Root cell wall polysaccharides are involved in cadmium hyperaccumulation in Sedum alfredii

Plant and Soil

Volumn 389, Issue 1-2, 2015, Pages 387-399

  Li, Tingqiang ^a   Tao, Qi ^a   Shohag, Md Jahidul Islam ^a   Yang, Xiaoe ^a   Sparks, Donald L ^b   Liang, Yongchao ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b UNIVERSITY OF DELAWARE   (United States)

Author keywords

Cadmium; Cell wall; Hyperaccumulation; Pectin; Polysaccharides; Sedum alfredii

Indexed keywords

CADMIUM; CYTOLOGY; ECOTYPE; HERB; HYPERACCUMULATION; POLYSACCHARIDE;

SEDUM ALFREDII;

EID: 84926454111     PISSN: 0032079X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11104-014-2367-3     Document Type: Article

References (58)

1. Bernard C, Roosens N, Czernic P, Lebrun M, Verbruggen N (2004) A novel CPx-ATPase from the cadmium hyperaccumulator Thlaspi caerulescens. FEBS Lett 569:140–148
2. Bert V, Bonnin I, Saumitou-Laprade P, de Laguerie P, Petit D (2002) Do Arabidopsis halleri from nonmetallicolous populations accumulate zinc and cadmium more effectively than those from metallicolous populations? New Phytol 155:47–57
3. Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative-determination of uronic acids. Anal Biochem 54:484–489
4. Colzi I, Arnetoli M, Gallo A, Doumett S, Del Bubba M, Pignattelli S, Gabbrielli R, Gonnelli C (2012) Copper tolerance strategies involving the root cell wall pectins in Silene paradoxa L. Environ Exp Bot 78:91–98
5. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861
6. Courbot M, Willems G, Motte P, Arvidsson S, Roosens N, Saumitou-Laprade P, Verbruggen N (2007) A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiol 144:1052–1065
7. Douchiche O, Rihouey C, Schaumann A, Driouich A, Morvan C (2007) Cadmium-induced alterations of the structural features of pectins in flax hypocotyl. Planta 225:1301–1312
8. Ebbs SD, Zambrano MC, Spiller SM, Newville M (2009) Cadmium sorption, influx, and efflux at the mesophyll layer of leaves from ecotypes of the Zn/Cd hyperaccumulator Thlaspi caerulescens. New Phytol 181:626–636
9. Eren E, Argüello JM (2004) Arabidopsis HMA2, a divalent heavy metal-transporting P-IB-type ATPase, is involved in cytoplasmic Zn2+ homeostasis. Plant Physiol 136(3):3712–3723
10. Eticha D, Stass A, Horst WJ (2005) Cell-wall pectin and its degree of methylation in the maize root-apex: significance for genotypic differences in aluminium resistance. Plant Cell Environ 28:1410–1420
11. Gao J, Sun L, Yang XE, Liu JX (2013) Transcriptomic analysis of cadmium stress response in the heavy metal hyperaccumulator Sedum alfredii Hance. PLoS ONE 8(6):e64643
12. Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Kramer U (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395
13. Hassan Z, Aarts MGM (2011) Opportunities and feasibilities for biotechnological improvement of Zn, Cd or Ni tolerance and accumulation in plants. Environ Exp Bot 72:53–63
14. Krzeslowska M (2011) The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiol Plant 33:35–51
15. Krzeslowska M, Lenartowska M, Samardakiewicz S, Bilski H, Wozny A (2010) Lead deposited in the cell wall of Funaria hygrometrica protonemata is not stable - a remobilization can occur. Environ Pollut 158:325–338
16. Lasat MM, Baker AJM, Kochian LV (1998) Altered Zn compartmentation in the root symplasm and stimulated Zn absorption into the leaf as mechanisms involved in Zn hyperaccumulation in Thlaspi caerulescens. Plant Physiol 118:875–883
17. Li TQ, Yang XE, Meng FH, Lu LL (2007) Zinc adsorption and desorption characteristics in root cell wall involving zinc hyperaccumulation in Sedum alfredii Hance. J Zhejiang Univ Sci B 8:111–115
18. Li TQ, Tao Q, Liang CF, Shohag MJI, Yang XE, Sparks DL (2013) Complexation with dissolved organic matter and mobility control of heavy metals in the rhizosphere of hyperaccumulator Sedum alfredii. Environ Pollut 182:248–255
19. Lu LL, Tian SK, Yang XE, Wang XC, Brown P, Li TQ, He ZL (2008) Enhanced root-to-shoot translocation of cadmium in the hyperaccumulating ecotype of Sedum alfredii. J Exp Bot 59:3203–3213
20. Lu LL, Tian SK, Zhang J, Yang X, Labavitch JM, Webb SM, Latimer M, Brown PH (2013) Efficient xylem transport and phloem remobilization of Zn in the hyperaccumulator plant species Sedum alfredii. New Phytol 198:721–731
21. Lux A, Martinka M, Vaculik M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37
22. Micheli F (2001) Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Sci 6:414–419
23. Morel M, Crouzet J, Gravot A, Auroy P, Leonhardt N, Vavasseur A, Richaud P (2009) AtHMA3, a P-1B-ATPase allowing Cd/Zn/Co/Pb vacuolar sorage in Arabidopsis. Plant Physiol 149(2):894–904
24. Mori S, Kawasaki A, Ishikawa S, Arao T (2009) A new method for evaluating symplastic cadmium absorption in the roots of Solanum melongena using enriched isotopes 113Cd and 114Cd. Soil Sci Plant Nutr 55:294–299
25. Ni TH, Wei YZ (2003) Subcellular distribution of cadmium in mining ecotype Sedum alfredii. Acta Bot Sin 45:925–928
26. Nishizono H, Ichikawa H, Suziki S, Ishii F (1987) The Role of the Root Cell-Wall in the Heavy-Metal Tolerance of Athyrium-Yokoscense. Plant Soil 101:15–20
27. Nyquist J, Greger M (2007) Uptake of Zn, Cu, and Cd in metal loaded Elodea canadensis. Environ Exp Bot 60:219–226
28. Pelloux J, Rusterucci C, Mellerowicz EJ (2007) New insights into pectin methylesterase structure and function. Trends Plant Sci 12:267–277
29. Pence NS, Larsen PB, Ebbs SD, Letham DBL, Lasat MM, Garvin DF, Eide D, Kochian LV (2000) The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc Natl Acad Sci U S A 97:4956–4960
30. Robinson BH, Leblanc M, Petit D, Brooks RR, Kirkman JH, Gregg PEH (1998) The potential of Thlaspi caerulescens for phytoremediation of contaminated soils. Plant Soil 203:47–56
31. Schmohl N, Pilling J, Fisahn J, Horst WJ (2000) Pectin methylesterase modulates aluminium sensitivity in Zea mays and Solanum tuberosum. Physiol Plant 109:419–427
32. Shi Z, Di Toro DM, Allen HE, Sparks DL (2008) A WHAM-based kinetics model for Zn adsorption and desorption to soils. Environ Sci Technol 42:5630–5636
33. Sousa AI, Cacador I, Lillebo AI, Pardal MA (2008) Heavy metal accumulation in Halimione portulacoides: intra- and extra-cellular metal binding sites. Chemosphere 70:850–857
34. Tang YT, Qiu RL, Zeng XW, Fang XH, Yu FM, Zhou XY, Wu YD (2009) Zn and Cd hyperaccumulating characteristics of Picris divaricata Vant. Int J Environ Pollut 38:26–38
35. Tian SK, Lu LL, Yang XO, Webb SM, Du YH, Brown PH (2010) Spatial imaging and speciation of lead in the accumulator plant Sedum alfredii by microscopically focused synchrotron X-ray investigation. Environ Sci Technol 44:5920–5926
36. Tian SK, Lu LL, Labavitch J, Yang XE, He ZL, Hu HN, Sarangi R, Newville M, Commisso J, Brown P (2011) Cellular sequestration of cadmium in the hyperaccumulator plant species Sedum alfredii. Plant Physiol 157:1914–1925
37. Tsednee M, Yang SC, Lee DC, Yeh KC (2014) Root-secreted nicotianamine from Arabidopsis halleri facilitates zinc hypertolerance by regulating zinc bioavailability. Plant Physiol 166:839–852
38. Ueno D, Milner MJ, Yamaji N, Yokosho K, Koyama E, Clemencia Zambrano M, Kaskie M, Ebbs S, Kochian LV, Ma JF (2011) Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Plant J 66:852–862
39. Uraguchi S, Kiyono M, Sakamoto T, Watanabe I, Kuno K (2009) Contributions of apoplasmic cadmium accumulation, antioxidative enzymes and induction of phytochelatins in cadmium tolerance of the cadmium-accumulating cultivar of black oat (Avena strigosa Schreb.). Planta 230:267–276
40. van de Mortel JE, Schat H, Moerland PD, Loren V, van Themaat E, van der Ent S, Blankestijn H, Ghandilyan A, Tsiatsiani S, Aarts MG (2008) Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd-hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 31:301–324
41. Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776
42. Vogel-Mikus K, Drobne D, Regvar M (2005) Zn, Cd and Pb accumulation and arbuscular mycorrhizal colonisation of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia. Environ Pollut 133:233–242
43. Vollenweider P, Cosio C, Guenthardt-Goerg MS, Keller C (2006) Localization and effects of cadmium in leaves of a cadmium-tolerant willow (Salix viminalis L.) Part II Microlocalization and cellular effects of cadmium. Environ Exp Bot 58:25–40
44. Webb SM (2005) SIXpack: a graphical user interface for XAS analysis using IFEFFIT. Phys Scr 115:1011–1014
45. Wei L, Shu WS, Lan CY (2004) Viola baoshanensis, a plant that hyperaccumulates cadmium. Chin Sci Bull 49:29–32
46. Wei SH, Zhou QX, Wang X, Zhang KS, Guo GL, Ma QYL (2005) A newly-discovered Cd-hyperaccumulator Solanum nigrum L. Chin Sci Bull 50:33–38
47. White PJ (2001) The pathways of calcium movement to the xylem. J Exp Bot 52:891–899
48. Wierzbicka M (1998) Lead in the apoplast of Allium cepa L. root tips ultrastructural studies. Plant Sci 133:105–119
49. Willats WGT, Knox JP, Mikkelsen JD (2006) Pectin: new insights into an old polymer are starting to gel. Trends Food Sci Technol 17:97–104
50. Xiong J, Lu H, Lu KX, Duan YX, An LY, Zhu C (2009) Cadmium decreases crown root number by decreasing endogenous nitric oxide, which is indispensable for crown root primordia initiation in rice seedlings. Planta 230:599–610
51. Yang XE, Long XX, Ye HB, He ZL, Calvert DV, Stoffella PJ (2004) Cadmium tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species (Sedum alfredii Hance). Plant Soil 259:181–189
52. 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
53. Yang JL, Zhu XF, Peng YX, Zheng C, Li GX, Liu Y, Shi YZ, Zheng SJ (2011) Cell wall hemicellulose contributes significantly to aluminum adsorption and root growth in Arabidopsis. Plant Physiol 155:1885–1892
54. Zhao FJ, Hamon RE, Lombi E, McLaughlin MJ, McGrath SP (2002) Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. J Exp Bot 53:535–543
55. Zhao FJ, Jiang RF, Dunham SJ, McGrath SP (2006) Cadmium uptake, translocation and tolerance in the hyperaccumulator Arabidopsis halleri. New Phytol 172:646–654
56. Zhong HL, Lãuchli 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
57. Zhu XF, Lei GJ, Jiang T, Liu Y, Li GX, Zheng SJ (2012) Cell wall polysaccharides are involved in P-deficiency-induced Cd exclusion in Arabidopsis thaliana. Planta 236:989–997
58. Zhu QH, Huang DY, Liu SL, Luo ZC, Rao ZX, Cao XL, Ren XF (2013) Accumulation and subcellular distribution of cadmium in ramie (Boehmeria nivea L. Gaud.) planted on elevated soil cadmium contents. Plant Soil Environ 59:57–61