu Y, Li Y, Li L, Lin J, Zheng C, Zhang L (2009) Overexpression of PwTUA1, a pollen-specific tubulin gene, increases pollen tube elongation by altering the distribution of alpha-tubulin and promoting vesicle transport. J Exp Bot 60:2737–2749
Yu Y, Zhang H, Li W, Mu C, Zhang F, Wang L, Meng Z (2012) Genome-wide analysis and environmental response profiling of the FK506-binding protein gene family in maize (Zea mays L.). Gene 498:212–222
Zhao Y, Ma Q, Jin X, Peng X, Liu J, Deng L, Yan H, Sheng L, Jiang H, Cheng B (2014) A novel maize homeodomain-leucine zipper (HD-Zip) I gene, Zmhdz10, positively regulates drought and salt tolerance in both rice and Arabidopsis. Plant Cell Physiol 55:1142–1156
Zhou W, Zhou T, Li MX, Zhao CL, Jia N, Wang XX, Sun YZ, Li GL, Xu M, Zhou RG, Li B (2012) The Arabidopsis J-protein AtDjB1 facilitates thermotolerance by protecting cells against heat-induced oxidative damage. New Phytol1 94:364–378
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Yu, Y., Li, Y., Jia, F. et al. ZmFKBP20-1 improves the drought and salt tolerance of transformed Arabidopsis. J. Plant Biol. 60, 558–570 (2017). https://doi.org/10.1007/s12374-017-0262-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12374-017-0262-1