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Ascorbate metabolism in rice genotypes differing in zinc efficiency

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Abstract

Effects of zinc (Zn) deficiency on shoot metabolites were investigated in contrasting rice (Oryza sativa L.) genotypes with special focus on ascorbic acid (AsA) biosynthesis, recycling, and catabolism. The genotypes IR74 (sensitive) and RIL46 (tolerant) were subjected to −Zn and control treatments for 3 weeks, and samples were taken at three different stages representing the pre-stress phase, emergence of visible stress, and severe visible stress. The emergence of visible symptoms was paralleled by an increase in lipid peroxidation and a decrease in AsA concentration in the sensitive, but not in the tolerant genotype. The tolerant RIL46 showed enhanced transcript levels of several genes involved in the mannose/l-galactose pathway to AsA biosynthesis, and significant up-regulation of a gene involved in the putative alternative myo-inositol pathway under low Zn stress. The level of most AsA precursors was negatively affected by Zn deficiency, but RIL46 had a constitutively higher level of non-phosphorylated precursors. Products of AsA catabolism such as oxalate and threonate did not accumulate in either genotype, suggesting that AsA degradation did not contribute to the stress-induced decline of the AsA pool in IR74. Further factors possibly contributing to tolerance in RIL46 included an almost fivefold higher proline level under −Zn stress and significantly higher trehalose content. The implications of these compounds in AsA metabolism and Zn efficiency thus deserve further attention.

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Abbreviations

AsA:

Ascorbic acid

DHA:

Dehydroascorbic acid

DHAR:

Dehydroascorbic acid reductase

MDA:

Malondialdehyde

MDHA:

Monodehydroascorbic acid

MDHAR:

Monodehydroascorbic acid reductase

MIOX:

Myo-inositol oxygenase

PMI:

Phosphomannose isomerase

ROS:

Reactive oxygen species

QTL:

Quantitative trait locus

Zn:

Zinc

References

  • Agius F, Gonzalez-Lamothe R, Caballero JL, Munoz-Blanco J, Botella MA, Valpuesta V (2003) Engineering increased vitamin C levels in plants by overexpression of a d-galacturonic acid reductase. Nat Biotechnol 21:177–181

    Article  CAS  PubMed  Google Scholar 

  • Ahkami AH, Lischewski S, Haensch K-T, Porfirova S, Hofmann J, Rolletschek H, Melzer M, Franken P, Hause B, Druege U, Hajirezaei MR (2009) Molecular physiology of adventitious root formation in Petunia hybrida cuttings: involvement of wound response and primary metabolism. New Phytol 181:613–625

    Article  CAS  PubMed  Google Scholar 

  • Alloway BJ (2004) Zinc in soils and crop nutrition. International Fertilizer Industry Association, Paris

    Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Arnold T, Kirk GJD, Wissuwa M, Frei M, Zhao F-J, Mason TFD, Weiss DJ (2010) Evidence for the mechanisms of zinc uptake by rice using isotope fractionation. Plant Cell Environ 33:370–381

    Article  CAS  PubMed  Google Scholar 

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • Avonce N, Leyman B, Mascorro-Gallardo JO, Van Dijck P, Thevelein JM, Iturriaga G (2004) The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol 136:3649–3659

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bartoli CG, Guiamet JJ, Kiddle G, Pastori GM, Di Cagno R, Theodoulou FL, Foyer CH (2005) Ascorbate content of wheat leaves is not determined by maximal l-galactono-1,4-lactone dehydrogenase (GalLDH) activity under drought stress. Plant Cell Environ 28:1073–1081

    Article  CAS  Google Scholar 

  • Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702

    Article  CAS  PubMed  Google Scholar 

  • Cakmak I, Marschner H (1988) Enhanced superoxide radical production in roots of zinc deficient plants. J Exp Bot 39:1449–1460

    Article  Google Scholar 

  • Cakmak I, Marschner H, Bangerth F (1989) Effect of zinc nutritional status on growth, protein metabolism and levels of indole-3-acetic acid and other phytohormones in bean (Phaseolus vulgaris L.). J Exp Bot 40:405–412

    Article  CAS  Google Scholar 

  • Chen Z, Young TE, Ling J, Chang SC, Gallie DR (2003) Increasing vitamin C content of plants through enhanced ascorbate recycling. Proc Natl Acad Sci USA 100:3525–3530

    Article  CAS  PubMed  Google Scholar 

  • Conklin PL (2001) Recent advances in the role and biosynthesis of ascorbic acid in plants. Plant Cell Environ 24:383–394

    Article  CAS  Google Scholar 

  • Davey MW, Gilot C, Persiau G, Ostergaard J, Han Y, Bauw GC, Van Montagu MC (1999) Ascorbate biosynthesis in Arabidopsis cell suspension culture. Plant Physiol 121:535–543

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • DeBolt S, Hardie J, Tyerman S, Ford CM (2004) Composition and synthesis of raphide crystals and druse crystals in berries of Vitis vinifera L. cv. Cabernet Sauvignon: ascorbic acid as precursor for both oxalic and tartaric acids as revealed by radiolabelling studies. Aust J Grape Wine R 10:134–142

    Article  CAS  Google Scholar 

  • Dobermann A, Fairhurst T (2000) Rice: nutrient disorders & nutrient management. International Rice Research Institute, Los Banos

    Google Scholar 

  • Duan J, Zhang M, Zhang H, Xiong H, Liu P, Ali J, Li J, Li Z (2012) OsMIOX, a myo-inositol oxygenase gene, improves drought tolerance through scavenging of reactive oxygen species in rice (Oryza sativa L.). Plant Sci 196:143–151

    Article  CAS  PubMed  Google Scholar 

  • Endres S, Tenhaken R (2009) Myoinositol oxygenase controls the level of myoinositol in Arabidopsis, but does not increase ascorbic acid. Plant Physiol 149:1042–1049

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Frei M, Tanaka JP, Chen CP, Wissuwa M (2010a) Mechanisms of ozone tolerance in rice: characterization of two QTLs affecting leaf bronzing by gene expression profiling and biochemical analyses. J Exp Bot 61:1405–1417

    Article  CAS  PubMed  Google Scholar 

  • Frei M, Wang Y, Ismail AM, Wissuwa M (2010b) Biochemical factors conferring shoot tolerance to oxidative stress in rice grown in low zinc soil. Funct Plant Biol 37:74–84

    Article  CAS  Google Scholar 

  • French D (1954) The raffinose family of oligosaccharides. Adv Carbohyd Chem Bi 9:149–184

    Article  CAS  Google Scholar 

  • Garg AK, Kim JK, Owens TG, Ranwala AP, Do Choi Y, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99:15898–15903

    Article  CAS  PubMed  Google Scholar 

  • Goddijn OJM, van Dun K (1999) Trehalose metabolism in plants. Trends Plant Sci 4:315–319

    Article  PubMed  Google Scholar 

  • Gracy RW, Noltmann EA (1968a) Studies on phosphomannose isomerase. I. Isolation homogeneity measurements and determination of some physical properties. J Biol Chem 243:3161–3168

    CAS  PubMed  Google Scholar 

  • Gracy RW, Noltmann EA (1968b) Studies on phosphomannose isomerase: II. Characterization as a zinc metalloenzyme. J Biol Chem 243:4109–4116

    CAS  PubMed  Google Scholar 

  • Green MA, Fry SC (2005) Vitamin C degradation in plant cells via enzymatic hydrolysis of 4-O-oxalyl-l-threonate. Nature 433:83–87

    Article  CAS  PubMed  Google Scholar 

  • Guo ZF, Tan HQ, Zhu ZH, Lu SY, Zhou BY (2005) Effect of intermediates on ascorbic acid and oxalate biosynthesis of rice and in relation to its stress resistance. Plant Physiol Bioch 43:955–962

    Article  CAS  Google Scholar 

  • Hacisalihoglu G, Kochian LV (2003) How do some plants tolerate low levels of soil zinc? Mechanisms of zinc efficiency in crop plants. New Phytol 159:341–350

    Article  CAS  Google Scholar 

  • Hancock RD, Viola R (2005) Biosynthesis and catabolism of l-ascorbic acid in plants. Crit Rev Plant Sci 24:167–188

    Article  CAS  Google Scholar 

  • Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  CAS  Google Scholar 

  • Hoffland E, Wei C, Wissuwa M (2006) Organic anion exudation by lowland rice (Oryza sativa L.) at zinc and phosphorus deficiency. Plant Soil 283:155–162

    Article  CAS  Google Scholar 

  • Hossain MA, Asada K (1984) Purification of dehydroascorbate reductase from spinch and its characterization as a thiol enzyme. Plant Cell Physiol 25:85–92

    CAS  Google Scholar 

  • Hossain B, Hirata N, Nagatomo Y, Akashi R, Takaki H (1997) Internal zinc accumulation is correlated with increased growth in rice suspension culture. J Plant Growth Regul 16:239–243

    Article  CAS  Google Scholar 

  • Ishikawa T, Dowdle J, Smirnoff N (2006) Progress in manipulating ascorbic acid biosynthesis and accumulation in plants. Physiol Plant 126:343–355

    Article  CAS  Google Scholar 

  • Jo Y, Hyun TK (2011) Genome-wide identification of antioxidant component biosynthetic enzymes: comprehensive analysis of ascorbic acid and tocochromanols biosynthetic genes in rice. Comput Biol Chem 35:261–268

    Article  CAS  PubMed  Google Scholar 

  • Kitagishi K, Obata H (1986) Effects of zinc deficiency on the nitrogen-metabolism of meristematic tissue of rice plants with reference to protein synthesis. Soil Sci Plant Nutr 32:397–405

    Article  CAS  Google Scholar 

  • Linster CL, Clarke SG (2008) l-Ascorbate biosynthesis in higher plants: the role of VTC2. Trends Plant Sci 13:567–573

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Loewus FA, Kelly S (1961) Identity of l-ascorbic acid formed by d-glucose by strawberry (Fragaria). Nature 191:1059–1061

    Article  CAS  PubMed  Google Scholar 

  • Lorence A, Chevone BI, Mendes P, Nessler CL (2004) myo-Inositol oxygenase offers a possible entry point into plant ascorbate biosynthesis. Plant Physiol 134:1200–1205

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Luo Y, Li W-M, Wang W (2008) Trehalose: protector of antioxidant enzymes or reactive oxygen species scavenger under heat stress? Environ Exp Bot 63:378–384

    Article  CAS  Google Scholar 

  • Maruta T, Yonemitsu M, Yabuta Y, Tamoi M, Ishikawa T, Shigeoka S (2008) Arabidopsis phosphomannose isomerase 1, but not phosphomannose isomerase 2 is essential for ascorbic acid biosynthesis. J Biol Chem 283:28842–28851

    Article  CAS  PubMed  Google Scholar 

  • Matysik J, Alia, Bhalu B, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci India 82:525–532

    CAS  Google Scholar 

  • Molinari HBC, Marur CJ, Daros E, De Campos MKF, De Carvalho JFRP, Pereira LFP, Vieira LGE (2007) Evaluation of the stress-inducible production of proline in transgenic sugarcane (Saccharum spp.): osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiol Plant 130:218–229

    Article  CAS  Google Scholar 

  • Naqvi S, Zhu C, Farre G, Ramessar K, Bassie L, Breitenbach J, Perez Conesa D, Ros G, Sandmann G, Capell T, Christou P (2009) Transgenic multivitamin corn through biofortification of endosperm with three vitamins representing three distinct metabolic pathways. Proc Natl Acad Sci USA 106:7762–7767

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  CAS  PubMed  Google Scholar 

  • Parsons HT, Yasmin T, Fry SC (2011) Alternative pathways of dehydroascorbic acid degradation in vitro and in plant cell cultures: novel insights into vitamin C catabolism. Biochem J 440:375–383

    Article  CAS  PubMed  Google Scholar 

  • Patel RK, Jain M (2011) PlantRGS: a web server for the identification of most suitable candidate reference genes for quantitative gene expression studies in plants. DNA Res 18:463–470

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Possingham JV (1956) The effect of mineral nutrition on the content of free amino acids and amides in tomato plants. Aust J Biol Sci 9:539–551

    CAS  Google Scholar 

  • Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709

    Article  CAS  PubMed  Google Scholar 

  • Rontein D, Basset G, Hanson AD (2002) Metabolic engineering of osmoprotectant accumulation in plants. Metab Eng 4:49–56

    Article  CAS  PubMed  Google Scholar 

  • Rose MT, Rose TJ, Pariasca-Tanaka J, Widodo, Wissuwa M (2011) Revisiting the role of organic acids in the bicarbonate tolerance of zinc-efficient rice genotypes. Funct Plant Biol 38:493–504

    CAS  Google Scholar 

  • Rose MT, Rose TJ, Pariasca-Tanaka J, Yoshihashi T, Neuweger H, Goesmann A, Frei M, Wissuwa M (2012) Root metabolic response of rice (Oryza sativa L.) genotypes with contrasting tolerance to zinc deficiency and bicarbonate excess. Planta 236:959–973

    Article  CAS  PubMed  Google Scholar 

  • Smirnoff N (1996) Botanical briefing: the function and metabolism of ascorbic acid in plants. Ann Bot 78:661–669

    Article  CAS  Google Scholar 

  • Smirnoff N, Wheeler GL (2000) Ascorbic acid in plants: biosynthesis and function. Crit Rev Plant Sci 19:267–290

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Tausz M, Sircelj H, Grill D (2004) The glutathione system as a stress marker in plant ecophysiology: is a stress-response concept valid? J Exp Bot 55:1955–1962

    Article  CAS  PubMed  Google Scholar 

  • Tripathi B, Gaur J (2004) Relationship between copper-and zinc-induced oxidative stress and proline accumulation in Scenedesmus sp. Planta 219:397–404

    Article  CAS  PubMed  Google Scholar 

  • Ueda Y, Wu LB, Frei M (2013) A critical comparison of two high throughput ascorbate analyses methods for plant samples. Plant Physiol Bioch 70:418–423

    Article  CAS  Google Scholar 

  • Wheeler GL, Jones MA, Smirnoff N (1998) The biosynthetic pathway of vitamin C in higher plants. Nature 393:365–369

    Article  CAS  PubMed  Google Scholar 

  • Widodo B, Broadley MR, Rose T, Frei M, Pariasca-Tanaka J, Yoshihashi T, Thomson M, Hammond JP, Aprile A, Close TJ, Ismail AM, Wissuwa M (2010) Response to zinc deficiency of two rice lines with contrasting tolerance is determined by root growth maintenance and organic acid exudation rates, and not by zinc-transporter activity. New Phytol 186:400–414

    Article  PubMed  Google Scholar 

  • Wingler A, Wingler (2002) The function of trehalose biosynthesis in plants. Phytochemistry 60:437–440

    Article  CAS  PubMed  Google Scholar 

  • Wissuwa M, Ismail AM, Yanagihara S (2006) Effects of zinc deficiency on rice growth and genetic factors contributing to tolerance. Plant Physiol 142:731–741

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wolucka BA, Van Montagu M (2003) GDP-mannose 3′, 5′-epimerase forms GDP-l-gulose, a putative intermediate for the de novo biosynthesis of vitamin C in plants. J Biol Chem 278:47483–47490

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was partly funded by Deutsche Forschungsgemeinschaft (FR2952/1-1).

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Correspondence to Michael Frei.

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Höller, S., Hajirezaei, MR., von Wirén, N. et al. Ascorbate metabolism in rice genotypes differing in zinc efficiency. Planta 239, 367–379 (2014). https://doi.org/10.1007/s00425-013-1978-x

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