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Monday, 8 August 2016

Proteomic profile of Citrus grandis roots under long-term boron-deficiency revealed by iTRAQ

Published Date
Volume 30, Issue 4, pp 1057–1071

Title 

Proteomic profile of Citrus grandis roots under long-term boron-deficiency revealed by iTRAQ



  • Author 

Abstract

Key message

Eighty-six differentially abundant proteins were identified inCitrus grandisroots in response to boron-deficiency using the iTRAQ technique and possible mechanism underlying boron-deficiency tolerance of citrus plants was identified.

Abstract

Boron (B) is an essential element for plant growth and development and adequate B supply is an important determinant of good quality and high yield of crops. B-deficiency is a worldwide problem in agricultural production including citrus. However, little is known about the molecular mechanism of plant tolerance to B-deficiency. Using the iTRAQ technique, 86 differentially abundant proteins were identified from B-deficient Citrus grandis roots. The adaptive strategy of C. grandis roots under B-deficiency was summarized as follows: (1) enhancement of alternative splicing of mRNA and DNA methylation; (2) up-regulation of post-translation modification (PTM) and turnover of proteins; (3) reinforcement of cellular transport; (4) enhancement of antioxidant system and signal transduction. In general, these results increase our understanding of molecular mechanisms underlining the resistance of citrus plant under B-deficiency. Further studies should focus on how do roots perceive B deficiency in the rhizosphere and which pathway or proteins react to this adverse condition in the first place and then stimulates the downstream responses in Citrus plants.

References
  1. Ali AHN, Jarvis BC (1988) Effects of auxin and boron on nucleic acid metabolism and cell division during adventitious root regeneration. New Phytol 108:383–391CrossRef
  2. Alvarez S, Berla BM, Sheffield J, Cahoon RE, Jez JM, Hicks LM (2009) Comprehensive analysis of the Brassica juncea root proteome in response to cadmium exposure by complementary proteomic approaches. Proteomics 9(9):2419–2431CrossRefPubMed
  3. Alves M, Francisco R, Martins I, Ricardo CPP (2006) Analysis of Lupinus albus leaf apoplastic proteins in response to boron deficiency. Plant Soil 279:1–11CrossRef
  4. Alves M, Moes S, Jenö P, Pinheiro C, Passarinho J, Ricardo CP (2011) The analysis of Lupinus albus root proteome revealed cytoskeleton altered features due to long-term boron deficiency. J Proteomics 74:1351–1363CrossRefPubMed
  5. Besong BE, Lawanson AO (1991) Boron stress and mitochondrial quinone accumulation in Zea mays seedlings. J Plant Physiol 138:80–84CrossRef
  6. Byers DM, Gong H (2007) Acyl carrier protein: structure-function relationships in a conserved multifunctional protein family. Biochem Cell Biol 85(6):649–662CrossRefPubMed
  7. Cakmak L, Römhekd V (1997) Boron deficiency-induced impairments of cellular functions in plants. Plant Soil 193:71–83CrossRef
  8. Camacho-Cristóbal JJ, González-Fontes A (2007) Boron deficiency decreases plasmalemma H+-ATPase expression and nitrate uptake, and promotes ammonium assimilation into asparagine in tobacco roots. Planta 226:443–451CrossRefPubMed
  9. Cara FA, Sánchez E, Ruiz JM, Romero L (2002) Is phenol oxidation responsible for the short-term effects of boron deficiency on plasma-membrane permeability and function in squash roots? Plant Physiol Biochem 40:853–858CrossRef
  10. Chan DI, Vogel HJ (2010) Current understanding of fatty acid biosynthesis and the acyl carrier protein. Biochem J 430(3):559CrossRef
  11. Chapman HD (1968) The mineral nutrition of Citrus. In: Reuther W, Webber HJ, Batchelor LD (eds) The citrus industry, vol 2. Division of agricultural sciences, University of California, CA, pp 127–189
  12. Chaumont F, Barrieu F, Jung R, Chrispeels MJ (2000) Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity. Plant Physiol 122(4):1025–1034CrossRefPubMedPubMedCentral
  13. Chen LS, Han S, Qi Y, Yang LT (2012) Boron stresses and tolerance in citrus. Afr J Biotechnol 11:5961–5969
  14. Choi CS, Sano H (2007) Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants. Mol Genet Genome 277:589–600CrossRef
  15. Christensen AH, Sharrock RA, Quail PH (1992) Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol Biol 18:675–689CrossRefPubMed
  16. Cui G, Nan B, Hu J, Wang Y, Jin C, Xia B (2006) Identification and solution structures of a single domain biotin/lipoyl attachment protein from Bacillus subtilis. J Biol Chem 281(29):20598–20607CrossRefPubMed
  17. Dell B, Huang L (1997) Physiologic al response of plants to low boron. Plant Soil 193:103–120CrossRef
  18. Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM, Nery JR, Dixon JE, Ecker JR (2012) Widespread dynamic DNA methylation in response to biotic stress. Proc Natl Acad Sci USA 109(32):E2183–E2191CrossRefPubMedPubMedCentral
  19. El-Shintinawi F (1999) Structural and functional damage caused by boron deficiency in sunflower leaves. Photosynthetica 36:565–573CrossRef
  20. Garbarino JE, Rockhold DR, Belknap WR (1992) Expression of stress-responsive ubiquitin genes in potato tubers. Plant Mol Biol 20:235–244CrossRefPubMed
  21. Genschik P, Parmentier Y, Durr A, Marbach J, Criqui MC, Jamet E, Fleck J (1992) Ubiquitin genes are differentially regulated in protoplast-derived cultures of Nicotiana sylvestris and in response to various stresses. Plant Mol Biol 20:897–910CrossRefPubMed
  22. González-Fontes A, Rexach J, Quiles-Pando C, Herrera-Rodríguez MB, Camacho-Cristóbal JJ, Navarro-Gochiacoa MT (2013) Transcription factors as potential participants in the signal transduction pathway of boron deficiency. Plant Signal Behav 8(11):e2611CrossRef
  23. Han S, Chen LS, Jiang HX, Smith BR, Yang LT (2008) Boron deficiency decreases growth and photosynthesis, and increases starch and hexoses in leaves of citrus seedlings. J Plant Physiol 165:1331–1341CrossRefPubMed
  24. Han S, Tang N, Jiang H, Yang L, Li Y, Chen L (2009) CO2 assimilation, photosystem II photochemistry, carbohydrate metabolism and antioxidant system of citrus leaves in response to boron stress. Plant Sci 176:143–153CrossRef
  25. Hossain MA, da Silva JAT, Fujita M (2011) Glyoxalase system and reactive oxygen species detoxification system in plant abiotic stress response and tolerance: an intimate relationship. In: Shanker AK, Venkateswarlu B (eds) Abiotic stress in plants-mechanisms and adaptations. INTECH-Open Access Publisher, Rijeka, pp 235–266
  26. Huang JH, Cai ZJ, Wen SX, Guo P, Ye X, Lin GZ, Chen LS (2014) Effects of boron toxicity on root and leaf anatomy in two Citrus species differing in boron tolerance. Trees-Struct Funct 28:1653–1666CrossRef
  27. Jiang CC, Wang YH, Liu GD, Xia Y, Peng S, Zhong BL, Zeng QL (2009) Effect of boron on the leaf etiolation and fruit drop of Newhall Navel orange in southern Jiangxi. Plant Nutr Fert Sci 15:611–656
  28. Jiang HX, Yang LT, Qi YP, Lu YB, Huang ZR, Chen LS (2015) Root iTRAQ protein profile analysis of two citrus species differing in aluminum-tolerance in response to long-term aluminum-toxicity. BMC Genom 16:949CrossRef
  29. Kobayashi M, Matoh T, Azuma J (1996) Two chains of rhamnogalacturonan II are cross-linked by borate-diol ester bonds in higher plant cell walls. Plant Physiol 110:1017–1020PubMedPubMedCentral
  30. Kobayashi M, Mutoh T, Matoh T (2004) Boron nutrition of cultured tobacco BY-2 cells. IV. Genes induced under low boron supply. J Exp Bot 55:1441–1443CrossRefPubMed
  31. Kofler M, Motzny K, Freund C (2005) GYF domain proteomics reveals interaction sites in known and novel target proteins. Mol Cell Proteomics 4(11):1797–1811CrossRefPubMed
  32. Komander D (2009) The emerging complexity of protein ubiquitination. Biochem Soc Trans 37:937–953CrossRefPubMed
  33. Konsaeng S, Dell B, Rerkasen B (2005) A survey of woody tropical species for boron retranslocation. Plant Prod Sci 8:338–341CrossRef
  34. Krüger J, Thomas CM, Golstein C, Dixon MS, Smoker M, Tang S, Mulder L (2002) Jones JD (2002) A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296(5568):744–747CrossRefPubMed
  35. Kumar G, Srivastava N (2011) Genotoxic effects of two commonly used food additives of boric acid and sunset yellow in root meristems of Trigonella foenum-graecum. Iran J Environ Health Sci 8(4):361–366
  36. Labra M, Ghiani A, Citterio S, Sgorbati S, Sala F, Vannini C, Ruffini-Castiglione M, Bracale M (2002) Analysis of cytosine methylation pattern in response to water deficit in pea root tips. Plant Biol 4:694–699CrossRef
  37. Liu GD, Dong XC, Liu LC, Wu LS, Peng SA, Jiang CC (2015) Metabolic profiling reveals altered pattern of central metabolism in navel orange plants as a result of boron deficiency. Physiol Plant 153(4):513–524CrossRefPubMed
  38. Lyzenga WJ, Stone SL (2012) Abiotic stress tolerance mediated by protein ubiquitination. J Exp Bot 63(2):599–616CrossRefPubMed
  39. Milla MAR, Maurer A, Rodriguez Huete A, Gustafson JP (2003) Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signaling pathways. Plant J 36(5):602–615CrossRef
  40. Miwa K, Takano J, Fujiwara T (2006) Improvement of seed yields under boron-limiting conditions through overexpression of BOR1, a boron transporter for xylem loading, in Arabidopsis thaliana. Plant J 46:1084–1091CrossRefPubMed
  41. Mustafiz A, Singh AK, Pareek A, Sopory SK, Singla-Pareek SL (2011) Genome-wide analysis of rice and Arabidopsis identifies two glyoxalase genes that are highly expressed in abiotic stresses. Funct Integr Genomics 11(2):293–305CrossRefPubMed
  42. Ndong C, Anzellotti D, Ibrahim RK, Huner NP, Sarhan F (2003) Daphnetin methylation by a novel O-methyltransferase is associated with cold acclimation and photosystem II excitation pressure in rye. J Biol Chem 278(9):6854–6861CrossRefPubMed
  43. O’Neill MA, Warrenfeltz D, Kates K, Pellerin P, Doco T, Darill AG, Albersheim P (1996) Rhamnogalacturonan-II, a pectic polysaccharide in the walls of growing plant cell, forms a dimer that is covalently cross-linked by a borate ester. J Biol Chem 271:22923–22930CrossRefPubMed
  44. Pradet-Balade B, Boulme F, Beug H, Mullner EW, Garcia-Sanz JA (2001) Translation control: bridging the gap between genomics and proteomics? Trends Biochem Sci 26:225–229CrossRefPubMed
  45. Quiles-Pando C, Rexach J, Navarro-Gochicoa MT, Camacho-Cristóbal JJ, Herrera-Rodríguez MB, González-Fontes A (2013) Boron deficiency increases the levels of cytosolic Ca(2+) and expression of Ca(2+)-related genes in Arabidopsis thaliana roots. Plant Physiol Biochem 65:55–60CrossRefPubMed
  46. Reguera M, Bonilla I, Bolaños L (2010) Boron deficiency results in induction of pathogenesis-related proteins from the PR-10 family during the legume-rhizobia interaction. J Plant Physiol 167:623–632CrossRef
  47. Ross PL, Huang Y, Marchese JN, Williamson B, Parker K, Hattan S, Khainovski N, Pillai S, Dey S, Daniels S, Purkayastha S, Juhasz P, Martin S, Bartlet-Jones M, He F, Jacobson A, Pappin DJ (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 3:1154–1169CrossRefPubMed
  48. Ryden P, Sugimoto-Shirasu K, Smith AC, Findlay K, Reiter WD, McCann MC (2003) Tensile properties of Arabidopsis cell walls depend on both a xyloglucan cross-linked microfibrillar network and rhamnogalacturonan II-borate complexes. Plant Physiol 132:1033–1040CrossRefPubMedPubMedCentral
  49. Sang W, Huang ZR, Qi YP, Yang LT, Guo P, Chen LS (2015) An investigation of boron-toxicity in leaves of two citrus species differing in boron-tolerance using comparative proteomics. J Proteomics 123:128–146CrossRefPubMed
  50. Shorrocks VM (1997) The occurrence and correction of boron deficiency. Plant Soil 193:121–148CrossRef
  51. Singer AC, Crowley DE, Thompson IP (2003) Secondary plant metabolites in phytoremediation and biotransformation. Trends Biotechnol 21(3):123–130CrossRefPubMed
  52. Sun CW, Callis J (1997) Independent modulation of Arabidopsis thaliana polyubiquitin mRNAs in different organs and in response to environmental changes. Plant J 11:1017–1027CrossRefPubMed
  53. Tajima T, Yamaguchi A, Matsushima S, Satoh M, Hayasaka S, Yoshimatsu K, Shioi Y (2011) Biochemical and molecular characterization of senescence-related cysteine protease-cystatin complex from spinach leaf. Physiol Plant 141(2):97–116CrossRefPubMed
  54. Takano J, Wada M, Ludewig U, Schaaf G, von Wirén N, Fujiwara T (2006) The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 18:1498–1509CrossRefPubMedPubMedCentral
  55. Tanaka M, Fujiwara T (2008) Physiological roles and transport mechanisms of boron: perspectives from plants. Eur J Physiol 456:671–677CrossRef
  56. Tewari RK, Kumar P, Sharma PN (2010) Morphology and oxidative physiology of boron-deficient mulberry plants. Tree Physiol 30:68–77CrossRefPubMed
  57. van der Linde K, Hemetsberger C, Kastner C, Kaschani F, van der Hoorn RA, Kumlehn J, Doehlemann G (2012) A maize cystatin suppresses host immunity by inhibiting apoplastic cysteine proteases. Plant Cell 24(3):1285–1300CrossRefPubMedPubMedCentral
  58. Wang ZF, Wang ZH, Shi L, Wang LJ, Xu FS (2010) Proteomic alterations of Brassica napusroot in response to boron deficiency. Plant Mol Biol 74:265–278CrossRefPubMed
  59. Wang ZH, Wang ZF, Chen SS, Shi L, Xu FS (2011) Proteomics reveals the adaptability mechanism of Brassica napus to short-term boron deprivation. Plant Soil 347:195–210CrossRef
  60. Warington K (1923) The effect of boric acid and borax on the broad bean and certain other plants. Ann Bot 27:629–672
  61. Washburn MP, Koller A, Oshiro G, Ulaszek RR, Plouffe D, Deciu C, Winzeler E, Yates JR (2003) Protein pathway and complex clustering of correlated mRNA and protein expression analyses in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 100:3107–3112CrossRefPubMedPubMedCentral
  62. Wimmer MA, Eichert T (2013) Review: mechanisms for boron deficiency-mediated changes in plant water relations. Plant Sci 203–204:25–32CrossRefPubMed
  63. Yang LT, Jiang HX, Tang N, Chen LS (2011) Mechanisms of aluminum-tolerance in two species of citrus: secretion of organic acid anions and immobilization of aluminum by phosphorus in roots. Plant Sci 180:521–530CrossRefPubMed
  64. Yang GH, Yang LT, Jiang HX, Wang P, Chen LS (2012) Physiological impacts of magnesium-deficiency in Citrus seedlings: photosynthesis, antioxidant system and carbohydrates. Trees-Struct Funct 26(4):1237–1250CrossRef
  65. Yang LT, Qi YP, Lu YB, Guo P, Sang W, Feng F, Zhang HX, Chen LS (2013) iTRAQ protein profile analysis of Citrus sinensis roots in response to long-term boron-deficiency. Proteomics 93:179–206CrossRefPubMed
  66. Zemach A, Grafi G (2007) Methyl-CpG-binding domain proteins in plants: interpreters of DNA methylation. Trends Plant Sci 12(2):80–85CrossRefPubMed
  67. Zhou C, Qi Y, You X, Yang L, Guo P, Ye X, Zhou XX, Ke FJ, Chen LS (2013) Leaf cDNA-AFLP analysis of two citrus species differing in manganese tolerance in response to long-term manganese-toxicity. BMC Genom 14(1):621CrossRef


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http://link.springer.com/article/10.1007/s00468-015-1344-7

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