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Identification of differentially expressed transcripts from leaves of the boron tolerant plant Gypsophila perfoliata L.

  • Biotic and Abiotic Stress
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Abstract

Very recently some of the species of Gypsophila genus collected from the boron rich soils in Turkey were shown to be remarkably tolerant to high levels of boron. A limited amount of boron is necessary for the normal development of plants; however, a high level of boron in soil is generally toxic. Nevertheless, the adaptability of plant species allows them to withstand the presence of extreme amounts of metal ion by various strategies. This study is conducted on highly boron tolerant Gypsophila perfoliata L. collected from a location in the boron mining area. The plant samples were transferred into plant nutritional medium in the presence high; ~500 (35 mg/kg), 1,000, and 30 μM (considered normal) boron concentrations. We compared the transcriptome of the plant sample treated with the excess levels of boron to that of the samples grown under normal concentration using differential display PCR (DDRT-PCR) method. Thirty bands showing differential expression levels (presence or absence of bands or varying intensities) in either of ~500 or 30 μM B concentrations at varying time points were excised, cloned, and sequenced. Among which, 18 of them were confirmed via quantitative reverse transcription real time PCR (qRT-PCR). We are reporting the first preliminary molecular level study of boron tolerance on this organism by attempting to identify putative genes related in the tolerance mechanism. The gene fragments are consistent with the literature data obtained from a proteomics study and a metabolomics study performed in barley under varying boron concentrations.

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References

  • Akpulat HA, Celik N (2005) Flora of gypsum areas in Sivas in the eastern part of Cappadocia in Central Anatolia, Turkey. J Arid Environ 61:27–46

    Article  Google Scholar 

  • Altschul SF, Gish W, Myers W, Miller EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Alves M, Francisco R, Martins I, Ricardo CPP (2006) Analysis of Lupinus albus leaf apoplastic proteins in response to boron deficiency. Plant Soil 279:1–11. doi:10.1007/s11104-005-3154-y

    Article  CAS  Google Scholar 

  • Babaoglu M, Gezgin S, Topal A, Sade B, Dural H (2004) Gypsophila sphaerocephala Fenzl ex Tchihat.: a boron hyperaccumulator plant species that may phytoremediate soils with toxic B levels. Turk J Bot 28:273–278

    Google Scholar 

  • Baker AJM (1981) Accumulators and excluders: strategies in the response of plants to trace metals. J Plant Nutr 3:643–654

    Article  CAS  Google Scholar 

  • Bezier A, Lambert B, Baillieul F (2002) Study of defense-related gene expression in grapevine leaves and berries infected with Botrytis cinerea. Eur J Plant Pathol 108:111–120. doi:10.1023/A:1015061108045

    Article  CAS  Google Scholar 

  • Brown PH, Bellaloui N, Wimmer MA, Bassil ES, Ruiz J, Hu H, Pfeffer H, Dannel F, Romheld V (2002) Boron in plant biology. Plant Biol 4:205–223. doi:10.1055/s-2002-25740

    Article  CAS  Google Scholar 

  • Cartwright B, Zarcinas BA, Spouncer IA (1986) Boron toxicity in South Australian barley crops. Aust J Agric Res 37:351–359

    Article  CAS  Google Scholar 

  • Chen X, Schauder S, Potier N, Van Dorsselaer A, Pelczer I, Bassler BL, Hughson FM (2002) Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415:545–549. doi:10.1038/415545a

    Article  PubMed  CAS  Google Scholar 

  • Cherepneva GN, Schmidt KH, Kulaeva ON, Oelmüller R, Kusnetsov VV (2003) Expression of the ribosomal proteins S14, S16, L13a and L30 is regulated by cytokinin and abscisic acid: implication of the involvement of phytohormones in translational processes. Plant Sci 165:925–932. doi:10.1016/S0168-9452(03)00204-8

    Article  CAS  Google Scholar 

  • Dannel F, Heidrun P, Römheld V (2000) Characterization of root boron pools, boron uptake and boron translocation in sunflower using the stable isotope 10B and 11B. Aust J Plant Physiol 156:756–761

    Google Scholar 

  • Dannel F, Pfeffer H, Ro¨mheld V (2002) Update on boron in higher plants uptake, primary translocation and compartmentation. Plant Biol 4:193–204. doi:10.1055/s-2002-25730

    Article  CAS  Google Scholar 

  • Dordas C, Chrispeels MJ, Brown PH (2000) Permeability and channel-mediated transport of boric acid across membrane vesicles isolated from squash roots. Plant Physiol 124:1349–1361. doi:10.1007/0-306-47624-X

    Article  PubMed  CAS  Google Scholar 

  • Ferrol N, Belver A, Roldan M, Rodriguezrosales MP, Donaire JP (1993) Effects of Boron on proton transport and membrane properties of sunflower (Helianthus annuus L.) cell microsomes. Plant Physiol 103:763–769

    PubMed  CAS  Google Scholar 

  • Grover A, Kapoor A, Lakshmi O S, Agarwal S, Sahi C, Katiyar-Agarwal S, Agarwal M, Dubey H (2001) Understanding molecular alphabets of the plant abiotic stress responses. Curr Sci 80:206–216

    CAS  Google Scholar 

  • Guo P, Bai G, Carver B, Li R, Bernardo A, Baum M (2007) Transcriptional analysis between two wheat near-isogenic lines contrasting in aluminum tolerance under aluminum stress. Mol Genet Genom 1:1–12. doi:10.1007/s00438-006-0169-x

    CAS  Google Scholar 

  • Hakki EE, Unlu A, Ozbek Z, Gezgin S, Babaoglu M (2006) Characterization of plants in the genus Gypsophila via molecular genetic methods. Selçuk Üniversitesi, Ziraat Fakültesi dergisi 20:27–31

  • Hellmann H, Estelle M (2002) Plant development: regulation by protein degradation. Science 297:793–797. doi:10.1126/science.1072831

    Article  PubMed  CAS  Google Scholar 

  • Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425–479

    Article  PubMed  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circular 347. Univ Calif Agric Exp Stn Berkeley, CA, pp 1–39

  • Jakubowski H (1983) Synthesis of diadenosine 5, 5-P1, P4-tetraphosphate and related compounds by plant (Lupinus luteus) seryl-tRNA and phenylalanyl-tRNA synthetases. Acta Biochim Polon 30:51–69

    PubMed  CAS  Google Scholar 

  • Kamata T, Hiramoto H, Morita N, Shen JR, Mann NH, Yamamoto Y (2005) Quality control of photosystem II: an FtsH protease plays an essential role in the turnover of the reaction center D1 protein in Synechocystis PCC 6803 under heat stress as well as light stress conditions. Photochem Photobiol Sci 4:983–990. doi:10.1016/j.bbabio.2007.05.001

    Article  PubMed  CAS  Google Scholar 

  • Kaya Z, Zeydanli U, Cengel B, Yilmaz T (1999) Field guide to wildflowers of METU campus, suppl 23, p 456

  • Komenda J, Reisinger V, Muller B C, Dobakova M, Granvogl B, Eichacker LA (2004) Accumulation of the D2 protein is a key regulatory step for assembly of the photosystem II reaction center complex in Synechocystis PCC 6803. J Biol Chem 279:48620–48629

    Article  PubMed  CAS  Google Scholar 

  • Lee P C, Bochner BN, Ames BN (1983) AppppA, heat shock stress and cell oxidation. Proc Natl Acad Sci USA 80:7496–7500

    Article  PubMed  CAS  Google Scholar 

  • Liang P, Pardee AB (1992) Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257:967–971

    Article  PubMed  CAS  Google Scholar 

  • Lukaszewski KM, Blevins DG (1996) Root growth inhibition in boron deficient and aluminum stressed squash may be a result of impaired ascorbate metabolism. Plant Physiol 112:1235–1240

    Google Scholar 

  • Maas EV (1987) Salt tolerance of plants. In: Christie lBR (ed) Handbook of plant science in agriculture. CRC Press, Boca Raton, p 57

    Google Scholar 

  • Marin K, Suzuki I, Yamaguchi K, Ribbeck K, Yamamoto H, Kanesaki Y, Hagemann M, Murata N (2003) Identification of histidine kinases that act as sensors in the perception of salt stress in Synechocystis sp. strain PCC 6803. Proc Natl Acad Sci USA 100:9061–9066. doi:10.1073/pnas.1532302100

    Article  PubMed  CAS  Google Scholar 

  • Marschner H (1995) Nutritional physiology. In: Mineral nutrition of higher plants, 2nd edn. Academic Press, San Diego, pp 379–396

  • Miwa K, Takano J, Fujiwara T (2006) Improvement of seed yields under boron-limiting conditions through overexpression of BOR1, a boron transporter for xylem loading, in Arabidopsis thaliana. Plant J 46:1084–1091. doi:10.1111/j.1365-313X.2006.02763.x

    Article  PubMed  CAS  Google Scholar 

  • Miwa K, Takano J, Omori H, Seki M, Shinozaki K, Fujiwara T (2007) Plants tolerant of high boron levels. Science 318:1417. doi:10.1126/science.1146634

    Article  PubMed  CAS  Google Scholar 

  • Motoyama T, Kadokura K, Ohira T, Ichiishi A, Fujimura M, Yamaguchi I, Kudo T (2005) A two-component histidine kinase of the rice blast fungus is involved in osmotic stress response and fungicide action. Fungal Genet Biol 42:200–212. doi:10.1016/j.fgb.2004.11.002

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nable RO (1988) Resistance to boron toxicity amongst several barley and wheat cultivars: a preliminary examination of the resistance mechanism. Plant Soil 112:45–57

    Article  CAS  Google Scholar 

  • Noguchi K, Yasumori M, Imai T, Naito S, Matsunaga T, Oda H, Hayashi H, Chino M, Fujiwara T (1997) bor1-1, an Arabidopsis thaliana mutant that requires a high level of boron. Plant Physiol 115:901–906

    Article  PubMed  CAS  Google Scholar 

  • Noh B, Lee SH, Kim HJ, Yi G, Shin EA, Lee M, Jung KJ, Doyle MR, Amasino RM, Noh YS (2004) Divergent roles of a pair of homologous jumonji/zinc-finger-class transcription factor proteins in the regulation of Arabidopsis flowering time. Plant Cell 10:2601–2613. doi:10.1105/tpc.104.025353

    Article  Google Scholar 

  • Noh YS, Amasino RM (2003) PIE1, an ISWI family gene, is required for FLC activation and floral repression in Arabidopsis. Plant Cell 15:1671–1682. doi:10.1105/tpc.012161

    Article  PubMed  CAS  Google Scholar 

  • O’Neill MA, Eberhard S, Albersheim P, Darvill AG (2001) Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science 294:846–849. doi:10.1126/science.1062319

    Article  PubMed  CAS  Google Scholar 

  • Patterson J, Ford K, Cassin A, Natera S, Bacic A (2007) Increased abundance of proteins involved in phytosiderophore production in boron-tolerant barley. Plant Physiol 144:1612–31. doi:10.1104/pp.107.096388

    Article  PubMed  CAS  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucl Acids Res 29:2002–2007

    Article  Google Scholar 

  • Pollard AS, Parr AJ, Loughman BC (1977) Boron in relation to membrane function in higher plants. J Exp Bot 28:831–841

    Article  CAS  Google Scholar 

  • Ratcliffe OJ, Riechmann JL (2002) Arabidopsis transcription factors and the regulation of flowering time: a genomic perspective. Curr Issues Mol Biol 4:77–91

    PubMed  CAS  Google Scholar 

  • Raven JA (1980) Short- and long-distance transport of boric acid in plants. New Phytol 84:231–249

    Article  CAS  Google Scholar 

  • Rawson HM (1996) The developmental stage during which boron limitation causes sterility in wheat genotypes and recovery of fertility. Aust J Plant Physiol 99:1271–1274

    Google Scholar 

  • Reid RJ, Hayes JE, Post A, Stangoulis JCR, Graham RD (2004) A critical analysis of the causes of boron toxicity in plants. Plant Cell Environ 25:1405–1414. doi:10.1111/j.1365-3040.2004.01243.x

    Article  Google Scholar 

  • Roessner U, Patterson JH, Forbes MG, Fincher GB, Langridge P, Bacic A (2006) An investigation of boron toxicity in barley using metabolomics. Plant Physiol 142:1087–101. doi:10.1104/pp.106.084053

    Article  PubMed  CAS  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    PubMed  CAS  Google Scholar 

  • Savenstrand H, Brosche M, Strid A (2002) Regulation of gene expression by low levels of ultraviolet-B radiation in Pisum sativum: isolation of novel genes by suppression subtractive hybridization. Plant Cell Physiol 43:402–410. doi:10.1046/j.1365-3040.2000.00586.x

    Article  PubMed  CAS  Google Scholar 

  • Shorrocks VM (1997) The occurrence and correction of boron deficiency. Plant Soil 193:121–148

    Article  CAS  Google Scholar 

  • Simpson GG, Dean C (2002) Arabidopsis, the Rosetta stone of flowering time? Science 12:285–289. doi:10.1126/science.296.5566.285

    Article  Google Scholar 

  • Singh Z, Dhillan BS (1989) Effect of foliar application of boron on vegetative and panicle growth, sex expression, fruit retention and physicochemical characteristics of mango (Mangifera indica cv Dusheri). Trop Agric 64:305–308

    Google Scholar 

  • Stangoulis JC, Reid RJ, Brown PH, Graham RD (2001) Kinetic analysis of boron transport in Chara. Planta 213:142–146

    Article  PubMed  CAS  Google Scholar 

  • Stürzenbaum SR, Kille P (2001) Control genes in quantitative molecular biological techniques: the variability of invariance. Comp Biochem Physiol Part B 130:281–289

    Article  Google Scholar 

  • Sullivan JA, Shirasu K, Deng X (2003) The diverse roles of ubiquitin and the 26S proteosome in the life of plants. Nat Rev Genet 4:948–958. doi:10.1038/nrg1228

    Article  PubMed  CAS  Google Scholar 

  • Szymanski M, Deniziak M, Barciszewski J (2000) The new aspects of aminoacyl-tRNA synthetases. Acta Biochim Pol 47:821–834

    PubMed  CAS  Google Scholar 

  • Takano J, Noguchi K, Yasumori M, Kobayashi M, Gajdos Z, Miwa K, Hayashi H, Yoneyama T, Fujiwara T (2002) Arabidopsis boron transporter for xylem loading. Nature 420:337–340. doi:10.1038/nature01139

    Article  PubMed  CAS  Google Scholar 

  • Takano J, Miwa K, Yuan L, von Wiren N, Fujiwara T (2005) Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc Natl Acad Sci USA 102:12276–12281. doi:10.1073/pnas.0502060102

    Article  PubMed  CAS  Google Scholar 

  • Takano J, Wada M, Ludewig U, Schaaf G, von Wirén N, Fujiwara T (2006) The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 18:1498–509. doi:10.1105/tpc.106.041640

    Article  PubMed  Google Scholar 

  • Takeuchi T (1997) A gene trap approach to identify genes that control development. Dev Growth Differ 39:127–134

    Article  PubMed  CAS  Google Scholar 

  • Takeuchi T, Watanabe Y, Takano-Shimizu T, Kondo S (2006) Roles of jumonji and jumonji family genes in chromatin regulation and development. Takashi Dev Dyn 235:2449–2459

    Article  CAS  Google Scholar 

  • Toyoda M, Kojima M, Takeuchi T (2000) Jumonji is a nuclear protein that participates in the negative regulation of cell growth. Biochem Biophys Res Commun 274:332–336

    Article  PubMed  CAS  Google Scholar 

  • Toyoda M, Shirato H, Nakajima K, Kojima M, Takahashi M, Kubota M, Suzuki Migishima R, Motegi Y, Yokoyama M, Takeuchi T (2003) Jumonji downregulates cardiac cell proliferation by repressing cyclin D1 expression. Dev Cell 5:85–97. doi:10.1016/S1534-5807(03)00189-8

    Article  PubMed  CAS  Google Scholar 

  • Tsukada YI, Fang J, Erdjument-Bromage H, Warren ME, Borchers CH, Tempst P, Zhang Y (2006) Histone demethylation by a family of JmjC domain-containing proteins. Nature 439:811–816. doi:10.1038/nature04433

    Article  PubMed  CAS  Google Scholar 

  • Türe C, Bell RW (2004) Plant distribution and its relationship to extractable boron in naturally-occurring high boron soils in Turkey. Isr J Plant Sci 52:125–132

    Article  Google Scholar 

  • Yang X, Xi Jin, Feng Y, Islam E (2005) Molecular mechanisms and genetic basis of heavy metal tolerance/hyperaccumulation in plants. J Integr Plant Biol 47:1025–1035. doi:10.1111/j.1744-7909.2005.00144.x

    Article  CAS  Google Scholar 

  • Warington K (1923) The effect of boric acid and borax on the broad been and certain other plants. Ann Bot Lond 37:629–672

    Google Scholar 

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Acknowledgments

The authors thank to Dr. M. Babaoglu of Selcuk University, Konya, for sharing plant samples. We are also grateful for the support made available by METU funds and the State Planning Organization of the Republic of Turkey (Grant no. DPT2004K120750).

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  1. Department of Chemistry, Middle East Technical University, 06531, Ankara, Turkey

    Turgay Unver, Osman Bozkurt & Mahinur S. Akkaya

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  1. Turgay Unver
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  2. Osman Bozkurt
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Correspondence to Mahinur S. Akkaya.

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Communicated by M.C. Jordan.

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Unver, T., Bozkurt, O. & Akkaya, M.S. Identification of differentially expressed transcripts from leaves of the boron tolerant plant Gypsophila perfoliata L.. Plant Cell Rep 27, 1411–1422 (2008). https://doi.org/10.1007/s00299-008-0560-7

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