Skip to main content
SpringerLink
Log in

Comparative proteomic analysis reveals the roots response to low root-zone temperature in Malus baccata

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Soil temperature is known to affect plant growth and productivity. In this study we found that low root-zone temperature (LRT) inhibited the growth of apple (Malus baccata Borkh.) seedlings. To elucidate the molecular mechanism of LRT response, we performed comparative proteome analysis of the apple roots under LRT for 6 days. Total proteins of roots were extracted and separated by two-dimensional gel electrophoresis (2-DE) and 29 differentially accumulated proteins were successfully identified by MALDI-TOF/TOF mass spectrometry. They were involved in protein transport/processing/degradation (21%), glycometabolism (20%), response to stress (14%), oxidoreductase activity (14%), protein binding (7%), RNA metabolism (7%), amino acid biosynthesis (3%) and others (14%). The results revealed that LRT inhibited glycometabolism and RNA metabolism. The up-regulated proteins which were associated with oxidoreductase activity, protein metabolism and defense response, might be involved in protection mechanisms against LRT stress in the apple seedlings. Subsequently, 8 proteins were selected for the mRNA quantification analysis, and we found 6 of them were consistently regulated between protein and mRNA levels. In addition, the enzyme activities in ascorbate–glutathione (AsA–GSH) cycle were determined, and APX activity was increased and GR activity was decreased under LRT, in consistent with the protein levels. This study provides new insights into the molecular mechanisms of M. baccata in responding to LRT.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Agrawal GK, Rakwal R (2006) Rice proteomics: a cornerstone for cereal food crop proteomes. Mass Spectrom Rev 25:1–53

    Article  CAS  Google Scholar 

  • Ahn SJ, Im YJ, Chung GC, Cho BH, Suh SR (1999) Physiological responses of grafted-cucumber leaves and rootstock roots affected by low root temperature. Sci Hortic 81:397–408

    Article  Google Scholar 

  • Airaki M, Leterrier M, Mateos RM, Valderrama R, Chaki M, Barroso JB, Del Río LA, Palma JM, Corpas FJ (2012) Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant Cell Environ 35:281–295

    Article  CAS  Google Scholar 

  • Allen RD, Webb RP, Schake SA (1997) Use of transgenic plants to study antioxidant defenses. Free Rad Biol Med 23:473–479

    Article  CAS  Google Scholar 

  • Anderson JV, Li QB, Haskell DW, Guy CL (1994) Structural organization of the spinach endoplasmic reticulum-luminal 70-kilodalton heat-shock cognate gene and expression of 70-kilodalton Heat-Shock genes during cold acclimation. Plant Physiol 104:1359–1370

    Article  CAS  Google Scholar 

  • Arisz SA, van W Rv, Roels W, Zhu JK, Haring MA, Munnik T (2013) Rapid phosphatidic acid accumulation in response to low temperature stress in Arabidopsis is generated through diacylglycerol kinase. Front Plant Sci 4:1

    Article  CAS  Google Scholar 

  • Badowiec A, Weidner S (2014) Proteomic changes in the roots of germinating Phaseolus vulgaris seeds in response to chilling stress and post-stress recovery. J Plant Physiol 171:389–398

    Article  CAS  Google Scholar 

  • Cao S, Zheng Y, Wang K, Jin P, Rui H (2009) Methyl jasmonate reduces chilling injury and enhances antioxidant enzyme activity in postharvest loquat fruit. Food Chem 115:1458–1463

    Article  CAS  Google Scholar 

  • Caraglia M, Marra M, Giuberti G, D’Alessandro MA, Budillon A, del Prete S, Lentini A, Beninati S, Abbruzzese A (2001) The role of eukaryotic initiation factor 5A in the control of cell proliferation and apoptosis. Amino Acids 20:91–104

    Article  CAS  Google Scholar 

  • Chew O, Whelan J, Millar AH (2003) Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278:46869–46877

    Article  CAS  Google Scholar 

  • Chou WC, Huang YW, Tsay WS, Chiang TY, Huang DD, Huang HJ (2004) Expression of genes encoding the rice translation initiation factor, eIF5A, is involved in developmental and environmental responses. Physiol Plant 121:50–57

    Article  CAS  Google Scholar 

  • Dar TA, Uddin M, Khan MMA, Hakeem KR, Jaleel H (2015) Jasmonates counter plant stress: a review. Environ Exp Bot 115:49–57

    Article  CAS  Google Scholar 

  • Davik J, Koehler G, From B, Torp T, Rohloff J, Eidem P, Wilson RC, Sønsteby A, Randall SK, Alsheikh M (2013) Dehydrin, alcohol dehydrogenase, and central metabolite levels are associated with cold tolerance in diploid strawberry (Fragaria spp.). Planta 237:265–277

    Article  CAS  Google Scholar 

  • Deng G, Liu LJ, Zhong XY, Lao CY, Wang HY, Wang B, Zhu C, Shah F, Peng DX (2014) Comparative proteome analysis of the response of ramie under N, P and K deficiency. Planta 239:1175–1186

    Article  CAS  Google Scholar 

  • Ding X, Lv ZM, Zhao Y, Min H, Yang WJ (2008) MTH1745, a protein disulfide isomerase-like protein from thermophilic archaea, Methanothermobacter thermoautotrophicum involving in stress response. Cell Stress Chaperon 13:239–246

    Article  CAS  Google Scholar 

  • Domisch T, Finér L, Lehto T (2001) Effects of soil temperature on biomass and carbohydrate allocation in Scots pine (Pinus sylvestris) seedlings at the beginning of the growing season. Tree Physiol 21:465–472

    Article  CAS  Google Scholar 

  • Drążkiewicz M, Skórzyńska-Polit E, Krupa Z (2003) Response of the ascorbate–glutathione cycle to excess copper in Arabidopsis thaliana (L.). Plant Sci 164:195–202

    Article  Google Scholar 

  • Duguay J, Jamal S, Liu Z, Wang TW, Thompson JE (2007) Leaf-specific suppression of deoxyhypusine synthase in Arabidopsis thaliana enhances growth without negative pleiotropic effects. J Plant Physiol 164:408–420

    Article  CAS  Google Scholar 

  • Edwards EA, Rawsthorne S, Mullineaux PM (1990) Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.). Planta 180:278–284

    Article  CAS  Google Scholar 

  • Gambino G, Perrone I, Gribaudo I (2008) A Rapid and effective method for RNA extraction from different tissues of grapevine and other woody plants. Phytochem Anal 19:520–525

    Article  CAS  Google Scholar 

  • Grodzinski B, Jiao J, Knowles VL, Plaxton WC (1999) Photosynthesis and carbon partitioning in transgenic tobacco plants deficient in leaf cytosolic pyruvate kinase. Plant Physiol 120:887–896

    Article  CAS  Google Scholar 

  • Gu XC, Chen JF, Xiao Y, Di P, Xuan HJ, Zhou X, Zhang L, Chen WS (2012) Overexpression of allene oxide cyclase promoted tanshinone/phenolic acid production in Salvia miltiorrhiza. Plant Cell Rep 31:2247–2259

    Article  CAS  Google Scholar 

  • He J, Qin J, Long L, Ma Y, Li H, Li K, Jiang X, Liu T, Polle A, Liang Z, Luo ZB (2011) Net cadmium flux and accumulation reveal tissue-specific oxidative stress and detoxification in Populus × canescens. Physiol Plant 143:50–63

    Article  CAS  Google Scholar 

  • Hong S, Huaiyu M, Deguo L (2016) Effects of calcium on mitochondrial function and antioxidant defense in roots of apple rootstock (Malus baccata Borkh.) under rapid changes in temperature. Res J Biotech 11:55–63

    Article  CAS  Google Scholar 

  • Hu Y, Jiang L, Wang F, Yu D (2013) Jasmonate regulates the inducer of cbf expression-C-repeat binding factor/DRE binding factor 1 cascade and freezing tolerance in Arabidopsis. Plant Cell 25:2907–2924

    Article  CAS  Google Scholar 

  • Huang LB, Ye ZQ, Bell RW, Dell B (2005) Boron nutrition and chilling tolerance of warm climate crop species. Ann Bot 96:755–767

    Article  CAS  Google Scholar 

  • Janmohammadi M, Zolla L, Rinalducci S (2015) Low temperature tolerance in plants: Changes at the protein level. Phytochemistry 117:76–89

    Article  CAS  Google Scholar 

  • Jarillo JA, Capel J, Leyva A, Martínez-Zapater JM, Salinas J (1994) Two related low-temperature-inducible genes of Arabidopsis encode proteins showing high homology to 14-3-3 proteins, a family of putative kinase regulators. Plant Mol Biol 25:693–704

    Article  CAS  Google Scholar 

  • Kang HM, Saltveit ME (2002) Effect of chilling on antioxidant enzymes and DPPH-radical scavenging activity of high- and low-vigour cucumber seedling radicles. Plant Cell Environ 25:1233–1238

    Article  CAS  Google Scholar 

  • Kim JM, Sasaki T, Ueda M, Sako K, Seki M (2015) Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Front Plant Sci 6:114

    PubMed  PubMed Central  Google Scholar 

  • Kuk YI, Shin JS, Burgos NR, Hwang TE, Han O, Cho BH, Jung S, Guh JO (2003) Antioxidative enzymes offer protection from chilling damage in rice plants. Crop Sci 43:2109–2117

    Article  CAS  Google Scholar 

  • Kumar SP, Varman PAM, Kumari BR (2011) Identification of differentially expressed proteins in response to Pb stress in Catharanthus roseus. Afr J Environ Sci Technol 5:689–699

    CAS  Google Scholar 

  • Lauro FM, Tran K, Vezzi A, Vitulo N, Valle G, Bartlett DH (2008) Large-scale transposon mutagenesis of photobacterium profundum SS9 reveals new genetic loci important for growth at low temperature and high pressure. J Bacteriol 190:1699–1709

    Article  CAS  Google Scholar 

  • Li W, Wei Z, Qiao Z, Wu Z, Cheng L, Wang Y (2013) Proteomics analysis of alfalfa response to heat stress. PLoS One 8:e82725

    Article  Google Scholar 

  • Liu H, Sultan MARF, Liu XL, Zhang J, Yu F, Zhao H (2015) Physiological and comparative proteomic analysis reveals different drought responses in roots and leaves of drought-tolerant wild wheat (Triticum boeoticum). PLoS One 10:e0121852

    Article  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Lu DP, Christopher DA (2008) Endoplasmic reticulum stress activates the expression of a sub-group of protein disulfide isomerase genes and AtbZIP60 modulates the response in Arabidopsis thaliana. Mol Genet Genom 280:199–210

    Article  CAS  Google Scholar 

  • Mori H, Tanizawa K, Fukui T (1993) A chimeric alpha-glucan phosphorylase of plant type L and H isozymes. Functional role of 78-residue insertion in type L isozyme. J Biol Chem 268:5574–5581

    CAS  PubMed  Google Scholar 

  • Narindrasorasak S, Yao P, Sarkar B (2003) Protein disulfide isomerase, a multifunctional protein chaperone, shows copper-binding activity. Biochem Biophys Res Commun 311:405–414

    Article  CAS  Google Scholar 

  • Page D, Gouble B, Valot B, Bouchet JP, Callot C, Kretzschmar A, Causse M, Renard CMCG., Faurobert M (2010) Protective proteins are differentially expressed in tomato genotypes differing for their tolerance to low-temperature storage. Planta 232:483–500

    Article  CAS  Google Scholar 

  • Peters JS, Frenkel C (2004) Relationship between alcohol dehydrogenase activity and low-temperature in two maize genotypes, Silverado F 1 and Adh1-Adh2–doubly null. Plant Physiol Biochem 42:841–846

    Article  CAS  Google Scholar 

  • Pi Y, Jiang K, Cao Y, Wang Q, Huang Z, Li L, Hu L, Li W, Sun X, Tang K (2008) Allene oxide cyclase from Camptotheca acuminata improves tolerance against low temperature and salt stress in tobacco and bacteria. Mol Biotechnol 41:115–122

    Article  Google Scholar 

  • Polle A, Chakrabarti K, Schürmann W, Renneberg H (1990) Composition and properties of hydrogen peroxide decomposing systems in extracellular and total extracts from needles of Norway Spruce (Picea abies L., Karst.). Plant Physiol 94:312–319

    Article  CAS  Google Scholar 

  • Renaut J, Lutts S, Hoffmann L, Hausman JF (2004) Responses of poplar to chilling temperatures: proteomic and physiological aspects. Plant Biol 6:81–90

    Article  CAS  Google Scholar 

  • Riga P (2015) Effect of rootstock on growth, fruit production and quality of tomato plants grown under low temperature and light conditions. Hortic Environ Biotechnol 56:626–638

    Article  CAS  Google Scholar 

  • Simões AE, Pereira DM, Amaral JD, Nunes AF, Gomes SE, Rodrigues PM, Lo AC, D’Hooge R, Steer CJ, Thibodeau SN, Borralho PM, Rodrigues CM (2013) Efficient recovery of proteins from multiple source samples after trizol® or trizol®LS RNA extraction and long-term storage. BMC Genom 14:1–15

    Article  Google Scholar 

  • Solfjeld I, Johnsen Ø (2006) The influence of root-zone temperature on growth of Betula pendula Roth. Trees 20:320–328

    Article  Google Scholar 

  • Su H, Li L, Ma H, Lyu D, Sun J (2016) Calcium alleviates temperature stress by regulating nitrogen and respiratory metabolism in Malus baccata roots. Int J Agric Biol 18:286–292

    Article  CAS  Google Scholar 

  • Tai SL, Daran-Lapujade P, Luttik MAH, Walsh MC, Diderich JA, Krijger GC, van Gulik WM, Pronk JT, Daran JM (2007) Control of the glycolytic flux in Saccharomyces cerevisiae grown at low temperature: a multi-level analysis in anaerobic chemostat cultures. J Biol Chem 282:10243–10251

    Article  CAS  Google Scholar 

  • Thompson JE, Hopkins MT, Taylor C, Wang TW (2004) Regulation of senescence by eukaryotic translation initiation factor 5A: implications for plant growth and development. Trends Plant Sci 9:174–179

    Article  CAS  Google Scholar 

  • Tougou M, Hashiguchi A, Yukawa K, Nanjo Y, Hiraga S, Nakamura T, Nishizawa K, Komatsu S (2012) Responses to flooding stress in soybean seedlings with the alcohol dehydrogenase transgene. Plant Biotechnol 29:301–305

    Article  CAS  Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66

    Article  CAS  Google Scholar 

  • Walker JM (1969) One-degree increments in soil temperatures affect maize seedling behavior. Soil Sci Soc Am J 33:729–736

    Article  Google Scholar 

  • Wang TW, Lu L, Wang D, Thompson JE (2001) Isolation and characterization of senescence-induced cDNAs encoding deoxyhypusine synthase and eucaryotic translation initiation factor 5A from tomato. J Biol Chem 276:17541–17549

    Article  CAS  Google Scholar 

  • Wang L, Liu X, Liang M, Tan F, Liang W, Chen Y, Lin Y, Huang L, Xing J, Chen W (2014) Proteomic analysis of salt-responsive proteins in the leaves of Mangrove Kandelia candel during short-term stress. PLoS One 9:e83141

    Article  Google Scholar 

  • Wu X, Xu C, Wang W (2017) Reduction and alkylation of proteins in 2D gel electrophoresis: before or after isoelectric focusing? Front Chem 5:59

    Article  Google Scholar 

  • Xu J, Zhang B, Jiang C, Ming F (2011) RceIF5A, encoding an eukaryotic translation initiation factor 5A in Rosa chinensis, can enhance thermotolerance, oxidative and osmotic stress resistance of Arabidopsis thaliana. Plant Mol Biol 75:167–178

    Article  CAS  Google Scholar 

  • Yamori W, Hikosaka K, Way DA (2014) Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosyn Res 119:101–117

    Article  CAS  Google Scholar 

  • Yan QY, Duan ZQ, Mao JD, Li X, Dong F (2013) Low root zone temperature limits nutrient effects on cucumber seedling growth and induces adversity physiological response. J Integr Agric 12:1450–1460

    Article  Google Scholar 

  • Yang A, Akhtar S, Amjad M, Iqbal S, Jacobsen SE (2016) Growth and physiological responses of quinoa to drought and temperature stress. J Agron Crop Sci 202:445–453

    Article  CAS  Google Scholar 

  • Yoshida S, Eguchi H (1989) Effect of root temperature on gas exchange and water uptake in intact roots of cucumber plants (Cucumis sativus L.) in hydroponics. Biotronics Rep Biotron Inst 18:15–21

    Google Scholar 

  • Zeng Y, Yu J, Cang J, Liu L, Mu Y, Wang J, Zhang D (2011) Detection of sugar accumulation and expression levels of correlative key enzymes in winter wheat (Triticum aestivum) at low temperatures. Biosci Biotechnol Biochem 75:681–687

    Article  CAS  Google Scholar 

  • Zhang XM (2014) Effect of the calcium regulation on nitrogen metabolism of Malus baccata Borkh. Roots under mild hypothermia. Shenyang Agricultural University

  • Zhang Y, Feng F, He C (2012) Downregulation of OsPK1 contributes to oxidative stress and the variations in ABA/GA balance in rice. Plant Mol Biol Rep 30:1006–1013

    Article  CAS  Google Scholar 

  • Zhang XL, Liu GL, Li TL, Qi MF, Mei M, Lu XJ (2014b) Differential proteome analysis of mature and germinated seeds of Magnolia sieboldii K. Koch Trees 28:859–870

    Article  CAS  Google Scholar 

  • Zhao Y, Dong W, Zhang N, Ai X, Wang M, Huang Z, Xiao L, Xia G (2014) A wheat allene oxide cyclase gene enhances salinity tolerance via jasmonate signaling. Plant Physiol 164:1068–1076

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the Nation Natural Science Foundation of China (No. 31000887), China Agriculture Research System (No. CARS-28), Research and Demonstration of the Main Natural Disasters Prevention of Friuts Trees (No. 2014BAD16B0703), the Institutions of Higher Learning Fruit Tree Cultivation and Physio-Ecology Innovation Team of Liaoning Province (No. LT2014014), and the Science and Technology Research Projects for Apple of Liaoning Province (No. 2014204004).

Author information

Authors and Affiliations

  1. College of Horticulture, Shenyang Agricultural University, Shenyang, 110866, China

    Li-jie Li, Xiao-chen Lu, Huai-yu Ma & De-guo Lyu

  2. Key Lab of Fruit Quality Development and Regulation of Liaoning Province, Shenyang, 110866, China

    Huai-yu Ma & De-guo Lyu

Authors
  1. Li-jie Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiao-chen Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Huai-yu Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. De-guo Lyu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Huai-yu Ma or De-guo Lyu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Lj., Lu, Xc., Ma, Hy. et al. Comparative proteomic analysis reveals the roots response to low root-zone temperature in Malus baccata. J Plant Res 131, 865–878 (2018). https://doi.org/10.1007/s10265-018-1045-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-018-1045-6

Keywords

Search

Navigation