Abstract
Phosphomannomutase (PMM, EC 5.4.2.8) catalyzes the interconversion of mannose-6-phosphate to mannose-1-phosphate, the precursor for the synthesis of GDP-mannose. In this study, the complementary DNA (cDNA) of the Phosphomannomutase (PMM) gene was initially cloned from Dendrobium officinale by RACE method. Transient transform result showed that the DoPMM protein was localized in the cytoplasm. The DoPMM gene was highly expressed in the stems of D. officinale both in vegetative and reproductive developmental stages. The putative promoter was cloned by TAIL-PCR and used for searched cis-elements. Stress-related cis-elements like ABRE, TCA-element, and MBS were found in the promoter regions. The DoPMM gene was up-regulated after treatment with abscisic acid, salicylic acid, cold, polyethylene glycol, and NaCl. The total ascorbic acid (AsA) and polysaccharide content in all of the 35S::DoPMM Arabidopsis thaliana transgenic lines #1, #2, and #5 showed a 40, 39, and 31% increase in AsA and a 77, 22, and 39% increase in polysaccharides, respectively more than wild-type (WT) levels. All three 35S::DoPMM transgenic lines exhibited a higher germination percentage than WT plants when seeded on half-strength MS medium supplemented with 150 mM NaCl or 300 mM mannitol. These results provide genetic evidence for the involvement of PMM genes in the biosynthesis of AsA and polysaccharides and the mediation of PMM genes in abiotic stress tolerance during seed germination in A. thaliana.
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Abbreviations
- ABA:
-
Abscisic acid
- DW:
-
Dry weight
- FW:
-
Fresh weight
- GMP:
-
GDP-mannose pyrophosphorylase
- HAD:
-
Haloalkanoic acid dehalogenase
- PEG:
-
Polyethylene glycol
- PMM:
-
Phosphomannomutase
- ROS:
-
Reactive oxygen species
- SA:
-
Salicylic acid
References
Aimar D, Calafat M, Andrade AM, Carassay L, Abdala GI, Molas ML (2011) Drought tolerance and stress hormones: from model organisms to forage crops. In: Vasanthaiah H, Kambiranda D (eds) Plants and environment. InTech, Rijeka, Croatia, pp 137–164
Allen KN, Dunaway-Mariano D (2004) Phosphoryl group transfer: evolution of a catalytic scaffold. Trends Biochem Sci 29:495–503
Ananieva EA, Christov KN, Popova LP (2004) Exogenous treatment with salicylic acid leads to increased antioxidant capacity in leaves of barley plants exposed to paraquat. J Plant Physiol 161:319–328
Badejo AA, Jeong ST, Goto-Yamamoto N, Esaka M (2007) Cloning and expression of GDP-D-mannose pyrophosphorylase gene and ascorbic acid content of acerola (Malpighia glabra L.) fruit at ripening stages. Plant Physiol Biochem 45:665–672
Badejo AA, Eltelib HA, Fukunaga K, Fujikawa Y, Esaka M (2009) Increase in ascorbate content of transgenic tobacco plants overexpressing the acerola (Malpighia glabra) phosphomannomutase gene. Plant Cell Physiol 50:423–428
Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126:1024–1030
Burroughs AM, Allen KN, Dunaway-Mariano D, Aravind L (2006) Evolutionary genomics of the HAD superfamily: understanding the structural adaptations and catalytic diversity in a superfamily of phosphoesterases and allied enzymes. J Mol Biol 361:1003–1034
Citovsky V, Lee L-Y, Vyas S, Glick E, Chen M-H, 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
Clifford S, Arndt S, Popp M, Jones H (2002) Mucilages and polysaccharides in Ziziphus species (Rhamnaceae): localization, composition and physiological roles during drought-stress. J Exp Bot 53:131–138
Cline A, Gao N, Flanagan-Steet H, Sharma V, Rosa S, Sonon R, Azadi P, Sadler KC, Freeze HH, Lehrman MA (2012) A zebrafish model of PMM2-CDG reveals altered neurogenesis and a substrate-accumulation mechanism for N-linked glycosylation deficiency. Mol Biol Cell 23:4175–4187
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Conklin PL, Norris SR, Wheeler GL, Williams EH, Smirnoff N, Last RL (1999) Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin C) biosynthesis. Proc Natl Acad Sci U S A 96:4198–4203
Conzelmann A, Fankhauser C, Desponds C (1990) Myoinositol gets incorporated into numerous membrane glycoproteins of Saccharomyces cerevisiae; incorporation is dependent on phosphomannomutase (SEC53). EMBO J 9:653–661
Cromphout K, Vleugels W, Heykants L, Schollen E, Keldermans L, Sciot R, D’Hooge R, De Deyn P, von Figura K, Hartmann D (2006) The normal phenotype of Pmm1-deficient mice suggests that Pmm1 is not essential for normal mouse development. Mol Cell Biol 26:5621–5635
Dalessandro G, Piro G, Northcote D (1986) Glucomannan-synthase activity in differentiating cells of Pinus sylvestris L. Planta 169:564–574
Dubois M, Gilles KA, Hamilton JK, Rebers P, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Eager RE, Raman S, Wootten A, Westphal DL, Reid JS, Al Mandoos A (1988) The yeast SEC53 gene encodes phosphomannomutase. J Biol Chem 263:9155–9161
Edwards M, Bulpin PV, Dea IC, Reid JG (1989) Biosynthesis of legume-seed galactomannans in vitro. Planta 178:41–51
Elbein A (1969) Biosynthesis of a cell wall glucomannan in mung bean seedlings. J Biol Chem 244:1608–1616
Gilbert L, Alhagdow M, Nunes-Nesi A, Quemener B, Guillon F, Bouchet B, Faurobert M, Gouble B, Page D, Garcia V, Petit J, Stevens R, Causse M, Fernie AR, Lahaye M, Rothan C, Baldet P (2009) GDP-D-mannose 3,5-epimerase (GME) plays a key role at the intersection of ascorbate and non-cellulosic cell-wall biosynthesis in tomato. Plant J 60:499–508
Glaser L, Kornfeld S, Brown DH (1959) Preparation and properties of phosphomannomutase from baker’s yeast. Biochim Biophys Acta 33:522–526
Grünewald S (2009) The clinical spectrum of phosphomannomutase 2 deficiency (CDG-Ia). Biochim Biophys Acta 1792:827–834
Hancock RD, McRae D, Haupt SP, Viola R (2003) Synthesis of L-ascorbic acid in the phloem. BMC Plant Biol 3:7
Hansen SH, Frank SR, Casanova JE (1997) Cloning and characterization of human phosphomannomutase, a mammalian homologue of yeast SEC53. Glycobiology 7:829–834
He C, Zhang J, Liu X, Zeng S, Wu K, Yu Z, Wang X, Teixeira da Silva JA, Lin Z, Duan J (2015) Identification of genes involved in biosynthesis of mannan polysaccharides in Dendrobium officinale by RNA-seq analysis. Plant Mol Biol 88:219–231
Heykants L, Schollen E, Grünewald S, Matthijs G (2001) Identification and localization of two mouse phosphomannomutase genes, Pmm1 and Pmm2. Gene 270:53–59
Hinman MB, Villemez CL (1957) Glucomannan biosynthesis catalyzed by Pisum sativum enzymes. Plant Physiol 56:608–612
Hoeberichts FA, Vaeck E, Kiddle G, Coppens E, Van De Cotte B, Adamantidis A, Ormenese S, Foyer CH, Zabeau M, Inzé D (2008) A Temperature-sensitive mutation in the Arabidopsis thaliana phosphomannomutase gene disrupts protein glycosylation and triggers cell death. J Biol Chem 283:5708–5718
Iraki NM, Bressan RA, Carpita NC (1989) Extracellular polysaccharides and proteins of tobacco cell cultures and changes in composition associated with growth-limiting adaptation to water and saline stress. Plant Physiol 91:54–61
Keller R, Kossmann J (1999) Antisense inhibition of the GDP-mannose pyrophosphorylase reduces the ascorbate content in transgenic plants leading to developmental changes during senescence. Plant J 19:131–141
Kepes F, Schekma R (1988) The yeast SEC53 gene encodes phosphomannomutase. J Biol Chem 263:9155–9161
Kerepesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci 40:482–487
Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608
Kumar R, Mustafiz A, Sahoo KK, Sharma V, Samanta S, Sopory SK, Pareek A, Singla-Pareek SL (2012) Functional screening of cDNA library from a salt tolerant rice genotype Pokkali identifies mannose-1-phosphate guanyltransferase gene (OsMPG1) as a key member of salinity stress response. Plant Mol Biol 79:555–568
Lin L, Shi Q, Wang H, Qin A, Yu X (2011) Over-expression of tomato GDP-mannose pyrophosphorylase (GMPase) in potato increases ascorbate content and delays plant senescence. Agric Sci China 10:534–543
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408
Lu S, Su W, Li H, Guo Z (2009) Abscisic acid improves drought tolerance of triploid Bermudagrass and involves H2O2- and NO-induced antioxidant enzyme activities. Plant Physiol Biochem 47:132–138
Lukowitz W, Nickle TC, Meinke DW, Last RL, Conklin PL, Somerville CR (2001) Arabidopsis cyt1 mutants are deficient in a mannose-1-phosphate guanylyltransferase and point to a requirement of N-linked glycosylation for cellulose biosynthesis. Proc Natl Acad Sci U S A 98:2262–2267
Matthijs G, Schollen E, Pirard M, Budarf ML, Van Schaftingen E, Cassiman JJ (1997) PMM (PMM1), the human homologue of SEC53 or yeast phosphomannomutase, is localized on chromosome 22q13. Genomics 40:41–47
Meng L-Z, Lv G-P, Hu D-J, Cheong K-L, Xie J, Zhao J, Li S-P (2013) Effects of polysaccharides from different species of Dendrobium (Shihu) on macrophage function. Molecules 18:5779–5791
Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497
Murata T (1976) Purification and some properties of phosphomannomutase from corms of Amorphophallus konjac C. Koch. Plant Cell Physiol 17:1099–1109
Ng TB, Liu J, Wong JH, Ye X, Sze SCW, Tong Y, Zhang KY (2012) Review of research on Dendrobium, a prized folk medicine. Appl Microbiol Biotechnol 93:1795–1803
Oesterhelt C, Schnarrenberger C, Gross W (1996) Phosphomannomutase and phosphoglucomutase in the red alga Galdieria sulphuraria. Plant Sci 121:19–27
Popova T, Matasova L, Lapot’ko A (1998) Purification, separation and characterization of phosphoglucomutase and phosphomannomutase from maize leaves. Biochem Mol Biol Int 46:461–470
Qian W, Yu C, Qin H, Liu X, Zhang A, Johansen IE, Wang D (2007) Molecular and functional analysis of phosphomannomutase (PMM) from higher plants and genetic evidence for the involvement of PMM in ascorbic acid biosynthesis in Arabidopsis and Nicotiana benthamiana. Plant J 49:399–413
Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227
Silvaggi NR, Zhang C, Lu Z, Dai J, Dunaway-Mariano D, Allen KN (2006) The X-ray crystal structures of human alpha-phosphomannomutase 1 reveal the structural basis of congenital disorder of glycosylation type 1a. J Biol Chem 281:14918–14926
Singer T, Ellen Burke MS (2003) High-throughput TAIL-PCR as a tool to identify DNA flanking insertions. Methods Mol Biol 236:241–272
Small DM, Matheson NK (1979) Phosphomannomutase and phosphoglucomutase in developing Cassia corymbosa seeds. Phytochemistry 18:1147–1150
Smith D, Cooper M, Detiani M, Losberger C, Payton M (1992) The Candida albicans PMM1 gene encoding phosphomannomutase complements a Saccharomyces cerevisiae sec53-6 mutation. Curr Genet 22:501–503
Staneva D, Uccelletti D, Farina F, Venkov P, Palleschi C (2004) KlSEC53 is an essential Kluyveromyces lactis gene and is homologous with the SEC53 gene of Saccharomyces cerevisiae. Yeast 21:41–51
Thiel C, Lübke T, Matthijs G, Von Figura K, Körner C (2006) Targeted disruption of the mouse phosphomannomutase2 gene causes early embryonic lethality. Mol Cell Biol 26:5615–5620
Ueda Y, Wu L, Frei M (2013) A critical comparison of two high-throughput ascorbate analyses methods for plant samples. Plant Physiol Biochem 70:418–423
Wang HS, Yu C, Zhu ZJ, Yu XC (2011) Overexpression in tobacco of a tomato GMPase gene improves tolerance to both low and high temperature stress by enhancing antioxidation capacity. Plant Cell Rep 30:1029–1040
Wang HS, Zhu ZJ, Feng Z, Zhang SG, Yu C (2012) Antisense-mediated depletion of GMPase gene expression in tobacco decreases plant tolerance to temperature stresses and alters plant development. Mol Biol Rep 39:10413–10420
Wei W, Feng L, Bao W-R, Ma D-L, Leung C-H, Nie S-P, Han Q-B (2016) Structure characterization and immunomodulating effects of polysaccharides isolated from Dendrobium officinale. J Agric Food Chem 64:881–889
Westpha V, Peterson S, Patterson M, Tournay A, Blumenthal A, Treacy EP, Freeze HH (2001) Functional significance of PMM2 mutations in mildly affected patients with congenital disorders of glycosylation Ia. Genet Med 3:393–398
Xing X, Cui SW, Nie S, Phillips GO, Goff HD, Wang Q (2014) Study on Dendrobium officinale O-acetyl-glucomannan (Dendronan®): Part I. Extraction, purification, and partial structural characterization. Bioact Carbohydr Diet Fibre 4:74–83
Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572
Yu C, Li Y, Li B, Liu X, Hao L, Chen J, Qian W, Li S, Wang G, Bai S (2010) Molecular analysis of phosphomannomutase (PMM) genes reveals a unique PMM duplication event in diverse Triticeae species and the main PMM isozymes in bread wheat tissues. BMC Plant Biol 10:214
Acknowledgments
This work was supported by the National Science Foundation of China Projects (Grant number 31370365), the Transformation of Agricultural Science and Technology Achievement Fund (Contract number 2013GB24910676), and the Science and Technology Planning Project of Guangdong Province (Project number 2012A020602100).
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JD conceived the experiments and experimental design. CH, SZ, and JT analyzed the data. ZY analyzed the polysaccharides. CH and JATdS collectively interpreted all data and results and wrote all drafts. All six authors approved the final draft for submission, take full public responsibility for the content, and abide and satisfy the conditions of authorship as defined by the four clauses of the ICMJE.
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ESM 1
Fig. S1 Schematic representation of the secondary structure of DoPMM by using two online software (http://distill.ucd.ie/porter/ and http://www.predictprotein.org/). The red area represents the core domain, the cyan area the cap domain, and the blue area the linker. Fig. S2 The tertiary structure of the DoPMM protein with a cap domain and a core domain. The tertiary structure was predicted by SWISS-MODEL (http://swissmodel.expasy.org/). Fig. S3 The DoPMM protein without the transmembrane spanning domain predicted by TMHMM v. 2.0 (http://www.cbs.dtu.dk/services/TMHMM/). Fig. S4 The two stages of development (vegetative and reproductive) of D. officinale. In vitro-derived seedlings about 8 cm in height in the vegetative stage were cultured on half-strength MS medium containing 0.1% activated carbon, 2% sucrose, and 0.6% agar (pH 5.4). Seedlings were grown in a growth chamber at 26 ± 1 °C, 40 μmol m−2 s−1, and a 12-h photoperiod. The flowering D. officinale plants, about 13 months old, were grown in a greenhouse (Guangzhou, China) under natural conditions. (DOCX 2591 kb)
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He, C., Zeng, S., Teixeira da Silva, J.A. et al. Molecular cloning and functional analysis of the phosphomannomutase (PMM) gene from Dendrobium officinale and evidence for the involvement of an abiotic stress response during germination. Protoplasma 254, 1693–1704 (2017). https://doi.org/10.1007/s00709-016-1044-1
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DOI: https://doi.org/10.1007/s00709-016-1044-1