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Phosphorus-mediated alleviation of aluminum toxicity revealed by the iTRAQ technique in Citrus grandis roots


Autoři: Lin-Tong Yang aff001;  Yang-Fei Zhou aff001;  Yan-Yu Wang aff001;  Yan-Mei Wu aff001;  Bing Qian aff001;  Heng Wang aff001;  Li-Song Chen aff001
Působiště autorů: Institute of Plant Nutritional Physiology and Molecular Biology, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, China aff001;  Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, Fujian Agriculture and Forestry University, Fuzhou, China aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223516

Souhrn

Citrus grandis seedlings were irrigated with nutrient solutions with four Al-P combinations [two Al levels (0 mM and 1.2 mM AlCl3·6H2O) × two P levels (0 μM and 200 μM KH2PO4)] for 18 weeks. Al dramatically inhibited the growth of C. grandis seedlings, as revealed by a decreased dry weight of roots and shoots. Elevating P level could ameliorate the Al-induced growth inhibition and organic acid (malate and citrate) secretion in C. grandis. Using a comparative proteomic approach revealed by the isobaric tags for relative and absolute quantification (iTRAQ) technique, 318 differentially abundant proteins (DAPs) were successfully identified and quantified in this study. The possible mechanisms underlying P-induced alleviation of Al toxicity in C. grandis were proposed. Furthermore, some DAPs, such as GLN phosphoribosyl pyrophosphate amidotransferase 2, ATP-dependent caseinolytic (Clp) protease/crotonase family protein, methionine-S-oxide reductase B2, ABC transporter I family member 17 and pyridoxal phosphate phosphatase, were reported for the first time to respond to Al stress in Citrus plants. Our study provides some proteomic details about the alleviative effects of P on Al toxicity in C. grandis, however, the exact function of the DAPs identified herein in response to Al tolerance in plants must be further investigated.

Klíčová slova:

Cellular stress responses – Membrane proteins – Plant resistance to abiotic stress – Protein metabolism – Rice – Secretion – Starches – Toxicity


Zdroje

1. Zhou D.; Yang Y.; Zhang J.; Jiang F.; Craft E.; Thannhauser T.W.; Kochian L.V.; Liu J. Quantitative iTRAQ proteomics revealed possible roles for antioxidant proteins in sorghum aluminum tolerance. Front. Plant Sci. 2017; 7, 2043. doi: 10.3389/fpls.2016.02043 28119720

2. Wang C.Y.; Shen R.F.; Wang C.; Wang W. Root protein profile changes induced by Al exposure in two rice cultivars differing in Al tolerance. J. Proteomics 2013; 78, 281–293. doi: 10.1016/j.jprot.2012.09.035 23059537

3. Yang Q.S.; Wang Y.Q.; Zhang J.J.; Shi W.P.; Qian C.M.; Peng X.X. Identification of aluminum-responsive proteins in rice roots by a proteomic approach: Cysteine synthase as a key player in Al response. Proteomics 2007; 7, 737–749. doi: 10.1002/pmic.200600703 17295357

4. Kumari M, Taylor GJ, Deyholos MK: Transcriptomic responses to aluminum stress in roots of Arabidopsis thaliana. Molecular Genetics & Genomics 2008; 279(4):339–357.

5. Oh M.W.; Roy S.K.; Kamal A.H.; Cho K.; Cho S.W.; Park C.S.; Choi J.S.; Komatsu S.; Woo S.H. Proteome analysis of roots of wheat seedlings under aluminum stress. Mol. Biol. Rep. 2014; 41(2), 671. doi: 10.1007/s11033-013-2905-8 24357239

6. Zhen Y.; Qi J.L.; Wang S.S.; Su J.; Xu G.H.; Zhang M.S.; Miao L.; Peng X.X.; Tian D.C.; Yang Y.H. Comparative proteome analysis of differentially expressed proteins induced by Al toxicity in soybean. Physiol. Plantarum 2007; 131(4), 542–545.

7. Yang L.T.; Liu J.W.; Wu Y.M.; Qi Y.P.; Wang J.L.; Lai N.W.; Ye X.; Chen L.S. Proteome profile analysis of boron-induced alleviation of aluminum-toxicity in Citrus grandis roots. Ecotox. Environ. Safe. 2018; 162, 488–498.

8. Guo P.; Li Q.; Qi Y.P.; Yang L.T.; Ye X.; Chen H.H.; Chen L.S. Sulfur-mediated-alleviation of aluminum-toxicity in Citrus grandis seedlings. Int. J. Mol. Sci. 2017; 18, 2570.

9. Guo P.; Qi Y.P.; Yang L.T.; Lai. N.W.; Ye, X.; Yang, Y.; Chen, L.S. Root adaptive responses to aluminum-treatment revealed by RNA-seq in two citrus species with different aluminum-tolerance. Front. Plant Sci. 2017; 8, 330. doi: 10.3389/fpls.2017.00330 28337215

10. Jiang H.X.; Tang N.; Zheng J.G.; Li Y.; Chen L.S. Phosphorus alleviates aluminum-induced inhibition of growth and photosynthesis in Citrus grandis seedlings. Physiol. Plant. 2009; 137(3), 298–311. doi: 10.1111/j.1399-3054.2009.01288.x 19832942

11. Kochian L.V.; Pineros M.A.; Liu J.; Magalhaes J.V. Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Ann. Rev. Plant Biol. 2015; 66, 571–598.

12. Ma J.F.; Ryan P.R.; Delhaize E. Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci. 2001; 6, 273–278. 11378470

13. Sasaki T.; Yamamoto Y.; Ezaki B.; Katsuhara M.; Ahn S.J.; Ryan P.R.; Delhaize E.; Matsumoto H. A wheat gene encoding an aluminum-activated malate transporter. Plant J. 2004; 37, 645–53. doi: 10.1111/j.1365-313x.2003.01991.x 14871306

14. Magalhaes J.V.; Liu J.; Guimaraes C.T.; Lana U.G.P.; Alves V.M.C., Wang Y.H., et al. A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat. Genet. 2007; 39, 1156–1161. doi: 10.1038/ng2074 17721535

15. Huang C.F; Yamaji N.; Mitani N.; Yano M.; Nagamura Y.; Ma J.F. A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell 2009; 21, 655–667. doi: 10.1105/tpc.108.064543 19244140

16. Larsen P.B.; Cancel J.; Rounds M.; Ochoa V. Arabidopsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment. Planta 2007; 225, 1447–1458. doi: 10.1007/s00425-006-0452-4 17171374

17. Negishi T.; Oshima K.; Hattori M.; Kanai M.; Mano S.; Nishimura M.; Yoshida K. Tonoplast- and plasma membrane-localized aquaporin-family transporters in blue hydrangea sepals of aluminum hyperaccumulating plant. PLoS One 2012; 7, e43189. doi: 10.1371/journal.pone.0043189 22952644

18. Fujii M.; Yokosho K.; Yamaji N.; Saisho D.; Yamane M.; Takahashi H.; Sato K.; Nakazono M.; Ma J.F. Acquisition of aluminium tolerance by modification of a single gene in barley. Nature Commun. 2012; 3, 713.

19. Li J.Y.; Liu J.; Dong D.; Jia X.; McCouch S.R; Kochian L.V. Natural variation underlies alterations in Nramp aluminum transporter (NRAT1) expression and function that play a key role in rice aluminum tolerance. Proc. Natl. Acad. Sci. 2014; 111, 6503–6508 doi: 10.1073/pnas.1318975111 24728832

20. Jiang H.X.; Yang L.T.; Qi Y.P.; Lu Y.B.; Huang Z.R.; Chen L.S. Root iTRAQ protein profile analysis of two Citrus species differing in aluminum-tolerance in response to long-term aluminum-toxicity. BMC Genomics 2015; 16(1), 949.

21. Marschner H. Mineral nutrition of higher plants. Harcourt Brace, London, Academic Press, 1995; ISBN 978-0-12-304905-2.

22. Yang L.T.; Jiang H.X.; Qi Y.P.; Chen L.S. Differential expression of genes involved in alternative glycolytic pathways, phosphorus scavenging and recycling in response to aluminum and phosphorus interactions in Citrus roots. Mol. Biol. Rep. 2012; 39(5), 6353–6366. doi: 10.1007/s11033-012-1457-7 22307782

23. Yang L.T.; Jiang H.X.; Tang N.; Chen L.S. Mechanisms of aluminum-tolerance in two species of citrus: secretion of organic acid anions and immobilization of aluminum by phosphorus in roots. Plant Sci. 2011; 180, 521–530. doi: 10.1016/j.plantsci.2010.11.011 21421400

24. Liao H.; Wan H.; Shaff J.; Wang X.; Yan X.; Kochian L.V. Phosphorus and aluminum interactions in soybean in relation to aluminum tolerance. Exudation of specific organic acids from different regions of the intact root system. Plant Physiol. 2006; 141(2), 674–684. doi: 10.1104/pp.105.076497 16648222

25. Iqbal M.T. Phosphorus alleviates aluminum toxicity in al-sensitive wheat seedlings. Commun Soil Sci Plan 2014; 45(4); 437–450.

26. He G.; Zhang J.; Hu X.; Wu J. Effect of aluminum toxicity and phosphorus deficiency on the growth and photosynthesis of oil tea (Camellia oleifera Abel.) seedlings in acidic red soils. Acta Physiol. Plant. 2011; 33(4), 1285–1292.

27. Sun Q.B.; Shen R.F.; Zhao X.Q.; Chen R.F.; Dong X.Y. Phosphorus enhances Al resistance in Al-resistant Lespedeza bicolor but not in Al-sensitive L. cuneata under relatively high Al stress. Ann. Bot. 2008; 102, 795–804. doi: 10.1093/aob/mcn166 18757448

28. Gaume A.; Mächler F.; Frossard E.; Aluminum resistance in two cultivars of Zea mays L.: Root exudation of organic acids and influence of phosphorus nutrition. Plant Soil 2001; 234(1), 73–81.

29. Nakagawa T.; Mori S.; Yoshimura E. Amelioration of aluminum toxicity by pretreatment with phosphate in aluminum‐tolerant rice cultivar. J. Plant Nutr. 2003; 26, 619–628.

30. Liu N.; You J.; Shi W.; Liu W.; Yang Z. Salicylic acid involved in the process of aluminum induced citrate exudation in Glycine max L. Plant Soil 2012; 352, 85–97.

31. Ligaba-Osena A.; Fei Z.; Liu J.; Xu Y.; Shaff J.; Lee S.C.; Luan S.; Kudla J.; Kochian L.V.; Pineros M. Loss-of-function mutation of the calcium sensor CBL1 increases aluminum sensitivity in Arabidopsis. New Phytol. 2017; 214(2), 830–841. doi: 10.1111/nph.14420 28150888

32. Freitas L.B.D.; Fernandes D.M.; Maia S.C.M.; Fernandes A.M. Effects of silicon on aluminum toxicity in upland rice plants. Plant Soil 2017; 420(1–2), 263–275.

33. Ames B.N. Assay of inorganic phosphate, total phosphate and phosphatase, Methods Enzymol. 1966; 8, 115–118.

34. Hsu P.H. Effect of initial pH, phosphate, and silicate on the determination of aluminum with aluminon. Soil Sci. 1963; 96, 230–238.

35. Hodges D.M.; DeLong J.M.; Forney C.F.; Prange R.K. Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 1999; 207, 604–611.

36. Morrison I.M. A semi-micro method for the determination of lignin and its use in predicting the digestibility of forage crops. J. Sci. Food Agr. 1972; 23(4), 455–463.

37. Bradford M.M. A rapid method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976; 72, 248–254. doi: 10.1006/abio.1976.9999 942051

38. Yang L.T.; Qi Y.P.; Lu Y.B.; Guo P.; Sang W.; Feng H.; Zhang H.X.; Chen L.S. iTRAQ protein profile analysis of Citrus sinensis roots in response to long-term boron-deficiency. J. Proteimics 2013; 93, 179–206.

39. Washburn M.P.; Koller A.; Oshiro G.; Ulaszek R.R.; Plouffe D.; Deciu C.; Winzeler E.; Yates J.R. Protein pathway and complex clustering of correlated mrna and protein expression analyses in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. 2003; 100(6), 3107–3112. doi: 10.1073/pnas.0634629100 12626741

40. Rengel Z.; Bose J.; Chen Q.; Tripathi B.N. Magnesium alleviates plant toxicity of aluminium and heavy metals. Crop Pasture Sci. 2015; 66: 1298–1307.

41. Peng H.Y.; Qi Y.P.; Lee J.; Yang L.T.; Guo P.; Jiang H.X.; Chen L.S. Proteomic analysis of Citrus sinensis roots and leaves in response to long-term magnesium-deficiency. BMC genomics 2015; 16(1), 253.

42. Sang W.; Huang Z.R.; Yang L.T.; Guo P.; Ye X.; Chen L.S. Effects of high toxic boron concentration on protein profiles in roots of two citrus species differing in boron-tolerance revealed by a 2-DE based MS approach. Front. Plant Sci. 2017; 8(8), 1–19.

43. Lan P.; Li W.; Wen T.; Shiau J.; Wu Y.; Lin W.; Schmidt W. iTRAQ protein profile analysis of Arabidopsis roots reveals new aspects critical for iron homeostasis. Plant Sig. Beh. 2011; 155(4), 821–834.

44. Jiang Y.; Yang B.; Harris N.S.; Deyholos M.K. Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. J. Exp. Bot. 2007; 8(13), 3591–3607.

45. Wang Z.Q.; Xu X.Y.; Gong Q.Q.; Xie C.; Fan W.; Yang J.L.; Lin Q.S.; Zheng S.J. Root proteome of rice studied by iTRAQ provides integrated insight into aluminum stress tolerance mechanisms in plants. J. Proteomics 2014; 98, 189–205. doi: 10.1016/j.jprot.2013.12.023 24412201

46. Zheng L.; Lan P.; Shen R.F.; Li W.F. Proteomics of aluminum tolerance in plants. Proteomics 2014; 14, 566–578. doi: 10.1002/pmic.201300252 24339160

47. Yang L.M; Tian D.G.; Todd C.D.; Luo Y.M.; Hu X.Y. Comparative proteome analyses reveal that nitric oxide is an important signal molecule in the response of rice to aluminum toxicity. J. Proteome Res. 2013; 12, 1316–1330. doi: 10.1021/pr300971n 23327584

48. Shi H.; Xiong L.; Stevenson B.; Lu T.; Zhu J.K. The Arabidopsis salt overly sensitive 4 mutants uncover a critical role for vitamin B6 in plant salt tolerance. Plant Cell 2002; 14(3), 575–588. doi: 10.1105/tpc.010417 11910005

49. Hýsková V.D.; Miedzińska L.; Dobra J.; Vankova R.; Ryšlavá H. Phosphoenolpyruvate carboxylase, NADP-malic enzyme, and pyruvate, phosphate dikinase are involved in the acclimation of Nicotiana tabacum L. to drought stress. J. Plant Physiol. 2014; 171, 19–25. doi: 10.1016/j.jplph.2013.10.017 24484954

50. Yang L.T.; Chen L.S.; Peng H.Y.; Guo P.; Wang P.; Ma C.L. Organic acid metabolism in Citrus grandis leaves and roots is differently affected by nitric oxide and aluminum interactions. Sci. Hortic. 2012; 133, 40–46.

51. Hernández I.; Munné-Bosch S. Linking phosphorus availability with photo-oxidative stress in plants. J. Exp. Bot. 2015; 66, 2889–2900. doi: 10.1093/jxb/erv056 25740928

52. Xia J.X.; Yamaji N.; Kasai T.; Ma J.F. Plasma membrane-localized transporter for aluminum in rice. Proc. Natl. Acad. Sci. 2010; 107(43), 18381–18385. doi: 10.1073/pnas.1004949107 20937890

53. Ma B.; Gao L.; Zhang H.; Cui J.; Shen Z. Aluminum-induced oxidative stress and changes in antioxidant defenses in the roots of rice varieties differing in Al tolerance. Plant Cell Rep. 2012; 31(4), 687–696. doi: 10.1007/s00299-011-1187-7 22086537

54. Yamamoto Y.; Kobayashi Y.; Devi S.R.; Rikiishi S.; Matsumoto H. Oxidative stress triggered by aluminum in plant roots. Plant Soil 2003; 255, 239–243.

55. Yan L.; Riaz M.; Wu X.W.; Du C.Q.; Liu Y.L.; Jiang C.C. Ameliorative effects of boron on aluminum induced variations of cell wall cellulose and pectin components in trifoliate orange (Poncirus trifoliate (L.) Raf.) rootstock. Environ. Pollut. 2018; 240, 764–774. doi: 10.1016/j.envpol.2018.05.022 29778812

56. Yin L.; Mano J.; Wang S.; Tsuji W.; Tanaka K. The involvement of lipid peroxide-derived aldehydes in aluminum toxicity of tobacco roots. Plant Physiol. 2010; 152, 1406–1417. doi: 10.1104/pp.109.151449 20023145

57. Jones D.L.; Blancaflor E.B.; Kochian L.V.; Gilroy S. Spatial coordination of aluminium uptake, production of reactive oxygen species, callose production and wall rigidification in maize roots. Plant Cell Environ. 2006; 29, 1309–1318. 17080952

58. Li H.; Yang L.T.; Qi Y.P.; Guo P.; Lu Y.B.; Chen L.S. Aluminum toxicity-induced alterations of leaf proteome in two citrus species differing in aluminum tolerance. Int. J. Mol. Sci. 2016; 17, 1180.

59. Minic Z. Physiological roles of plant glycoside hydrolases. Planta 2008; 227, 723. doi: 10.1007/s00425-007-0668-y 18046575

60. Hou Q.C.; Ufer G.; Bartels D. Lipid signalling in plant responses to abiotic stress. Plant Cell Environ. 2016; 39(5), 1029–1048. doi: 10.1111/pce.12666 26510494

61. Lindberg S.; Griffiths G. Aluminium effects on ATPase activity and lipid composition of plasma membranes in sugar beet roots. J. Exp. Bot. 1993; 44(10), 1543–1550.

62. Molina I.; Kosma D. Role of HXXXD-motif/BAHD acyltransferases in the biosynthesis of extracellular lipids. Plant Cell Rep. 2015; 34(4), 587–601. doi: 10.1007/s00299-014-1721-5 25510356

63. Jaskowiak J.; Tkaczyk O.; Slota M.; Kwasniewska J.; Szarejko I. Analysis of aluminum toxicity in Hordeum vulgare roots with an emphasis on DNA integrity and cell cycle. PLoS One 2018; 13(2), e0193156. doi: 10.1371/journal.pone.0193156 29466444

64. Zhu J.K. Abiotic stress signaling and responses in plants. Cell 2016; 167(2), 313–324. doi: 10.1016/j.cell.2016.08.029 27716505

65. Guo H.; Li L.; Ye H.; Yu X.; Algreen A.; Yin Y. Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc. Natl. Acad. Sci. 2009; 106, 7648–7653. doi: 10.1073/pnas.0812346106 19383785

66. Tamás L.; Šimonoviová M.; Huttová J.; Mistrík I. Elevated oxalate oxidase activity is correlated with Al-induced plasma membrane injury and root growth inhibition in young barley roots. Acta Physiol. Plant. 2004; 26(1), 85–93.


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