Abstract
Recent discoveries show that TIFY family genes are plant-specific genes involved in the response to several abiotic stresses, also acting as key regulators of jasmonate signaling in Arabidopsis thaliana. However, there is limited information about this gene family in wild soybean, nor is its role in plant bicarbonate stress adaptation completely understood. Here, we isolated and characterized a novel TIFY family gene, GsTIFY10, from Glycine soja. GsTIFY10 could be induced by bicarbonate, salinity stress and the phytohormone JA, both in the leaves and roots of wild soybean. Over-expression of GsTIFY10 in Arabidopsis resulted in enhanced plant tolerance to bicarbonate stress during seed germination, early seedling and adult seedling developmental stages, and the expression levels of some bicarbonate stress response and stress-inducible marker genes were significantly higher in the GsTIFY10 overexpression lines than in wild-type plants. It was also found that GsTIFY10 could repress JA signal transduction. The roots of plants overexpressing GsTIFY10 grew longer than wild-type in the presence of MeJA, and some JA response and JA biosynthesis marker genes were suppressed in the GsTIFY10 overexpression lines. Subcellular localization studies using a GFP fusion protein showed that GsTIFY10 is localized to the nucleus. These results suggest that the newly isolated wild soybean GsTIFY10 is a positive regulator of plant bicarbonate stress tolerance and is also a repressor of jasmonate signaling, from hormone perception to transcriptional activity.
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References
Alhendawi RA, Römheld V, Kirkby EA, Marschner H (1997) Influence of increasing bicarbonate concentration on plant growth, organic acid accumulation in roots and iron uptake by barley, sorghum and maize. J Plant Nutr 20:1731–1753
Arnon DI (1949) Copper enzymes in isolated chloroplasts in Beta vulgaris. Plant Physiol 24:1–15
Bailey TL, Boden M, Buske FA et al (2009) MEME Suite: tools for motif discovery and searching. Nucleic Acids Res 37(Web Server issue):W202–W208
Bell E, Mullet JE (1993) Characterization of an Arabidopsis lipoxygenase gene responsive to methyl jasmonate and wounding. Plant Physiol 103:1133–1137
Benedetti CE, Xie D, Turner JG (1995) Coi1-dependent expression of an Arabidopsis vegetative storage protein in flowers and siliques and in response to coronatine or methyl jasmonate. Plant Physiol 109:567–572
Browse J (2005) Jasmonate: an oxylipin signal with many roles in plants. Vitam Horm 72:431–456
Casal JJ (2002) Environmental cues affecting development. Curr Opin Plant Biol 5:37–42
Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signaling. Nature 448:666–671
Chung HS, Howe GA (2009) A critical role for the TIFY motif in repression of jasmonate signaling by a stabilized splice variant of the JASMONATE ZIM-domain protein JAZ10 in Arabidopsis. Plant Cell 21:131–145
Chung HS, Koo AJ, Gao X, Jayanty S, Thines B, Jones AD, Howe GA (2008) Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory. Plant Physiol 146:952–964
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Conconi A, Smerdon MJ, Howe GA, Ryan CA (1996) The octadecanoid signaling pathway in plants mediates a response to ultraviolet radiation. Nature 383:826–829
Davies DD (1986) The fine control of cytosolic pH. Physiol Plant 67:702–706
Devoto A, Turner JG (2003) Regulation of jasmonate-mediated plant responses in Arabidopsis. Ann Bot-London 92(3):329–337
Devoto A, Ellis C, Magusin A, Chang HS, Chilcott C, Zhu T, Turner JG (2005) Expression profiling reveals COI1 to be a key regulator of genes involved in wound- and methyl jasmonate-induced secondary metabolism, defence, and hormone interactions. Plant Mol Biol 58:497–513
Ellis C, Turner JG (2002) A conditionally fertile coi1 allele indicates cross-talk between plant hormone signaling pathways in Arabidopsis thaliana seeds and young seedlings. Planta 215:549–556
Frelin C, Vigne P, Ladoux A, Lazdunski M (1988) The regulation of the intracellular pH in cells from vertebrates. Eur J Biochem 174:3–14
Fushimi T, Umeda M, Shimazaki T, Kato A, Toriyama K, Uchimiya H (1994) Nucleotide sequence of a rice cDNA similar to a maize NADP-dependent Malic enzyme. Plant Mol Biol 24:965–967
Ge Y, Zhu YM, Lv DK, Dong TT, Wang WS, Tan SJ, Liu CH, Zou P (2009) Research on responses of wild soybean to alkaline stress. Pratacultural Science 26(2):47–52
Ge Y, Li Y, Zhu YM, Bai X, Lv DK, Guo DJ, Ji W, Cai H (2010) Global transcriptome profiling of wild soybean (Glycine soja) roots under NaHCO3 treatment. BMC Plant Biol 10(1):153
Gout E, Bligny R, Douce R (1992) Regulation of in tracellular pH values in higher plant cells: carbon-13 and phosphorus-31 nuclear magnetic resonance studies. J Biol Chem 267:13903–13909
Hussam HN, Bjarne GH, Morten HH, Jacob KJ, Barbara AH (2006) Advancing uracil-excision based cloning towards an ideal technique for cloning PCR fragments. Nucleic Acids Res 34(18):e122
Jiang Y, Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biol 6:25. doi:10.1186/1471-2229-6-25
Jin H, Plaha P, Park JY, Hong CP, Lee IS, Yang ZH, Jiang GB, Kwak SS, Liu SK, Lee JS, Kim YA, Lim YP (2006) Comparative EST profiles of leaf and root of Leymus chinensis, a xerophilous grass adapted to high pH sodic soil. Plant Sci 170(6):1081–1086
Kanna M, Tamaoki M, Kubo A, Nakajima N, Rakwal R, Agrawal GK, Tamogami S, Ioki M, Ogawa D, Saji H, Aono M (2003) Isolation of an ozone-sensitive and jasmonate-semi-insesitive Arabidopsis mutant (oji1). Plant Cell Physiol 44:1301–1310
Kessler A, Halitschke R, Baldwin IT (2004) Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 305:665–668
Kumar S, Dudley J, Nei M, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299–306
Kurkela S, Franck M (1990) Cloning and characterization of a cold- and ABA-inducible Arabidopsis gene. Plant Mol Biol 15:137–144
Laudert D, Weiler EW (1998) Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signaling. Plant J 15:675–684
Liu J, Zhu JK (1997) Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiol 114:591–596
Liu CK, Zhang XX, Chen YX (2004) Is the “plant intracellular pH regulation system” a tolerance mechanism adapting to environmental stress? Molecular Plant Breeding 2(2):179–186
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
Lorenzo O, Solano R (2005) Molecular players regulating the jasmonate signaling network. Curr Opin Plant Biol 8:532–540
Major IT, Constabel CP (2006) Molecular analysis of poplar defense against herbivory: comparison of wound-and insect elicitorinduced gene expression. New Phytol 172:617–635
Marre E, Ballarin-Denti A (1985) The proton pumps at the plasmalemma and the tonoplast of higher plants. J Bioenerg Biomembr 17:1–21
McConn M, Creelman RA, Bell E, Mullet JE, Browse J (1997) Jasmonate is essential for insect defence in Arabidopsis. Proc Natl Acad Sci 94:5473–5477
Melotto M, Mecey C, Niu Y, Chung HS, Katsir L, Yao J, Zeng W, Thines B, Staswick P, Browse J, Howe G, He SY (2008) A critical role of two positively charged amino acids in the Jas motif of Arabidopsis JAZ proteins in mediating coronatine- and jasmonoyl isoleucine-dependent interaction with the COI1 F-box protein. Plant J 55:979–988
Mueller LA, Hinz U, Uzé M, Sautter C, Zryd J-P (1997) Biochemical complementation of the betalain biosynthetic pathway in Portulaca grandiflora by a fungal 3, 4-dihydroxyphenylalanine dioxygenase. Planta 203(2):260–263
Nordin K, Vahala T, Palva ET (1993) Differential expression of two related low-temperature-induced genes in Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 21:641–653
Overmyer K, Tuominen H, Kettunen R, Betz C, Langebartels C, HJr Sandermann, Kangasjarvi J (2000) Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. Plant Cell 12:1849–1862
Penninckx IA, Thomma BP, Buchala A, Metraux JP, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10:2103–2113
Rajendra BR, Jonathan DG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488
Rao MV et al (2000) Jasmonic acid signaling modulates ozoneinduced hypersensitive cell death. Plant Cell 12:1633–1646
Reymond P, Bodenhausen N et al (2004) A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16:3132–3147
Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386
Sakano K (1998) Revision of biochemical pH-stat: involvement of alternative pathway metabolisms. Plant Cell Physiol 39(5):467–473
Sasaki Y, Asamizu E, Shibata D, Nakamura Y, Kaneko T, Awai K, Amagai M, Kuwata C, Tsugane T, Masuda T, Shimada H, Takamiya X, Ohta H, Tabata S (2001) Monitoring of methyl jasmonate-responsive genes in Arabidopsis by cDNA macroarray: self-activation of jasmonic acid biosynthesis and crosstalk with other phytohormone signaling pathways. DNA Res 8:153–161
Shikata M, Takemura M, Yokota A, Kohchi T (2003) Arabidopsis ZIM, a plant-specific GATA factor, can function as a transcriptional activator. Biosci Biotechnol Biochem 67:2495–2497
Shikata M, Matsuda Y, Ando K, Nishii A, Takemura M, Yokota A, Kohchi T (2004) Characterization of Arabidopsis ZIM, a member of a novel plant-specific GATA factor gene family. J Exp Bot 55:631–639
Staswick PE (2008) JAZing up jasmonate signaling. Trends Plant Sci 13:66–71
Staswick PE, Su W, Howell SH (1992) Methyl jasmonat inhibition of root growth and induction of a leaf protein are decrease in an Arabidopsis thaliana mutant. Proc Natl Acad Sci 89:6837–6840
Staswick PE, Yuen GY, Lehman CC (1998) Jasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregulare. Plant J 15:747–754
Tang CX, Robson AD (1993) pH above 6.0 reduces nodulation in Lupinus species. Plant Soil 152(2):269–276
Tardien F, Davies WJ (1992) Stomatal response to abscisic acid is a function of current plant water status. Plant Physiol 98:540–545
Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signaling. Nature 448:661–665
Thomma BPHJ, Eggermont K, Penninckx IAMA, MauchMani B, Vogelsang R, Cammue BPA, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defence-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci 95:15107–15111
Torimitsu K, Yazaki Y, Nagasuka K, Ohta E, Sakata M (1984) Effect of external pH on the cytoplasmic and vacuolar pHs in mung bean root-tip cells: a 31P nuclear magnetic-resonance study. Plant Cell Physiol 25(8):1043–1409
Troll W, Lindsley J (1955) A photometric method for the determination of proline. J Biol Chem 215:655–660
Vanholme B, Grunewald W, Bateman A, Kohchi T, Gheysen G (2007) The TIFY family previously known as ZIM. Trends Plant Sci 12:239–244
Vijayan P, Shockey J, Le′vesque CA, Cook RJ, Browse J (1998) A role for jasmonate in pathogen defense of Arabidopsis. Proc Natl Acad Sci 95:7209–7214
Wang H, Datla R, Georges F, Loewen M, Cutler AJ (1995) Promoters from kin1 and cor6.6, two homologous Arabidopsis thaliana genes: transcriptional regulation and gene expression induced by low temperature, ABA, osmoticum and dehydration. Plant Mol Biol 28:605–617
Wang YN, Liu C, Li KX et al (2007) Arabidopsis EIN2 modulates stress response through abscisic acid response pathway. Plant Mol Biol 64:633–644
Wasternack C (2006) Oxilipins: biosynthesis, signal transduction and action. In: Hedden P, Thomas S (eds) Plant hormone signaling. Annual plant reviews. Blackwell Publishing Ltd, Oxford, pp 185–228
Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100(4):681–697
White DWR (2006) PEAPOD regulates lamina size and curvature in Arabidopsis. Proc Natl Acad Sci 103:13238–13243
Willems E, Leyns L, Vandesompele J (2008) Standardization of real-time PCR gene expression data from independent biological replicates. Anal Biochem 379:127–129
Xu B, Timko MP (2004) Methyljasmonate induced expression of the tobacco putrescine N-methyltransferase genes requires both G-box an GCC-motif elements. Plant Mol Biol 55:743–761
Yamaguchi-Shinozaki K, Shinozaki K (1993a) The plant hormone abscisic acid mediates the drought-induced expression but not the seed-speciWc expression of rd22, a gene responsive to dehydration stress in Arabidopsis thaliana. Mol Gen Genet 238:17–25
Yamaguchi-Shinozaki K, Shinozaki K (1993b) Arabidopsis DNA encoding two desiccation-responsive rd29 genes. Plant Physiol 101:1119–1120
Yan Y, Stolz S, Chetelat A, Reymond P, Pagni M, Dubugnon L, Farmer EE (2007) A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell 19:2470–2483
Yang X, Romheld V, Marschner H (1994a) Effect of bicarbonate on root growth and accumulation of organic acids in Zn-inefficient and Zn-efficient rice cultivars (Oryza sativa L.). Plant Soil 164:1–7
Yang X, Römheld V, Marschner H (1994b) Effect of bicarbonate on root growth and accumulation of organic acids in Zn-inefficient and Zn-efficient rice cultivars (Oryza sativa L.). Plant Soil 164:1–7
Ye HY, Du H, Tang N, Li XH, Xiong LZ (2009) Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice. Plant Mol Biol 71:291–305
Zhu JK, Hasegawa PM, Bressan RA (1997) Molecular aspects of osmotic stress in plants. CRC Crit Rev Plant Sci 16:253–277
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This work was supported by the National Natural Science Foundation of China (30570990, 30471059), the“863” project (2008AA10Z153), National Major Project for Cultivation of Transgenic Crops (2008ZX08004), the Key Research Plan of Heilongjiang Province (GA06B103-3), the Innovation Research Group of NEAU (CXT004), and the Basic Research Preliminary Study Foundation of the Ministry of Science and Technology of the PRC (2003CCA03500).
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Zhu, D., Bai, X., Chen, C. et al. GsTIFY10, a novel positive regulator of plant tolerance to bicarbonate stress and a repressor of jasmonate signaling. Plant Mol Biol 77, 285–297 (2011). https://doi.org/10.1007/s11103-011-9810-0
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DOI: https://doi.org/10.1007/s11103-011-9810-0