Abstract
In plants, trehalose-6-phosphate (Tre6P) synthesized by the Tre6P synthase (TPS) acts as a signal metabolite in regulating sucrose metabolism in relation to plant growth and development. The Hevea genome predicts a total of 14 TPS genes, and two class I TPS members, HbTPS1 and 2, were explored here for their expressions under various hormone and abiotic stress treatments. HbTPS1 and 2 expressions in latex, cytoplasm of rubber-producing laticifers, were markedly affected by the treatments of ethephon (2-chloroethylphosphonic acid, an ethylene releaser), 2,4-dichlorophenoxyacetic acid, jasmonic acid and salicylic acid although in a distinct manner. HbTPS1 and 2 expressions were significantly up-regulated in a similar manner by cold (5 °C) and heat (40 °C) as examined in Hevea seedling leaves and roots, and by wounding in latex. In comparison, the drought treatment (20% PEG) posed a different effect on HbTPS1 and 2 expressions in Hevea seedlings. For example, in roots, HbTPS1 transcripts accumulated with the treatment, whereas those of HbTPS2 decreased for the first 24 h. Various hormone- and stress-responsive elements could be in silico predicted in HbTPS1 and 2 promoters, and a universal expression was observed for the HbTPS1::GUS activity in all growth stages of transgenic Arabidopsis. These results, coupled with the fact of rubber biosynthesis as a defense response using sucrose as the precursor molecule, propose a potential role of TPS genes in regulating rubber production.
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References
Allen GC, Flores-Vergara MA, Krasynanski S et al (2006) A modified protocol for rapid DNA isolation from plant tissues using cetyltrimethylammonium bromide. Nat Protoc 1:2320–2325
Avonce N, Mendoza-Vargas A, Morett E et al (2006) Insights on the evolution of trehalose biosynthesis. BMC Evol Biol 6:109–123
Ball P (2000) Fresh and dry. Nat News. doi:10.1038/news000720-3
Bell W, Klaassen P, Ohnacker M et al (1992) Characterization of the 56-kDa subunit of yeast trehalose-6-phosphate synthase and cloning of its gene reveal its identity with the product of CZFl, a regulator of carbon catabolite inactivation. Eur J Biochem 209:951–959
Boudreau BA, Larson TM, Brown DW et al (2013) Impact of temperature stress and validamycin A on compatible solutes and fumonisin production in F. verticillioides: role of trehalose-6-phosphate synthase. Fungal Genet Biol 57:1–10
Boyes DC, Zayed AM, Ascenzi R et al (2001) Growth stage based phenotypic analysis of Arabidopsis a model for high throughput functional genomics in plants. Plant Cell 13:1499–1510
Clough SJ, Bent AF (1998) A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
d’Auzac J, Jacob JL, Prévôt JC et al (1997) The regulation of cis-polyisoprene production (natural rubber) from Hevea brasiliensis. In: Pandalai SG (ed) Recent research developments in plant physiology, vol 1. Research Signpost, Trivandrum, pp 273–332
Delorge I, Figueroa CM, Feil R et al (2015) Trehalose-6-phosphate synthase 1 is not the only active TPS in Arabidopsis thaliana. Biochem J 466:283–290
Du HW, Zhang ZX, Li JS (2010) Isolation and functional characterization of a waterlogging-induced promoter from maize. Plant Cell Rep 29:1269–1275
Duan CF, Rio M, Leclercq J et al (2010) Gene expression pattern in response to wounding, methyl jasmonate and ethylene in the bark of Hevea brasiliensis. Tree Physiol 30:1349–1359
Eastmond PJ, van Dijken AJ, Spielman M et al (2002) Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation. Plant J 29:225–235
Elbein AD (1974) The metabolism of alpha, alpha-trehalose. Adv Carbohydr Chem Biochem 30:227–256
Ezcurra I, Ellerström M, Wycliffe P et al (1999) Interaction between composite elements in the napA promoter: both the B-box ABA-responsive complex and the RY/G complex are necessary for seed-specific expression. Plant Mol Biol 40:699–709
Fernandez O, Bethencourt L, Quero A et al (2010) Trehalose and plant stress responses: friend or foe? Trends Plant Sci 15:409–417
Garg AK, Kim JK, Owens TG et al (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99:15898–15903
Ge LF, Chao DY, Shi M et al (2008) Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes. Planta 228:191–201
Glasel JA (1995) Validity of nucleic acid purities monitored by 260 nm/280 nm absorbance ratios. Biotechniques 18:62–63
Goddijn O, Smeekens S (1998) Sensing trehalose biosynthesis in plants. Plant J 14:143–146
Gómez LD, Gilday A, Feil R et al (2010) AtTPS1-mediated trehalose 6-phosphate synthesis is essential for embryogenic and vegetative growth and responsiveness to ABA in germinating seeds and stomatal guard cells. Plant J 64:1–13
Higo K, Ugawa Y, Iwamoto M et al (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circ Calif Agric Exp Stn 347:1–39
Jang IC, Oh SJ, Seo JS et al (2003) Expression of a bifunctional fusion of the Escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance without stunting growth. Plant Physiol 131:516–524
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907
Jiang W, Fu FL, Zhang SZ et al (2010) Cloning and characterization of functional trehalose-6-phosphate synthase gene in maize. J Plant Biol 53:134–141
Karim S, Aronsson H, Ericson H et al (2007) Improved drought tolerance without undesired side effects in transgenic plants producing trehalose. Plant Mol Biol 64:371–386
Kosmas SA, Argyrokastritis A, Loukas MG et al (2006) Isolation and characterization of drought-related trehalose 6-phosphate-synthase gene from cultivated cotton (Gossypium hirsutum L.). Planta 223:329–339
Lapp D, Patterson B, Elbein A (1971) Properties of a trehalose phosphate synthetase from Mycobacterium smegmatis. J Biol Chem 246:4567–4579
Lescot M, Déhais P, Thijs G et al (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327
Li HP, Qin YX, Xiao XH et al (2011a) Screening of valid reference genes for real-time RT-PCR data normalization in Hevea brasiliensis and expression validation of a sucrose transporter gene HbSUT3. Plant Sci 181:132–139
Li HW, Zang BS, Deng XW et al (2011b) Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta 234:1007–1018
Liu SJ, Lan JX, Zhou BH et al (2015) HbNIN2, a cytosolic alkaline/neutral-invertase, is responsible for sucrose catabolism in rubber-producing laticifers of Hevea brasiliensis (para rubber tree). New Phytol 206:709–725
Lowe RG, Lord M, Rybak K et al (2009) Trehalose biosynthesis is involved in sporulation of Stagonospora nodorum. Fungal Genet Biol 46:381–389
Lunn JE (2007) Gene families and evolution of trehalose metabolism in plants. Funct Plant Biol 34:550–563
Lunn JE, Feil R, Hendriks JH et al (2006) Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADP-glucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem J 397:139–148
Miranda JA, Avonce N, Suárez R et al (2007) A bifunctional TPS-TPP enzyme from yeast confers tolerance to multiple and extreme abiotic-stress conditions in transgenic Arabidopsis. Planta 226:1411–1421
Mu M, Lu XK, Wang JJ et al (2016) Genome-wide Identification and analysis of the stress-resistance function of the TPS (trehalose-6-phosphate synthase) gene family in cotton. BMC Genet 17:54
Nwaka S, Holzer H (1998) Molecular biology of trehalose and the trehalases in the yeast Saccharomyces cerevisiae. Prog Nucleic Acid Res Mol Biol 58:197–237
Petzold EW, Himmelreich U, Mylonakis E et al (2006) Characterization and regulation of the trehalose synthesis pathway and its importance in the pathogenicity of Cryptococcus neoformans. Infect Immun 74:5877–5887
Rawat R, Xu ZF, Yao KM et al (2005) Identification of cis-elements for ethylene and circadian regulation of the Solanum melongena gene encoding cysteine proteinase. Plant Mol Biol 57:629–643
Rieping M, Schoffl 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
Schultz J, Milpetz F, Bork P et al (1998) SMART: a simple modular architecture research tool identification of signaling domains. Proc Natl Acad Sci USA 95:5857–5864
Sibéril Y, Doireau P, Gantet P (2001) Plant bZIP G-box binding factors. Eur J Biochem 268:5655–5666
Singh NK, Gupta DK, Jayaswal PK et al (2012) The first draft of the pigeonpea genome sequence. J Plant Biochem Biotechnol 21:98–112
Suárez R, Wong A, Ramirez M et al (2008) Improvement of drought tolerance and grain yield in common bean by overexpressing trehalose-6-phosphate synthase in rhizobia. Mol Plant Microbe Interact 21:958–966
Tang CR, Qi JY, Li HP et al (2007) A convenient and efficient protocol for isolating high-quality RNA from latex of Hevea brasiliensis (para rubber tree). J Biochem Biophys Methods 70:749–754
Tang B, Chen J, Yao Q et al (2010a) Characterization of a trehalose-6-phosphate synthase gene from Spodoptera exigua and its function identification through RNA interference. J Insect Physiol 56:813–821
Tang CR, Huang DB, Yang JH et al (2010b) The sucrose transporter HbSUT3 plays an active role in sucrose loading to laticifer and rubber productivity in exploited trees of Hevea brasiliensis (para rubber tree). Plant Cell Environ 33:1708–1720
Tang CR, Yang M, Fang YJ et al (2016) The rubber tree genome reveals new insights into rubber production and species adaptation. Nat Plants 2:16073
van Dijken AJ, Schluepmann H, Smeekens SC (2004) Arabidopsis trehalose-6-phosphate synthase 1 is essential for normal vegetative growth and transition to flowering. Plant Physiol 135:969–977
Vandesteene L, Ramon M, Le Roy K et al (2010) A single active trehalose-6-P synthase (TPS) and a family of putative regulatory TPS-like proteins in Arabidopsis. Mol Plant 3:406–419
Vuorio OE, Kalkkinen N, Londesborough J (1993) Cloning of two related genes encoding the 56-kDa and 123-kDa subunits of trehalose synthase from the yeast Saccharomyces cerevisiae. Eur J Biochem 216:849–861
Washida H, Wu CY, Suzuki A et al (1999) Identification of cis-regulatory elements required for endosperm expression of the rice storage protein glutelin gene GluB-1. Plant Mol Biol 40:1–12
Winderickx J, de Winde JH, Crauwels M et al (1996) Regulation of genes encoding subunits of the trehalose synthase complex in Saccharomyces cerevisiae: novel variations of STRE-mediated transcription control? Mol Gen Genet 252:470–482
Xiao XH, Tang CR, Fang YJ et al (2014) Structure and expression profile of the sucrose synthase gene family in the rubber tree: indicative of roles in stress response and sucrose utilization in the laticifers. FEBS J 281:291–305
Xin LS (2012) Cloning and functional analysis of the promoters of HbSUT3 and HbSUT5 in Hevea brasiliensis. Hainan University, Haikou
Yadav UP, Ivakov A, Feil R et al (2014) The sucrose-trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. J Exp Bot 65:1051–1068
Yang HL, Liu YJ, Wang CL et al (2012) Molecular evolution of trehalose-6-phosphate synthase (TPS) gene family in Populus, Arabidopsis and rice. PLoS ONE 7:e42438
Zähringer H, Thevelein J, Nwaka S (2000) Induction of neutral trehalase Nth1 by heat and osmotic stress is controlled by STRE elements and Msn2/Msn4 transcription factors: variations of PKA effect during stress and growth. Mol Microbiol 35:397–406
Zang BS, Li HW, Li WJ et al (2011) Analysis of trehalose-6-phosphate synthase (TPS) gene family suggests the formation of TPS complexes in rice. Plant Mol Biol 76:507–522
Zentella R, Mascorro-Gallardo J, Van DP et al (1999) A Selaginella lepidophylla trehalose-6-phosphate synthase complements growth and stress-tolerance defects in a yeast tps1 mutant. Plant Physiol 119:1473–1482
Zhang LF, Li WF, Han SY et al (2013) cDNA cloning, genomic organization and expression analysis during somatic embryogenesis of the translationally controlled tumor protein (TCTP) gene from Japanese larch (Larix leptolepis). Gene 529:150–158
Zhang J, Li Y, Jia HX et al (2015) The heat shock factor gene family in Salix suchowensis: a genome-wide survey and expression profiling during development and abiotic stresses. Front Plant Sci 6:748
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This work was supported by the Natural Science Foundation of China (31570672) and the National High Technology Research and Development Program (863) (2013AA102605).
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Zhou, B., Fang, Y., Fan, Y. et al. Expressional characterization of two class I trehalose-6-phosphate synthase genes in Hevea brasiliensis (para rubber tree) suggests a role in rubber production. New Forests 48, 513–526 (2017). https://doi.org/10.1007/s11056-017-9578-4
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DOI: https://doi.org/10.1007/s11056-017-9578-4