Abstract
Aims
As a vital polysaccharide related to mechanisms of plant resistance to trace metal in the root cell wall, the role of hemicellulose in cadmium (Cd) accumulation in hyperaccumulators is still unknown. We investigated hemicellulose modification in response to Cd in two populations of Sedum alfredii.
Methods
Nonhyperaccumulating population (NHP) and hyperaccumulating population (HP) of S. alfredii were grown in nutrient solutions with or without 25 μM Cd for 15 d. Monosaccharide composition of root cell wall hemicellulose and its remolding mechanisms (e.g. enzyme activity and gene expression) were analyzed by using gas chromatography-mass spectrometer (GC-MS), fourier transform infrared spectrometer (FTIR), nuclear magnetic resonance (NMR) and quantitative real-time PCR techniques.
Results
In 25 μM Cd treatment, root cell wall hemicellulose in the NHP significantly (P < 0.05) increased and its hemicellulose-bound Cd was nearly 2.5-fold higher than that of HP. In the presence of Cd, xylose and glucose, proved to be the main component of hemicellulose, were higher in the NHP than in the HP owing to the up-regulation of XET/XEH and encoding gene (XTH 31). 113Cd-NMR and FTIR results indicated that hemicellulose with hydroxyl and carboxyl groups of HP retained less Cd than that of NHP.
Conclusion
Hemicellulose modification decreased the Cd-binding capacity of the root cell wall and increased the entry of Cd in the shoot of HP S. alfredii.
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References
Avci U, Pattathil S, Hahn MG (2012) Immunological approaches to plant cell wall and biomass characterization: immunolocalization of glycan epitopes. Methods Mol Biol 908:73–82
Baumann MJ, Eklöf JM, Michel G, Kallas AM, Teeri TT, Czjzek M, Brumer H (2007) Structural evidence for the evolution of Xyloglucanase activity from Xyloglucan Endo-Transglycosylases: biological implications for Cell Wall metabolism. Plant Cell 19:1947–1963
Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Biochem 54(2):484–489
Broadley MR, Willey NJ, Wilkins JC, Mead A, White PJ (2001) Phylogenetic variation in heavy metal accumulation in angiosperms. New Phytol 152:9–27
Burton RA, Gidley MJ, Fincher GB (2010) Heterogeneity in the chemistry, structure and function of plant cell walls. Nat Chem Biol 6(10):724–732
Carrier P, Baryla A, Havaux M (2003) Cadmium distribution and microlocalization in oilseed rape (Brassica napus) after long-term growth on cadmium-contaminated soil. Planta 216:939–950
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
Chao YE, Feng Y, Yang XE, Liu D (2008) Effect of long-term stress of high Pb/Zn levels on genomic variation of Sedum alfredii Hance. Bull Environ Contam Toxicol 81:445–448
Cheng L, Wang L, Wei L, Wu Y, Alam A, Xu C, Wang Y, Tu Y, Peng L, Xia T (2019) Combined mild chemical pretreatments for complete cadmium release and cellulosic ethanol co-production distinctive in wheat mutant straw. Green Chem 21:3693–3700
Chen X, Kim J (2009) Callose synthesis in higher plants. Plant Signaling Behavior 4:489–492
Chudzik B, Szczuka E, Leszczuk A, Strubińska J (2018) Modification of pectin distribution in sunflower (Helianthus annuus L.) roots in response to lead exposure. Environ Exp Bot 155:251–259
Clemens S, Aarts MGM, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18:92–99
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
Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Bio 6:850–861
Cui X, Fang S, Yao Y, Li T, Ni Q, Yang X, He Z (2016) Potential mechanisms of cadmium removal from aqueous solution by Canna indica derived biochar. Sci Total Environ 562:517–525
Davis TA, Llanes F, Volesky B, Mucci A (2003) Metal selectivity of Sargassum spp. and their alginates in relation to their α-l-guluronic acid content and conformation. Environ Sci Technol 37:261–267
Deng J, Liao B, Mai Y, Deng D, Lan C, Shu W (2007) The effects of heavy metal pollution on genetic diversity in zinc/cadmium hyperaccumulator Sedum alfredii populations. Plant Soil 297:83–92
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
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28(3):350–356
Fry SC, Smith RC, Renwick KF, Martin DJ, Hodge SK, Matthews KJ (1992) Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants. Biochem J 282(3):821–828
Gao J, Sun L, Yang X, Liu J (2014) Transcriptomic analysis of cadmium stress response in the heavy metal hyperaccumulator Sedum alfredii Hance. PLoS One 8:e64643
Günl M, Neumetzler L, Kraemer F, De Souza A, Schultink A, Pena M, York WS, Markus P (2011) Axy8 encodes an α-fucosidase, underscoring the importance of apoplastic metabolism on the fine structure of Arabidopsis cell wall polysaccharides. Plant Cell 23(11):4025–4040
Han Y, Sa G, Sun J, Shen Z, Zhao R, Ding M, Deng S, Lu Y, Zhang Y, Shen X, Chen S (2014) Overexpression of Populus euphratica xyloglucan endotransglucosylase/hydrolase gene confers enhanced cadmium tolerance by the restriction of root cadmium uptake in transgenic tobacco. Environ Exp Bot 100:74–83
Hématy K, Cherk C, Somerville S (2009) Host-pathogen warfare at the plant cell wall. Curr Opin Biotech 12:406–413
Hossain A K M Z, Koyama H, Hara T (2006) Growth and cell wall properties of two wheat cultivars differing in their sensitivity to aluminum stress. J Plant Physiol 163:39–47
Houston K, Tucker MR, Chowdhury J, Shirley N, Little A (2016) The plant Cell Wall: a complex and dynamic structure as revealed by the responses of genes under stress conditions. Front Plant Sci 7:1–18
Inoue H, Fukuoka D, Tatai Y, Kamachi H, Hayatsu M, Ono M, Suzuki S (2013) Properties of lead deposits in cell walls of radish (Raphanus sativus) roots. J Plant Res 126:51–61
Kochian LV, Piñeros MA, Liu J, Magalhaes JV (2015) Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Ann Rev Plant Biol 66:571–598
Kollárová K, Kamenická V, Vatehová Z, Lišková D (2018) Impact of galactoglucomannan oligosaccharides and cd stress on maize root growth parameters, morphology, and structure. J Plant Physiol 222:59–66
Konno H, Nakashima S, Katoh K (2010) Metal-tolerant moss Scopelophila cataractae accumulates copper in the cell wall pectin of the protonema. J Plant Physiol 167:358–364
Krämer U (2010) “Metal hyperaccumulation in plants” Ann Rev Plant Biol 61(1):517–534
Krzesłowska 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
Krzesłowska M, Rabęda I, Basińska A, Lewandowski M, Mellerowicz EJ, Napieralska A, Samardakiewicz S, Woźny A (2016) Pectinous cell wall thickenings formation – a common defense strategy of plants to cope with Pb. Environ Pollut 214:354–361
Krzesłowska M, Timmers A.C.J, Mleczek M, Niedzielski P, Rabęda I, Woźny A, Goliński P, 2019. Alterations of root architecture and cell wall modifications in Tilia cordata miller (Linden) growing on mining sludge, Environ Pollut 248:247–259
Kučerová D, Kollárová K, Zelko I, Vatehová Z, Lišková D (2014) Galactoglucomannan oligosaccharides alleviate cadmium stress in Arabidopsis. J Plant Physiol 171:518–524
Lasat MM, Baker AJ, 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(3):875–883
Li F, Ren S, Zhang W, Xu Z, Xie G, Chen Y, Tu Y, Li Q, Zhou S, Li Y, Tu F, Liu L, Wang Y, Jiang J, Qin J, Li S, Li Q, Jing H, Zhou F, Gutterson N, Peng L (2013) Arabinose substitution degree in xylan positively affects lignocellulose enzymatic digestibility after various NaOH/H2SO4 pretreatments in Miscanthus. Bioresour Technol 130:629–637
Li JT, Gurajala HK, Wu L, Ent AVD, Qiu R, Baker AJM, Tang Y, Yang X, Shu W (2018) Hyperaccumulator plants from China: a synthesis of the current state of knowledge. Environ Sci Technol 52:11980–11994
Li T, Tao Q, Shohag MJI, Yang X, Sparks DL, Liang Y (2015) Root cell wall polysaccharides are involved in cadmium hyperaccumulation in Sedum alfredii. Plant Soil 389:387–399
Li T, Yang X, Ma H, Lu L (2007) Zinc adsorption and desorption characteristics in root cell wall involving zinc hyperaccumulation in Sedum alfredii Hance. Journal of Zhejiang University B(biomedical and bioengineering edition) 8(2):111–115
Liu T, Shen C, Wang Y, Huang C, Shi J (2014) New insights into regulation of proteome and polysaccharide in cell wall of Elsholtzia splendens in response to copper stress. PLoS One 9:e109573
Lux A, Martinka M, Vaculik M, White PJ (2010) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37
Ma JF, Hiradate S, Nomoto K, Iwashita T, Matsumoto H (1997) Internal detoxification mechanism of Al in Hydrangea (identification of Al form in the leaves). Plant Physiol 113(4):1033
McCartha GL, Taylor CM, Ent AVD, Guillaume E, Gutiérrez DMN, Pollard AJ (2019) Phylogenetic and geographic distribution of nickel hyperaccumulation in neotropical Psychotria. American J Botany. https://doi.org/10.1002/ajb2.1362
Mengoni A, Baker AJM, Bazzicalupo M, Reeves RD, Adigüzel N, Chianni E, Galardi F, Gabbrielli R, Gonnelli C (2003) Evolutionary dynamics of nickel Hyperaccumulation in Alyssum revealed by ITS nrDNA analysis. New Phytol 159:691–699
Nishikubo N, Takahashi J, Roos AA, Derba-Maceluch M, Piens K, Brumer H, Teeri TT, Stalbrand H, Mellerowicz EJ (2011) Xyloglucan endo-Transglycosylase-mediated Xyloglucan rearrangements in developing wood of hybrid Aspen. Plant Physiol 155:399–413
Nunan KJ, Sims IM, Bacic A, Fincher RGB (1998) Changes in cell wall composition during ripening of grape berries. Plant Physiol 118(3):783–792
Park YB, Cosgrove DJ (2015) Xyloglucan and its interactions with other components of the growing Cell Wall. Plant Cell Physiol 56:180–194
Parrotta L, Guerriero G, Sergeant K, Cai G, Hausman JF (2015) Target or barrier? The cell wall of early- and later-diverging plants vs cadmium toxicity: differences in the response mechanisms. Front Plant Sci 6:133
Pelloux J, Rusterucci C, Mellerowicz E (2007) New insights into pectin methylesterase structure and function. Trends Plant Sci 12:267–277
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:45–45
Pollard AJ, Powell KD, Harper FA, Smith JAC (2002) The genetic basis of metal Hyperaccumulation in plants. Crit Rev Plant Sci 21:539–566
Rancour DM, Marita JM, Hatfield RD (2012) Cell wall composition throughout development for the model grass Brachypodium distachyon. Front Plant Sci 3:266
Reimann C, Fabian K, Flem B (2019) Cadmium enrichment in topsoil: separating diffuse contamination from biosphere-circulation signals. Sci Total Environ 651:1344–1355
Rennie EA, Scheller HV (2014) Xylan biosynthesis. Curr Opin Biotech 26(7):100–107
Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61(1):263–289
Schmohl N, Pilling J, Fisahn J, Horst WJ (2010) Pectin methylesterase modulates aluminium sensitivity in zea mays and solanum tuberosum. Physiol Plant 109(4):419–427
Singh AP, Tripathi SK, Nath P, Sane AP (2011) Petal abscission in rose is associated with the differential expression of two ethylene-responsive xyloglucan endotransglucosylase/hydrolase genes, RbXTH1 and RbXTH2. J Exp Bot 62(14):5091–5103
Song L, Valliyodan B, Prince S, Wan J, Nguyen H (2018) Characterization of the XTH gene family: new insight to the roles in soybean flooding tolerance. Int J Mol Sci 19:2705
Sulová Z, Baran R, Farkaš V (2001) Release of complexed xyloglucan endotransglycosylase (XET) from plant cell walls by a transglycosylation reaction with xyloglucan-derived oligosaccharides. Plant Physiol Bioch 39:927–932
Tucker M, Lou H, Aubert M, Wilkinson L, Little A, Houston K, Pinto S, Shirley N (2018) Exploring the role of Cell Wall-related genes and polysaccharides during plant development. Plants 7:42
Verbruggen N, Juraniec M, Baliardini C, Meyer C (2013) Tolerance to cadmium in plants: the special case of hyperaccumulators. Biometals 26:633–638
Wan J, Zhu X, Wang Y, Liu L, Zhang B, Li G, Zhou Y, Zheng S (2018) Xyloglucan Fucosylation modulates Arabidopsis Cell Wall hemicellulose Aluminium binding capacity. Sci Rep 8(1):428–439
Wang J, Su L, Yang J, Yuan J, Yin A, Qiu Q, Zhang K, Yang Z (2015) Comparisons of cadmium subcellular distribution and chemical forms between low-cd and high-cd accumulation genotypes of watercress (Nasturtium officinale L. R. Br.). Plant Soil 396:325–337
Wu J, Mock H, Giehl RFH, Pitann B, Mühling KH (2019) Silicon decreases cadmium concentrations by modulating root endodermal suberin development in wheat plants. J Hazard Mater 364:581–590
Wu, L H, Luo, Y M, Liu, Y J, Guo, F G, Zhou and S B (2013) Sedum plumbizincicola X.H. Guo et S.B. Zhou ex L.H. Wu (Crassulaceae): a new species from Zhejiang Province, China. Plant Syst Evol 299:487–498
Xin J, Zhang Y, Tian R (2018) Tolerance mechanism of Triarrhena sacchariflora (maxim.) Nakai. Seedlings to lead and cadmium: translocation, subcellular distribution, chemical forms and variations in leaf ultrastructure. Ecotox Environ Safe 165:611–621
Xiong YH, Yang XE, Ye ZQ, He ZL (2004) Characteristics of cadmium uptake and accumulation by two contrasting ecotypes of Sedum alfredii Hance. J Environ Sci Health A Tox Hazard Subst Environ Eng 39:2925–2940
Xuan Y, Zhou ZS, Li HB, Yang ZM (2016) Identification of a group of XTHs genes responding to heavy metal mercury, salinity and drought stresses in Medicago truncatula. Ecotox Environ Safe 132:153–163
Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR, Wu P, Zheng SJ (2007) Cell Wall polysaccharides are specifically involved in the exclusion of aluminum from the Rice root apex. Plant Physiol 146:602–611
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
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
Zhang B, Zhang L, Li F, Zhang D, Liu X, Wang H, Xu Z, Chu C, Zhou Y (2017) Control of secondary cell wall patterning involves xylan deacetylation by a GDSL esterase. Nat Plants 3:17017
Zhong H, Lãuchli A (1993) Changes of cell wall composition and polymer size in primary roots of cotton seedlings under high salinity. J Exp Bot 44(261):773–778
Zhu XF, Lei GJ, Jiang T, Liu Y, Li GX, Zheng SJ (2012a) Cell wall polysaccharides are involved in P-deficiency-induced cd exclusion in Arabidopsis thaliana. Planta 236:989–997
Zhu XF, Shi YZ, Lei GJ, Fry SC, Zhang BC, Zhou YH, Braam J, Jiang T, Xu XY, Mao CZ, Pan YJ, Yang JL, Wu P, Zheng SJ (2012b) XTH31, encoding an in vitro XEH/XET-active enzyme, regulates aluminum sensitivity by modulating in vivo XET action, Cell Wall Xyloglucan content, and aluminum binding capacity in Arabidopsis. Plant Cell 24:4731–4747
Zhu XF, Wan JX, Wu Q, Zhao XS, Zheng SJ, Shen RF (2017) PARVUS affects aluminium sensitivity by modulating the structure of glucuronoxylan in Arabidopsis thaliana. Plant Cell Environ 40:1916–1925
Zhu XF, Wan JX, Sun Y, Shi YZ, Braam J, Li GX, Zheng SJ (2014) Xyloglucan Endotransglucosylase-Hydrolase17 interacts with Xyloglucan Endotransglucosylase-Hydrolase31 to confer Xyloglucan Endotransglucosylase action and affect aluminum sensitivity in Arabidopsis. Plant Physiol 165:1566–1574
Zhu XF, Wang ZW, Dong F, Lei GJ, Shi YZ, Li GX, Zheng SJ (2013) Exogenous auxin alleviates cadmium toxicity in Arabidopsis thaliana by stimulating synthesis of hemicellulose 1 and increasing the cadmium fixation capacity of root cell walls. J Hazard Mater 263:398–403
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This research was financially supported by the National Natural Science Foundation of China (21477104, 41671315) and Zhejiang Provincial Natural Science Foundation of China (No. LZ18D010001).
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Guo, X., Liu, Y., Zhang, R. et al. Hemicellulose modification promotes cadmium hyperaccumulation by decreasing its retention on roots in Sedum alfredii. Plant Soil 447, 241–255 (2020). https://doi.org/10.1007/s11104-019-04339-9
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DOI: https://doi.org/10.1007/s11104-019-04339-9