Abstract
Aims
Cadmium (Cd) is absorbed by plants into the food chain as a trace pollutant harmful to humans. The rice (Oryza sativa. L) glycosyltransferases (OsGTs) family is a large protein family with over hundreds of members, however, prior studies have failed to identify which OsGTs has a role in plants' response to Cd toxicity. In this study, we defined the role of OsGT17 in the regulation of grain Cd accumulation in rice.
Methods
One-week-old Zhonghua 11 (ZH11), osgt17 mutants, and OsGT17 overexpressing lines were treated with or without 1 μM Cd in solution for 7 days. Roots were then harvested for analysis of Cd as well as for cell wall and RNA extraction, while shoots were collected for Cd analysis.
Results
OsGT17 was located in the cell wall and displayed constitutive expression, despite its expression and protein accumulation were repressed by Cd. OsGT17 positively regulated Cd resistance in rice, as osgt17 mutants exhibited Cd sensitive phenotype while OsGT17 overexpressing plants exhibited Cd resistant phenotype. Furthermore, we showed that OsGT17 could regulate hemicellulose, especially xyloglucan level in root cell wall, which acted as a Cd compartmentalization sites, thus more Cd was accumulated in osgt17 mutants’ root cell wall and root, as a result, high levels of Cd were accumulated in osgt17 mutants’ shoots and grains that led them more sensitivity to Cd stress.
Conclusions
We first identified the role of a specific cell wall associated gene-OsGT17 in decreasing Cd accumulation in rice grains by fixing Cd in the root cell wall.
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Data availability
All data supporting the findings of this study are available within the paper and within its supplementary data published online.
References
Arrivault S, Senger T, Kramer U (2006) The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn oversupply. Plant J 46(5):861–879. https://doi.org/10.1111/j.1365-313X.2006.02746.x
Aspeborg H, Schrader J, Coutinho PM, Stam M, Kallas A, Djerbi S, Nilsson P, Denman S, Amini B, Sterky F, Master E, Sandberg G, Mellerowicz E, Sundberg B, Henrissat B, Teeri TT (2005) Carbohydrate-active enzymes involved in the secondary cell wall biogenesis in hybrid aspen. Plant Physiol 137(3):983–997. https://doi.org/10.1104/pp.104.055087
Bowles D, Isayenkova J, Lim EK, Poppenberger B (2005) Glycosyltransferases: managers of small molecules. Curr Opin Plant Biol 8(3):254–263. https://doi.org/10.1016/j.pbi.2005.03.007
Brown DM, Zeef LAH, Ellis J, Goodacre R, Turner SR, Notes AT (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17(8):2281–2295. https://doi.org/10.1105/tpc.105.031542
Brown DM, Goubet F, Wong VW, Goodacre R, Stephens E, Dupree P, Turner SR (2007) Comparison of five xylan synthesis mutants reveals new insight into the mechanisms of xylan synthesis. Plant J 52(6):1154–1168. https://doi.org/10.1111/j.1365-313X.2007.03307.x
Brown DM, Zhang ZN, Stephens E, Dupree P, Turner SR (2009) Characterization of IRX10 and IRX10-like reveals an essential role in glucuronoxylan biosynthesis in Arabidopsis. Plant J 57(4):732–746. https://doi.org/10.1111/j.1365-313X.2008.03729.x
Cao PJ, Bartley LE, Jung KH, Ronald PC (2008) Construction of a rice glycosyltransferase phylogenomic database and identification of rice-diverged glycosyltransferases. Mol Plant 1(5):858–877. https://doi.org/10.1093/mp/ssn052
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. https://doi.org/10.1007/s00425-002-0947-6
Chakrabarty D, Trivedi PK, Misra P, Tiwari M, Shri M, Shukla D, Kumar S, Rai A, Pandey A, Nigam D, Tripathi RD, Tuli R (2009) Comparative transcriptome analysis of arsenate and arsenite stresses in rice seedlings. Chemosphere 74(5):688–702. https://doi.org/10.1016/j.chemosphere.2008.09.082
Chen GC, Liu YQ, Wang RM, Zhang JF, Owens G (2013) Cadmium adsorption by willow root: the role of cell walls and their subfractions. Environ Sci Pollut Res 20:5665–5672. https://doi.org/10.1007/s11356-013-1506-3
Chen ZJ, Huang J, Li S, Shao JF, Shen RF, Zhu XF (2023) Salylic acid minimize cadmium accumulation in rice through regulating the fixation capacity of the cell wall to cadmium. Plant Sci 336:111839. https://doi.org/10.1016/j.plantsci.2023.111839
Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88(11):1707–1719. https://doi.org/10.1016/j.biochi.2006.07.003
Clemens S, Aarts MGA, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18(2):92–99. https://doi.org/10.1016/j.tplants.2012.08.003
Dalcorso G, Farinati S, Furini A (2010) Regulatory networks of cadmium stress in plants. Plant Signal Behav 5(6):663–667. https://doi.org/10.4161/psb.5.6.11425
Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46. https://doi.org/10.1016/j.envexpbot.2012.04.006
Guo JY, Zhang XZ, Ye DH, Huang HG, Wang YD, Zheng ZC, Li TX, Yu HY (2020) Crucial roles of cadmium retention in nodeII for restraining cadmium transport from straw to ear at reproductive period in a grain low-cadmium rice line (Oryza sativa L.). Ecotoxicol Environ Saf 205:111323. https://doi.org/10.1016/j.ecoenv.2020.111323
Hao XH, Zeng M, Wang J, Zeng ZZ, Dai JL, Xie ZJ, Yang YZ, Tian LF, Chen LB, Li DP (2018) A node-expressed transporter OsCCX2 is involved in grain cadmium accumulation of rice. Front Plant Sci 9:476. https://doi.org/10.3389/fpls.2018.00476
Huang J, Jing HK, Zhang Y, Chen SY, Wang HY, Cao Y, Zhang Z, Lu YH, Zheng QS, Shen RF, Zhu XF (2023) Melatonin reduces cadmium accumulation via mediating the nitric oxide accumulation and increasing the cell wall fixation capacity of cadmium in rice. J Hazard Mater 445:130529. https://doi.org/10.1016/j.jhazmat.2022.130529
Ishimaru Y, Takahashi R, Bashir K, Shimo H, Senoura T, Sugimoto K, Ono K, Yano M, Ishikawa S, Arao T, Nakanishi H, Nishizawa N (2012) Characterizing the role of rice NRAMP5 in Manganese, Iron and Cadmium Transport. Sci Rep 2:286. https://doi.org/10.1038/srep00286
Jing HK, Wu Q, Huang J, Yang XZ, Tao Y, Shen RF, Zhu XF (2022) Putrescine is involved in root cell wall phosphorus remobilization in a nitric oxide dependent manner. Plant Sci 316:111169. https://doi.org/10.1016/j.plantsci.2021.111169
Kawahigashi H (2009) Transgenic plants for phytoremediation of herbicides. Curr Opin Biotechnol 20(2):225–230. https://doi.org/10.1016/j.copbio.2009.01.010
Keppler BD, Showalter AM (2010) IRX14 and IRX14-LIKE, Two glycosyl transferases involved in glucuronoxylan biosynthesis and drought tolerance in Arabidopsis. Mol Plant 3(5):834–841. https://doi.org/10.1093/mp/ssq028
Klatte M, Schuler M, Wirtz M, Fink-Straube C, Hell R, Bauer P (2009) The analysis of Arabidopsis nicotianamine synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses. Plant Physiol 150(1):257–271. https://doi.org/10.1104/pp.109.136374
Lairson LL, Henrissat B, Davies GJ, Withers SG (2008) Glycosyltransferases structures, functions, and mechanisms. Annu Rev Biochem 77:521–555. https://doi.org/10.1146/annurev.biochem.76.061005.092322
Lee CH, O’Neill MA, Tsumuraya Y, Darvill AG, Ye ZH (2007a) The irregular xylem9 mutant is deficient in xylan xylosyltransferase activity. Plant Cell Physiol 48(11):1624–1634. https://doi.org/10.1093/pcp/pcm135
Lee CH, Zhong RQ, Richardson EA, Himmelsbach DS, McPhail BT, Ye ZH (2007b) The PARVUS gene is expressed in cells undergoing secondary wall thickening and is essential for glucuronoxylan biosynthesis. Plant Cell Physiol 48(12):1659–1672. https://doi.org/10.1093/pcp/pcm155
Lee CH, Teng Q, Huang WL, Zhong RQ, Ye ZH (2009) The F8H glycosyltransferase is a functional paralog of FRA8 involved in glucuronoxylan biosynthesis in Arabidopsis. Plant Cell Physiol 50(4):812–827. https://doi.org/10.1093/pcp/pcp025
Lin YF, Aarts MGM (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69(19):3187–3206. https://doi.org/10.1007/s00018-012-1089-z
Li TQ, Tao Q, Shohag MJI, Yang XE, Sparks D, Liang YC (2015) Root cell wall polysaccharides are involved in cadmium hyperaccumulation in Sedum alfredii. Plant Soil 389:387–399. https://doi.org/10.1007/s11104-014-2367-3
Li ZS, Yang Y, Guan WJ, Yu HY, Zou LY, Cui JH, Teng Y (2023) Insight into the subcellular mechanism of maximizing Cd accumulation in hyperaccumulator Solanum nigrum L. under the action of biodegradable chelating agent. Environ Exp Bot 207:105226. https://doi.org/10.1016/j.envexpbot.2023.105226
Lovegrove A, Wilkinson MD, Freeman J, Pellny TK, Tosi P, Saulnier L, Shewry PR, Mitchell RAC (2013) RNA interference suppression of genes in glycosyl transferase families 43 and 47 in wheat starchy endosperm causes large decreases in arabinoxylan content. Plant Physiol 163(1):95–107. https://doi.org/10.1104/pp.113.222653
Lu CN, Zhang LX, Tang Z, Huang XY, Ma JF, Zhao FJ (2019) Producing cadmium -free indica rice by overexpressing OsHMA3. Environ Int 126:619–626. https://doi.org/10.1016/j.envint.2019.03.004
Meng Y, Zhang XL, Wu Q, Shen RF, Zhu XF (2022) Transcription factor ANAC004 enhances Cd tolerance in Arabidopsis thaliana by regulating cell wall fixation, translocation and vacuolar detoxification of Cd, ABA accumulation and antioxidant capacity. J Hazard Mater 436:129121. https://doi.org/10.1016/j.jhazmat.2022.129121
Miyadate H, Adachi S, Hiraizumi A, Tezuka K, Nakazawa N, Kawamoto T, Katou K, Kodama I, Sakurai K, Takahashi H, Satoh-Nagasawa N, Watanabe A, Fujimura T, Akagi H (2011) OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol 189(1):190–199. https://doi.org/10.1111/j.1469-8137.2010.03459.x
Moons A (2003) Osgstu3 and osgstu4, encoding tau class glutathione S-transferases, are heavy metal- and hypoxic stress-induced and differentially salt stress-responsive in rice roots. FEBS Lett 553:427–432. https://doi.org/10.1016/S0014-5793(03)01077-9
Nakanishi H, Ogawa I, Ishimaru Y, Mori S, Nishizawa NK (2006) Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil Sci Plant Nutr 52(4):464–469. https://doi.org/10.1111/j.1747-0765.2006.00055.x
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. https://doi.org/10.3389/fpls.2015.00133
Pena MJ, Zhong RQ, Zhou GK, Richardson EA, O’Neill MA, Darvill AG, York WS, Ye ZH (2007) Arabidopsis irregular xylem8 and irregular xylem9: implications for the complexity of glucuronoxylan biosynthesis. Plant Cell 19(2):549–563. https://doi.org/10.1105/tpc.106.049320
Riaz M, Kamran M, Fang YZ, Yang GL, Rizwan M, Ali S, Zhou YY, Wang QQ, Deng LL, Wang YJ, Wang XR (2021) Boron supply alleviates cadmium toxicity in rice (Oryza sativa L.) by enhancing cadmium adsorption on cell wall and triggering antioxidant defense system in roots. Chemosphere 266:128938. https://doi.org/10.1016/j.chemosphere.2020.128938
Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24(5):2155–2167. https://doi.org/10.1105/tpc.112.096925
Schützendübel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R, Godbold DL, Polle A (2001) Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiol 127(3):887–898. https://doi.org/10.1104/pp.010318
Schröder P (2006) Enzymes transferring biomolecules to organic foreign compounds: a role for glucosyltransferase and glutathione S-transferase in phytoremediation. Phytoremediation Rhizoremediation 9A:133–142. https://doi.org/10.1007/978-1-4020-4999-4_10
Sharma R, Rensing C, Rosen BP, Mitra B (2000) The ATP hydrolytic activity of purified ZntA, a Pb(II)/Cd(II)/Zn(II)-translocating ATPase from Escherichia coli. J Biol Chem 275(6):3873–3878. https://doi.org/10.1074/jbc.275.6.3873
Smeets K, Ruytinx J, Semane B, Belleghem FV, Remans T, Sanden SV, Vangronsveld J, Cuyper A (2008) Cadmium-induced transcriptional and enzymatic alterations related to oxidative stress. Environ Exp Bot 63(1–3):1–8. https://doi.org/10.1016/j.envexpbot.2007.10.028
Takahashi R, Ishimaru Y, Nakanishi H, Nishizawa NK (2011a) Role of the iron transporter OsNRAMP1 in cadmium uptake and accumulation in rice. Plant Signal Behav 6(11):1813–1816. https://doi.org/10.4161/psb.6.11.17587
Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, Arao T, Nakanishi H, Nishizawa NK (2011b) The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J Exp Bot 62(14):4843–4850. https://doi.org/10.1093/jxb/err136
Takahashi R, Ishimaru Y, Shimo H, Ogo HS, Senoura T, Nishizawa NK, Nakanishi H (2012) The OsHMA2 transporter is involved in root to shoot translocation of Zn and Cd in rice. Plant Cell Environ 35(11):1948–1957. https://doi.org/10.1111/j.1365-3040.2012.02527.x
Tan LT, Qu MM, Zhu YX, Peng C, Wang JR, Gao DY, Chen CY (2020) ZINC TRANSPORTER5 and ZINC TRANSPORTER9 function synergistically in zinc/cadmium uptake. Plant Physiol 183(3):1235–1249. https://doi.org/10.1104/pp.19.01569
Tripathi P, Mishra A, Dwivedi S, Chakrabarty D, Trivedi PK, Singh RP, Tripathi RD (2012) Differential response of oxidative stress and thiol metabolism in contrasting rice genotypes for arsenic tolerance. Ecotoxicol Environ Saf 79:189–198. https://doi.org/10.1016/j.ecoenv.2011.12.019
Ueno D, Yamaji N, Kono I, Huang CF, Ando T, Yano M, Ma JF (2010) Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci USA 107(38):16500–16505. https://doi.org/10.1073/pnas.1005396107
Uraguchi S, Kamiya T, Sakamoto T, Kasai K, Sato Y, Nagamura Y, Yoshida A, Kyozuka J, Ishikawa S, Fujiwara T (2011) Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains. Proc Natl Acad Sci USA 108(52):20959–20964. https://doi.org/10.1073/pnas.1116531109
Uraguchi S, Fujiwara T (2012) Cadmium transport and tolerance in rice: perspectives for reducing grain cadmium accumulation. Rice 5(1):5. https://doi.org/10.1186/1939-8433-5-5
Vert G, Barberon M, Zelazny E, Séguéla M, Briat JF, Curie C (2009) Arabidopsis IRT2 cooperates with the high-affinity iron uptake system to maintain iron homeostasis in root epidermal cells. Planta 229:1171–1179. https://doi.org/10.1007/s00425-009-0904-8
Wang Y, Yu KF, Poysa V, Shi C, Zhou YH (2012) A single point mutation in GmHMA3 affects cadmium (Cd) translocation and accumulation in soybean seeds. Mol Plant 5(5):1154–1156. https://doi.org/10.1093/mp/sss069
Wang L, Li R, Yan XX, Liang XF, Sun YB, Xu YM (2020) Pivotal role for root cell wall polysaccharides in cultivar-dependent cadmium accumulation in Brassica chinensis L. Ecotoxicol Environ Saf 194:110369. https://doi.org/10.1016/j.ecoenv.2020.110369
Wu AM, Rihouey C, Seveno M, Hörnblad E, Singh SK, Matsunaga T, Ishii T, Lerouge P, Marchant A (2009) The Arabidopsis IRX10 and IRX10-LIKE glycosyltransferases are critical for glucuronoxylan biosynthesis during secondary cell wall formation. Plant J 57(4):718–731. https://doi.org/10.1111/j.1365-313X.2008.03724.x
Wu HL, Chen CL, Du J, Liu HF, Cui Y, Zhang Y, He Y, Wang YQ, Chu CC, Feng ZY, Li JM, Ling HQ (2012) Co-overexpression FIT with AtbHLH38 or AtbHLH39 in Arabidopsis-enhanced cadmium tolerance via increased cadmium sequestration in roots and improved iron homeostasis of shoots. Plant Physiol 158(2):790–800. https://doi.org/10.1104/pp.111.190983
Yan HL, Xu WX, Xie JY, Gao YW, Wu LL, Sun L, Feng L, Chen X, Zhang T, Dai CH, Li T, Lin XN, Zhang ZY, Wang XQ, Li FM, Zhu XY, Li JJ, Li ZC, Chen CY, Ma M, Zhang HL, He ZY (2019) Variation of a major facilitator superfamily gene contributes to differential cadmium accumulation between rice subspecies. Nat Commun 10:2562. https://doi.org/10.1038/s41467-019-10544-y
Yang CH, Zhang Y, Huang CF (2019) Reduction in cadmium accumulation in japonica rice grains by CRISPR/Cas9-mediated editing of OsNRAMP5. J Integr Agric 18(3):688–697. https://doi.org/10.1016/S2095-3119(18)61904-5
Yu HY, Guo JY, Li Q, Zhang XZ, Huang HG, Huang F, Yang AQ, Li TX (2020) Characteristics of cadmium immobilization in the cell wall of root in a cadmium-safe rice line (Oryza sativa L.). Chemosphere 241:125095. https://doi.org/10.1016/j.chemosphere.2019.125095
Zhong RQ, Peña MJ, Zhou GK, Nairn CJ, Wood-Jones A, Richardson EA, Morrison WH III, Darvill AG, York WS, Ye ZH (2005) Arabidopsis fragile fiber8, which encodes a putative glucuronyltransferase, is essential for normal secondary wall synthesis. Plant Cell 17(12):3390–3408. https://doi.org/10.1105/tpc.105.035501
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(2):398–403. https://doi.org/10.1016/j.jhazmat.2013.09.018
Zhu XF, Wang ZW, Wan JX, Sun Y, Wu YR, Li GX, Shen RF, Zheng SJ (2015) Pectin enhances rice (Oryza sativa) root phosphorus remobilization. J Exp Bot 66:1017–1024. https://doi.org/10.1093/jxb/eru461
Zhu XF, Zhu CQ, Wang C, Dong XY, Shen RF (2017a) Nitric oxide acts upstream of ethylene in cell wall phosphorus reutilization in phosphorus-deficient rice. J Exp Bot 68:753–760. https://doi.org/10.1093/jxb/erw480
Zhu XF, Wan JX, Wu Q, Zhao XS, Zheng SJ, Shen RF (2017b) PARVUS affects aluminium sensitivity by modulating the structure of glucuronoxylan in Arabidopsis thaliana. Plant Cell Environ 40(9):1916–1925. https://doi.org/10.1111/pce.12999
Funding
This study was supported by the National Natural Science Foundation of China (Grant No. 42020104004), the Field Frontier Program of the Institute of Soil Science (ISSASIP2215), the Agricultural Science and Technology Independent Innovation Fund Project of Jiangsu Province [CX(21)2034], the Key Research and Development Project of Jiangsu Province [BE2021717], and the Special Fund Project of Soil Pollution Prevention and Control [Xinyi Agriculture and Rural Bureau, New Collection List (2021) 1468].
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Tu, C.Y., Guo, R., Chen, C.Z. et al. Disruption of a glycosyl transferase family 17 protein alters cadmium accumulation and resistance in rice (Oryza sativa). Plant Soil (2024). https://doi.org/10.1007/s11104-024-06539-4
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DOI: https://doi.org/10.1007/s11104-024-06539-4