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Differential Expression of Proteins in Response to Molybdenum Deficiency in Winter Wheat Leaves Under Low-Temperature Stress

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Abstract

Molybdenum (Mo) is an essential micronutrient for plants. To obtain a better understanding of the molecular mechanisms of cold resistance enhanced by molybdenum application in winter wheat, we applied a proteomic approach to investigate the differential expression of proteins in response to molybdenum deficiency in winter wheat leaves under low-temperature stress. Of 13 protein spots that were identified, five spots were involved in the light reaction of photosynthesis, five were involved in the dark reaction of photosynthesis, and three were highly involved in RNA binding and protein synthesis. Before the application of cold stress, four differentially expressed proteins between the Mo deficiency (−Mo) vs. Mo application (+Mo) comparison are involved in carbon metabolism and photosynthetic electron transport. After 48 h of cold stress, nine differentially expressed proteins between the −Mo vs. +Mo comparison are involved in carbon metabolism, photosynthetic electron transport, RNA binding, and protein synthesis. Under −Mo condition, cold stress induced a more than twofold decrease in the accumulation of six differential proteins including ribulose bisphosphate carboxylase large-chain precursor, phosphoglycerate kinase, cp31BHv, chlorophyll a/b-binding protein, ribulose bisphosphate carboxylase small subunit, and ribosomal protein P1, whereas under +Mo condition cold stress only decreased the expression of RuBisCO large subunit, suggesting that Mo application might contribute to the balance or stability of these proteins especially under low-temperature stress and that Mo deficiency has greater influence on differential protein expression in winter wheat after low-temperature stress. Further investigations showed that Mo deficiency decreased the concentrations of chlorophyll a, chlorophyll b, and carotenoids; the maximum net photosynthetic rate; the apparent quantum yield; and carboxylation efficiency, even before the application of the cold stress, although the decrease rates were greater after 48 h of cold treatment, which is consistent with changes in the expressions of differential proteins in winter wheat under low-temperature stress. These findings provide some new evidence that Mo might be involved in the light and dark reaction of photosynthesis and protein synthesis.

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Abbreviations

2-DE:

Two-dimensional electrophoresis

AQY:

Apparent quantum yield

CE:

Carboxylation efficiency

P max :

Maximum net photosynthetic rate

RuBisCO:

Ribulose-1,5-bisphosphate carboxylase/oxygenase

References

  • Agarwala SC, Sharma CP, Farooq S, Chatterjee C (1978) Effect of molybdenum deficiency on the growth and metabolism of corn plants raised in sand culture. Can J Bot 56:1905–1908

    Article  CAS  Google Scholar 

  • Bahrman N, Le Gouis J, Negroni L et al (2004) Differential protein expression assessed by two-dimensional gel electrophoresis for two wheat varieties grown at four nitrogen levels. Proteomics 4:709–719

    Article  CAS  PubMed  Google Scholar 

  • Basyuni M, Kinjo Y, Baba S et al (2010) Isolation of salt stress tolerance genes from roots of mangrove plant, Rhizophora stylosa Griff., using PCR-based suppression subtractive hybridization. Plant Mol Biol Report 29:533–543

    Article  Google Scholar 

  • Baxter I, Muthukumar B, Park HC et al (2008) Variation in molybdenum content across broadly distributed populations of Arabidopsis thaliana is controlled by a mitochondrial molybdenum transporter (MOT1). PLoS Genet 4:e1000004–e1000004. doi:10.1371/journal.pgen.1000004

    Article  PubMed Central  PubMed  Google Scholar 

  • Campo RJ, Araujo RS, Hungria M (2009) Molybdenum-enriched soybean seeds enhance N accumulation, seed yield, and seed protein content in Brazil. Field Crop Res 110:219–224

    Article  Google Scholar 

  • Caruso G, Cavaliere C, Guarino C et al (2008) Identification of changes in Triticum durum L. leaf proteome in response to salt stress by two-dimensional electrophoresis and MALDI-TOF mass spectrometry. Anal Bioanal Chem 391:381–390

    Article  CAS  PubMed  Google Scholar 

  • Churin Y, Hess WR, Börner T (1999) Cloning and characterization of three cDNAs encoding chloroplast RNA-binding proteins from barley (Hordeum vulgare L.): differential regulation of expression by light and plastid development. Curr Genet 36:173–181

    Article  CAS  PubMed  Google Scholar 

  • Cramer WA, Zhang H, Yan J et al (2006) Transmembrane traffic in the cytochrome b6f complex. Annu Rev Biochem 75:769–790

    Google Scholar 

  • Deng Y, Li C, Shao Q et al (2012) Differential responses of double petal and multi petal jasmine to shading: I. Photosynthetic characteristics and chloroplast ultrastructure. Plant Physiol Biochem 55:93–102

    Article  CAS  PubMed  Google Scholar 

  • Ding C, You J, Liu Z et al (2011) Proteomic analysis of low nitrogen stress-responsive proteins in roots of rice. Plant Mol Biol Report 29:618–625

    Article  CAS  Google Scholar 

  • Dong M, Zhang X, Zhuang Z et al (2011) Characterization of the LhcSR gene under light and temperature stress in the green alga Ulva linza. Plant Mol Biol Report 30:10–16

    Article  Google Scholar 

  • Du H, Wu N, Chang Y et al (2013) Carotenoid deficiency impairs ABA and IAA biosynthesis and differentially affects drought and cold tolerance in rice. Plant Mol Biol 83:475–488

    Article  CAS  PubMed  Google Scholar 

  • Dupont FM (2008) Metabolic pathways of the wheat (Triticum aestivum) endosperm amyloplast revealed by proteomics. BMC Plant Biol 8:39

    Article  PubMed Central  PubMed  Google Scholar 

  • Ensminger I, Busch F, Huner N (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126:28–44

    Article  CAS  Google Scholar 

  • Guo P, Baum M, Grando S et al (2009) Differentially expressed genes between drought-tolerant and drought-sensitive barley genotypes in response to drought stress during the reproductive stage. J Exp Bot 60:3531–3544

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gupta UC (1997) Molybdenum in agriculture. Cambridge University Press, New York, p 57

  • Hou D-Y, Xu H, Du G-Y et al (2009) Proteome analysis of chloroplast proteins in stage albinism line of winter wheat (Triticum aestivum) FA85. BMB Rep 42:450–455

    Article  CAS  PubMed  Google Scholar 

  • Hu C, Wang Y, Wei W (2002) Effect of molybdenum applications on concentrations of free amino acids in winter wheat at different growth stages. J Plant Nutr 25:1487–1499

    Article  CAS  Google Scholar 

  • Ide Y, Kusano M, Oikawa A et al (2011) Effects of molybdenum deficiency and defects in molybdate transporter MOT1 on transcript accumulation and nitrogen/sulphur metabolism in Arabidopsis thaliana. J Exp Bot 62:1483–1497

    Article  CAS  PubMed  Google Scholar 

  • Izumi M, Tsunoda H, Suzuki Y et al (2012) RBCS1A and RBCS3B, two major members within the Arabidopsis RBCS multigene family, function to yield sufficient Rubisco content for leaf photosynthetic capacity. J Exp Bot 63:2159–2170

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kundu S, Chakraborty D, Das K et al (2013) An efficient in-gel digestion protocol for mass spectral analysis by MALDI-TOF-MS and MS/MS and its use for proteomic analysis of Vigna mungo leaves. Plant Mol Biol Report 31:47–54

    Article  CAS  Google Scholar 

  • Lan P, Li W, Wen T-N et al (2011) iTRAQ protein profile analysis of Arabidopsis roots reveals new aspects critical for iron homeostasis. Plant Physiol 155:821–834

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li W, Wang Z, Mi G et al (2001) Molybdenum deficiency in winter wheat seedlings as enhanced by freezing temperature. J Plant Nutr 24:1195–1203

    Article  CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Mendel RR, Kruse T (2012) Cell biology of molybdenum in plants and humans. Biochim Biophys Acta 1823:1568–1579

    Article  CAS  PubMed  Google Scholar 

  • Mininno M, Brugiere S, Pautre V et al (2012) Characterization of chloroplastic fructose 1,6-bisphosphate aldolases as lysine-methylated proteins in plants. J Biol Chem 287:21034–21044

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Olsson T, Leverenz JW (1994) Non- uniform stomatal closure and the apparent convexity of the photosynthetic photon flux density response curve. Plant Cell Environ 17:701–710

    Article  Google Scholar 

  • Prioul JL, Chartier P (1977) Partitioning of transfer and carboxylation components of intracellular resistance to photosynthetic CO2 fixation: a critical analysis of the methods used. Ann Bot 41:789–800

    Google Scholar 

  • Schwarz G, Mendel RR, Ribbe MW (2009) Molybdenum cofactors, enzymes and pathways. Nature 460:839–847

    Article  CAS  PubMed  Google Scholar 

  • Shao N, Vallon O, Dent R et al (2006) Defects in the cytochrome b6/f complex prevent light-induced expression of nuclear genes involved in chlorophyll biosynthesis. Plant Physiol 141:1128–1137

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58:199–217

    Article  CAS  PubMed  Google Scholar 

  • Stitt M, Hurry V (2002) A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. Curr Opin Plant Biol 5:199–206

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Hu C, Tan Q et al (2010) Endogenous hormone in response to molybdenum in winter wheat roots under low temperature stress. J Agric Environ 8:597–601

    CAS  Google Scholar 

  • Sun X, Hu C, Tan Q et al (2009) Effects of molybdenum on expression of cold-responsive genes in abscisic acid (ABA)-dependent and ABA-independent pathways in winter wheat under low-temperature stress. Ann Bot 104:345–356

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sun X, Tan Q, Hu C et al (2006) Effects of molybdenum on antioxidative enzymes in winter wheat under low temperature stress. Sci Agric Sin 39:952–959

    Google Scholar 

  • Tejada-jimenez M, Galván A, Fernández E, Tejada-Jiménez M (2011) Algae and humans share a molybdate transporter. Proc Natl Acad Sci U S A 108:6420–6425

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tomatsu H, Takano J, Takahashi H et al (2007) An Arabidopsis thaliana high-affinity molybdate transporter required for efficient uptake of molybdate from soil. Proc Natl Acad Sci U S A 104:18807–188012

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Uematsu K, Suzuki N, Iwamae T et al (2012) Increased fructose 1,6-bisphosphate aldolase in plastids enhances growth and photosynthesis of tobacco plants. J Exp Bot 63:3001–3009

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Xu C, Wang C, Wang Y (2012a) Characterization of a eukaryotic translation initiation factor 5A homolog from Tamarix androssowii involved in plant abiotic stress tolerance. BMC Plant Biol 12:118

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang S-S, Song Z-B, Sun Z et al (2012b) Effects of formaldehyde stress on physiological characteristics and gene expression associated with photosynthesis in Arabidopsis thaliana. Plant Mol Biol Report 30:1291–1302

    Article  CAS  Google Scholar 

  • Wang Y, Wei W, Tan Q (1995) A study on molybdenum deficiency and molybdenum application of winter wheat in yellow-brown soil of Hubei province. Soil Fertil 8:24–28

    Google Scholar 

  • Winfield MO, Lu C, Wilson ID et al (2010) Plant responses to cold: transcriptome analysis of wheat. Plant Biotechnol J 8:749–771

    Article  CAS  PubMed  Google Scholar 

  • Wu L, Zu X, Wang X et al (2012) Comparative proteomic analysis of the effects of salicylic acid and abscisic acid on maize (Zea mays L.) leaves. Plant Mol Biol Report 31:507–516

    Article  CAS  Google Scholar 

  • Xu Y-H, Liu R, Yan L et al (2012) Light-harvesting chlorophyll a/b-binding proteins are required for stomatal response to abscisic acid in Arabidopsis. J Exp Bot 63:1095–1106

    Article  PubMed Central  PubMed  Google Scholar 

  • Yan JX, Wait R, Berkelman T et al (2000) A modified silver staining protocol for visualization of proteins compatible with matrix-assisted laser desorption/ionization and electrospray ionization–mass spectrometry. Electrophoresis 21:3666–3672

    Article  CAS  PubMed  Google Scholar 

  • Yaneva I, Mäck G, Vunkova-Radeva R, Tischner R (1996) Changes in nitrate reductase activity and the protective effect of molybdenum during cold stress in winter wheat grown on acid soil. J Plant Physiol 149:211–216

    Article  CAS  Google Scholar 

  • Yao Y, Ni Z, Du J et al (2006) Isolation and characterization of 15 genes encoding ribosomal proteins in wheat (Triticum aestivum L.). Plant Sci 170:579–586

    Article  CAS  Google Scholar 

  • Yin N, Ma X, Zhang W et al (2012) Analysis of differential proteins induced by forchlorfenuron in wheat. Plant Mol Biol Report 30:949–956

    Article  CAS  Google Scholar 

  • Yu M, Hu C, Sun X, Wang Y (2010) Influences of Mo on nitrate reductase, glutamine synthetase and nitrogen accumulation and utilization in Mo-efficient and Mo-inefficient winter wheat cultivars. Agric Sci China 9:355–361

    Article  CAS  Google Scholar 

  • Zhang Y, Fu J, Gu R et al (2008) Isolation and analysis of cold stress inducible genes in Zea mays by suppression subtractive hybridization and cDNA macroarray. Plant Mol Biol Report 27:38–49

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (program nos. 30671232 and .41171240) and the Fundamental Research Funds for the Central Universities (program nos. 2010QC037, 2010PY025, 2011PY150).

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Correspondence to Chengxiao Hu.

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Fig. S1

Sequence alignment of proteins CAA44027 (spot A1) and APP92166 (spot B1). Sequences were aligned in the online sequence alignment software Clustal Omega (http://www.ebi.ac.uk/Tools/msa/clustalo/) (JPEG 93 kb)

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Sun, X., Tan, Q., Nie, Z. et al. Differential Expression of Proteins in Response to Molybdenum Deficiency in Winter Wheat Leaves Under Low-Temperature Stress. Plant Mol Biol Rep 32, 1057–1069 (2014). https://doi.org/10.1007/s11105-014-0713-5

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