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Al-induced cell wall hydroxyproline-rich glycoprotein accumulation is involved in alleviating Al toxicity in rice

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Abstract

Cell wall components such as pectin and hemicelluloses have been proposed to be involved in aluminum resistance mechanisms in plants. However, whether hydroxyproline-rich glycoproteins (HRGPs), one of the most abundant proteins of the cell walls, are involved in Al resistance mechanisms remains elusive. In this study, two rice cultivars Xiushui 03 (Al resistant) and Xiushui 128 (Al sensitive) significantly differing in Al resistance were identified. In the absence of Al, no significant difference was observed in contents of glycoproteins and hydroxyproline in cell wall fractions of these two cultivars. At the early stage of Al toxicity, glycoproteins and hydroxyproline were significantly induced in these two cultivars, but levels of their accumulation in cell walls were much higher in cv. Xiushui 03 than in cv. Xiushui 128. At the late stage of Al toxicity, their accumulation in cell walls dramatically decreased in cv. Xiushui 128 and, however, still kept a high level in cv. Xiushui 03. The finding that Al-induced changes of glycoproteins and hydroxyproline were completely consistent indicates that Al-induced glycoproteins are HRGPs. Further observation utilizing transmission electron microscope showed that HRGPs were greatly accumulated in cell walls leading to thickening of cell walls in cv. Xiushui 03, however, HRGPs and cell walls greatly decreased in cv. Xiushui 128. These data suggest that Al-induced HRGP accumulation in cell walls is involved in alleviating Al toxicity in rice.

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References

  • Asamizu T, Shimizu K, Takesako K, Nishi A (1986) Glycoproteins associated with the cell wall of carrot cells in suspension culture. Plant Tissue Cult Lett 3:16–21

    CAS  Google Scholar 

  • Balestrini R, Romera C, Puigdomenech P, Bonfante P (1994) Location of a cell-wall hydroxyproline-rich glycoprotein, cellulose and β-l, 3-glucans in apical and differentiated regions of maize mycorrhizal roots. Planta 195:201–209

    Article  CAS  Google Scholar 

  • Chang YC, Yamamoto Y, Matsumoto H (1999) Accumulation of aluminium in the cell wall pectin in cultured tobacco (Nicotiana tabacum L.) cells treated with a combination of aluminium and iron. Plant Cell Environ 22:1009–1017

    Article  CAS  Google Scholar 

  • Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107:315–321

    CAS  PubMed  Google Scholar 

  • Ellis C, Karafyllidis I, Wasternack C, Turner J (2002) The arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. Plant Cell 14:1557–1566

    Article  CAS  PubMed  Google Scholar 

  • Horst WJ (1995) The role of the apoplast in aluminum toxicity and resistance of higher plants: a review. Z. Pflanzenernahr Bodenkd 158:419–428

    Article  CAS  Google Scholar 

  • Horst WJ, Schmohl N, Kollmeier M, Baluska F, Sivaguru M (1999) Does aluminium affect root growth of maize through interaction with the cell wall-plasma membrane-cytoskeleton continuum? Plant Soil 215:163–174

    Article  CAS  Google Scholar 

  • Iiyama K, Lam TBT, Stone BA (1994) Covalent cross-links in the cell wall. Plant Physiol 104:315–320

    CAS  PubMed  Google Scholar 

  • Jian LC, Sun LH, Sun DL (1986) Electron microscopic cytochemistry on the glycoproteins at the cell surface in several species of plants and its relations to stress resistance. Acta Biol Exp Sinica 19:261–271

    CAS  Google Scholar 

  • Kenjebaeva S, Yamamoto Y, Matsumoto H (2001) The impact of aluminum on the distribution of cell wall glycoproteins of pea root tip and their Al-binding capacity. Soil Sci Plant Nutr 47:629–636

    CAS  Google Scholar 

  • Kenzhebaeva SS, Yamamoto Y, Matsumoto H (2001) Aluminum-induced changes in cell-wall glycoproteins in the root tips of Al-tolerant and Al-sensitive wheat lines. Russ J Plant Physiol 48:441–447

    Article  CAS  Google Scholar 

  • Kivirikko KI, Liesmaa MA (1959) Colorimetric method for determination of hydroxyproline in tissue hydrolysates. Scand J Clin Lab Invest 11:128–133

    Article  CAS  Google Scholar 

  • Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol 46:237–260

    Article  CAS  Google Scholar 

  • Kochian LV, Hoekenga OA, Piñeros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminium tolerance and phosphorus efficiency. Annu Rev Plant Biol 55:459–493

    Article  CAS  PubMed  Google Scholar 

  • Kreuger M, van Holst GJ (1996) Arabinogalactan proteins and plant differentiation. Plant Mol Biol 30:1077–1086

    Article  CAS  PubMed  Google Scholar 

  • Li JH, Li XB (1993) Preparation and hydroxyproline analysis of plant cell wall. Plant Physiol Commun 29:363–365 (in Chinese)

    CAS  Google Scholar 

  • Llugany M, Poschenrieder C, Barcelό J (1995) Monitoring of aluminum induced inhibition of root elongation in four maize cultivars differing in tolerance to aluminum and proton toxicity. Physiol Plant 93:265–271

    Article  CAS  Google Scholar 

  • Luft JH (1971a) Ruthenium red and violet I Chemistry, purification, methods of use for electron microscopy and mechanism of action. Anat Rec 171:347–368

    Article  CAS  PubMed  Google Scholar 

  • Luft JH (1971b) Ruthenium red and violet II Fine structure localization in animal tissues. Ana Rec 171:369–380

    Article  CAS  Google Scholar 

  • Ma JF, Shen RF, Zhao ZQ, Wissuwa M, Takeuchi Y, Ebitani T, Yano M (2002) Response of rice to Al stress and identification of quantitative trait loci for Al tolerance. Plant Cell Physiol 43:652–659

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto H (2000) Cell biology of aluminum toxicity and tolerance in higher plants. Int Rev Cytol 200:1–46

    Article  CAS  PubMed  Google Scholar 

  • Mazau D, Esquerré-Tugayé MT (1986) Hydroxyproline-rich glycoprotein accumulation in the cell walls of plants infected by various pathogens. Physiol Mol Plant Pathol 29:147–157

    Article  CAS  Google Scholar 

  • Miyasaka SC, Buta JG, Howell RK, Foy CD (1991) Mechanism of aluminium tolerance in snapbeans: root exudation of citric acid. Plant Physiol 96:737–743

    Article  CAS  PubMed  Google Scholar 

  • Pan JW, Zheng K, Ye D, Yi HL, Jiang ZM, Jing CT, Pan WH, Zhu MY (2004) Aluminum-induced ultraweak luminescence changes and sister-chromatid exchanges in root tip cells of barley. Plant Sci 167:1391–1399

    Article  CAS  Google Scholar 

  • Pennell RI, Roberts K (1990) Sexual development in the pea is presaged by altered expression of arabinogalactan protein. Nature 344:547–549

    Article  Google Scholar 

  • Poschenrieder C, Gunsé B, Corrales I, Barceló J (2008) A glance into aluminum toxicity and resistance in plants. Sci Total Environ 400:356–368

    Article  CAS  PubMed  Google Scholar 

  • Reiter WD (1998) The molecular analysis of cell wall components. Trends Plant Sci 3(1):27–32

    Article  Google Scholar 

  • Roberts K (1990) Structures at the plant cell surface. Curr Opin Cell Biol 2:920–928

    Article  CAS  PubMed  Google Scholar 

  • Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Mol Biol 52:527–560

    Article  CAS  Google Scholar 

  • Scheres B, Wiel CVD, Zalensky A, Horvath B, Spaink H, Eck HV, Zwartkruis F, Wolters AM, Gloudemans T, Kammen AV, Bisseling T (1990) The ENOD12 gene product is involved in the infection process during the pea–rhizobium interaction. Cell 60:281–294

    Article  CAS  PubMed  Google Scholar 

  • Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5:9–23

    Article  CAS  PubMed  Google Scholar 

  • Showalter AM, Bell JN, Cramer CL, Bailey JA, Varner JE, Lamb CJ (1985) Accumulation of hydroxyproline-rich glycoprotein mRNAs in response to fungal elicitor and infection. Proc Natl Acad Sci 82:6551–6555

    Article  CAS  PubMed  Google Scholar 

  • Stacey NJ, Roberts K, Carpita NC, Wells B, McCann MC (1995) Dynamic changes in cell surface molecules are very early events in the differentiation of mesophyll cells from Zinnia elegans into tracheary elements. Plant J 8:891–906

    Article  CAS  Google Scholar 

  • Sun JY, Zhao YT, Liang BW, Liu F, You Y (2004) Changes of hydroxyproline-rich glycoprotein in wheat under cold stress and its relationship to cold resistance. J Plant Genet Res 5:6–11 (in Chinese)

    Google Scholar 

  • Willats WGT, Knox JP (1996) A role for arabinogalactan-proteins in plant cell expansion: evidence from studies on the interaction of -glucosyl Yariv reagent with seedlings of Arabidopsis thaliana. Plant J 9:919–925

    Article  CAS  PubMed  Google Scholar 

  • Wu HM, Wang H, Cheung AY (1995) A pollen tube growth stimulatory glycoprotein is deglycosylated by pollen tubes and displays a glycosylation gradient in the flower. Cell 82:395–403

    Article  CAS  PubMed  Google Scholar 

  • Wycoff K, Powell PA, Conzales RA, Corbin DR, Lamb C, Dixon RA (1995) Stress activation of a bean hydroxyproline-rich glycoprotein promoter is superimposed on a pattern of tissue-specific developmental expression. Plant Physiol 109:41–52

    Article  CAS  PubMed  Google Scholar 

  • Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR, Wu P, Zheng SJ (2008) Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiol 146:602–611

    Article  CAS  PubMed  Google Scholar 

  • Zhong HL, Lauchli A (1993) Changes of cell wall composition and polymer size in primary roots of cotton seedlings under high salinity. J Exp Bot 44:773–778

    Article  CAS  Google Scholar 

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Acknowledgments

We are grateful to Jiaxing Academy of Agricultural Sciences (China) for the gifts of rice cultivars, Danping Tong, Jiaping Pan, Zhao Shen, Ying Qian, Hua Yang, Xiuzhen Wang, and Zhongqiang Mi for their technical assistance, Shaojian Zheng (Zhejiang University) for critical reading of the manuscript. This work was supported by the National Natural Science Foundation of China (No. 30970255) and Zhejiang Provincial Natural Science Foundation of China (No. Y3100207), China National Key Programs for Transgenic Crops (No. 2009ZX08009-076B), Zhejiang Provincial Excellent Youth Foundation of China (No. R3100175), Zhejiang Provincial Qianjiang Talents Program of China (No. 2010R10085), the National High Technology Research and Development Program of China (863 Program, No. 2007AA10Z141), and Scientific Research Foundation for the Returned Overseas Chinese Scholars, State Education Ministry (SRF for ROCS, SEM).

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Correspondence to Jianwei Pan.

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Communicated by J. Zwiazek.

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Pan, W., Shou, J., Zhou, X. et al. Al-induced cell wall hydroxyproline-rich glycoprotein accumulation is involved in alleviating Al toxicity in rice. Acta Physiol Plant 33, 601–608 (2011). https://doi.org/10.1007/s11738-010-0684-6

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  • DOI: https://doi.org/10.1007/s11738-010-0684-6

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