Abstract
Main conclusion
Heterogeneous expression of the rice genes “fruit-weight 2.2-like” (OsFWL) affects Cd resistance in yeast, and OsFWL4 mediates the translocation of Cd from roots to shoots.
Cadmium (Cd) induces chronic and toxic effects in humans. In a previous study (Xu et al. in Planta 238:643–655, 2013), we cloned the rice genes, designated OsFWL1-8, homologous to the tomato fruit-weight 2.2. Here, we show that expression of genes OsFWL3-7 in yeast confers resistance to Cd. The Cd contents of OsFWL3-, -4-, -6- and -7-transformed Cd(II)-sensitive yeast mutant ycf1 cells were strongly decreased compared with those of empty vector, with the strongest resistance to Cd observed in cells expressing OsFWL4. Evaluation of truncated and site-directed mutation derivatives revealed that the CCXXG motifs near the second transmembrane region of OsFWL4 are involved in Cd resistance in yeast. Real-time PCR analysis showed that OsFWL4 expression was induced by CdCl2 stress in rice seedlings. Compared with WT plants, the Cd contents in the shoots of RNAi mediated OsFWL4 knockdown plants were significantly decreased, and Cd translocation from roots to shoots was reduced. According to bimolecular fluorescence complementation, yeast two-hybrid and Western-blotting assays, the OsFWL4 protein forms homo-oligomers. These results suggest that OsFWL4 might act directly as a transporter and is involved in the translocation of Cd from roots to shoots in rice.
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Abbreviations
- FW2.2:
-
Fruit-weight 2.2
- HMA:
-
Heavy metal ATPase
- LCT1:
-
Low-affinity cation transporter 1
- NRAMP:
-
Natural resistance-associated macrophage protein
- OsFWL:
-
Oryza sativa FW2.2-like
- PLAC8:
-
Placenta-specific 8
References
Abbà S, Vallino M, Daghino S, Di Vietro L, Borriello R, Perotto S (2011) A PLAC8-containing protein from an endomycorrhizal fungus confers cadmium resistance to yeast cells by interacting with Mlh3p. Nucleic Acids Res 39:7548–7563
Arao T, Ae N (2003) Genotypic variations in cadmium levels of rice grain. Soil Sci Plant Nutr 49:473–479
Baekgaard L, Mikkelsen MD, Sorensen DM, Hegelund JN, Persson DP, Mills RF, Yang Z, Husted S, Andersen JP, Buch-Pedersen MJ, Schjoerring JK, Williams LE, Palmgren MG (2010) A combined zinc/cadmium sensor and zinc/cadmium export regulator in a heavy metal pump. J Biol Chem 285:31243–31252
Chen J, Yang L, Gu J, Bai X, Ren Y, Fan T, Han Y, Jiang L, Xiao F, Liu Y, Cao S (2015) MAN3 gene regulates cadmium tolerance through the glutathione—dependent pathway in Arabidopsis thaliana. New Phytol 205:570–582
Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486
Clemens S, Antosiewicz DM, Ward JM, Schachtmani DP, Schroeder JI (1998) The plant cDNA LCT1 mediates the uptake of calcium and cadmium in yeast. Proc Natl Acad Sci USA 95:12043–12048
Clemens S, Kim EJ, Neumann D, Schroeder JI (1999) Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J 18:3325–3333
Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182
Cobbett CS, May MJ, Howden R, Rolls B (1998) The glutathione-deficient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in γ-glutamylcysteine synthetase. Plant J 16:73–78
Dahan Y, Rosenfeld R, Zadiranov V, Irihimovitch V (2010) A proposed conserved role for an avocado fw2.2-like gene as a negative regulator of fruit cell division. Planta 232:663–676
De Franceschi P, Stegmeir T, Cabrera A, van der Knaap E, Rosyara UR, Sebolt AM, Dondini L, Dirlewanger E, Quero-Garcia J, Campoy JA, Iezzoni AF (2013) Cell number regulator genes in Prunus provide candidate genes for the control of fruit size in sweet and sour cherry. Mol Breed 32:311–326
Egan SK, Bolger PM, Carrington CD (2007) Update of US FDA’s total diet study food list and diets. J Expo Sci Environ Epidemiol 17:573–582
Eren E, Kennedy DC, Maroney MJ, Arguello JM (2006) A novel regulatory metal binding domain is present in the C terminus of Arabidopsis Zn2+-ATPase HMA2. J Biol Chem 281:33881–33891
Frary A, Nesbitt TC, Frary A, Grandillo S, van der Knaap E, Cong B, Jp Liu, Meller J, Elber R, Alpert KB, Tanksley SD (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289:85–88
Gazzarrini S, Kang M, Abenavoli A, Romani G, Olivari C, Gaslini D, Ferrara G, van Etten James L, Kreim M, Kast Stefan M, Thiel G, Moroni A (2009) Chlorella virus ATCV-1 encodes a functional potassium channel of 82 amino acids. Biochem J 420:295–305
Gonzalez-Mendoza D, Moreno AQ, Zapata-Perez O (2007) Coordinated responses of phytochelatin synthase and metallothionein genes in black mangrove, Avicennia germinans, exposed to cadmium and copper. Aquat Toxicol 83:306–314
Grill E, Winnacker E-L, Zenk MH (1985) Phytochelatins: the principal heavy-metal complexing peptides of higher plants. Science 230:674–676
Guo M, Rupe MA, Dieter JA, Zou J, Spielbauer D, Duncan KE, Howard RJ, Hou Z, Simmons CR (2010) Cell number regulator 1 affects plant and organ size in maize: implications for crop yield enhancement and heterosis. Plant Cell 22:1057–1073
Ha SB, Smith AP, Howden R, Dietrich WM, Bugg S, O’Connell MJ, Goldsbrough PB, Cobbett CS (1999) Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. Plant Cell 11:1153–1163
Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282
Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51–59
Honda R, Swaddiwudhipong W, Nishijo M, Mahasakpan P, Teeyakasem W, Ruangyuttikarn W, Satarug S, Padungtod C, Nakagawa H (2010) Cadmium induced renal dysfunction among residents of rice farming area downstream from a zinc-mineralized belt in thailand. Toxicol Lett 198:26–32
Horiguchi H, Aoshima K, Oguma E, Sasaki S, Miyamoto K, Hosoi Y, Katoh T, Kayama F (2010) Latest status of cadmium accumulation and its effects on kidneys, bone, and erythropoiesis in inhabitants of the formerly cadmium-polluted Jinzu River Basin in Toyama, Japan, after restoration of rice paddies. Int Arch Occup Environ Health 83:953–970
Howden R, Andersen CR, Coldsbrough PB, Cobbet CS (1995) A cadmium-sensitive, glutathione-deficient mutant of Arabidopsis thaliana. Plant Physiol 107:1067–1073
Ishikawa S, Suzui N, Ito-Tanabata S, Ishii S, Igura M, Abe T, Kuramata M, Kawachi N, Fujimaki S (2011) Real-time imaging and analysis of differences in cadmium dynamics in rice cultivars (Oryza sativa) using positron-emitting107Cd tracer. BMC Plant Biol 11:172
Ishikawa S, Ishimaru Y, Igura M, Kuramata M, Abe T, Senoura T, Hase Y, Arao T, Nishizawa NK, Nakanishi H (2012) Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. Proc Natl Acad Sci USA 109:19166–19171
Ishimaru Y, Takahashi R, Bashir K, Shimo H, Senoura T, Sugimoto K, Nakanishi H (2012) Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport. Sci Rep 2:286
Jarup L, Akesson A (2009) Current status of cadmium as an environmental health problem. Toxicol Appl Pharm 238:201–208
Jin T, Nordberg M, Frech W, Dumont X, Bernard A, Ye TT, Kong Q, Wang Z, Li P, Lundström NG, Li Y, Nordberg GF (2002) Cadmium biomonitoring and renal dysfunction among a population environmentally exposed to cadmium from smelting in China (ChinaCad). Biometals 15:397–410
Kobayashi T, Nishizawa NK (2014) Iron sensors and signals in response to iron deficiency. Plant Sci 224:36–43
Kuramata M, Masuya S, Takahashi Y, Kitagawa E, Inoue C, Ishikawa S, Youssefian S, Kusano T (2008) Novel cysteine-rich peptides from Digitaria ciliaris and Oryza sativa enhance tolerance to cadmium by limiting its cellular accumulation. Plant Cell Physiol 50:106–117
Lam SK, Siu CL, Hillmer S, Jang S, An G, Robinson DG, Jiang L (2007) Rice SCAMP1 defines clathrin-coated, trans-golgi-located tubular-vesicular structures as an early endosome in tobacco BY-2 cells. Plant Cell 19:296–319
Lanquar V, Lelièvre F, Barbier-Brygoo H, Thomine S (2004) Regulation and function of AtNRAMP4 metal transporter protein. Soil Sci Plant Nutr 50:1141–1150
Lanquar V, Lelièvre F, Bolte S, Hamès C, Alcon C, Neumann D, Vansuyt G, Curie C, Schröder A, Krämer U, Barbier-Brygoo H, Thomine S (2005) Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J 24:4041–4051
Libault M, Zhang X-C, Govindarajulu M, Qiu J, Ong YT, Brechenmacher L, Berg RH, Hurley-Sommer A, Taylor CG, Stacey G (2010) A member of the highly conserved FWL (tomato FW2.2-like) gene family is essential for soybean nodule organogenesis. Plant J 62:852–864
Masters BA, Kelly EJ, Quaife CJ, Brinster RL, Palmiter RD (1994) Targeted disruption of metallothionein I and II genes increases sensitivity to cadmium. Proc Natl Acad Sci USA 91:584–588
Matsuda T, Kuramata M, Takahashi Y, Kitagawa E, Youssefian S, Kusano T (2009) A novel plant cysteine-rich peptide family conferring cadmium tolerance to yeast and plants. Plant Signal Behav 4:419–421
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 189:190–199
Molins H, Michelet L, Lanquar V, Agorio A, Giraudat J, Roach T, Krieger-Liszkay A, Thomine S (2013) Mutants impaired in vacuolar metal mobilization identify chloroplasts as a target for cadmium hypersensitivity in Arabidopsis thaliana. Plant Cell Environ 36:804–817
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiol Plant 15:473–497
Nakagawa Y, Katagiri T, Shinozaki K, Qi Z, Tatsumi H, Furuichi T, Kishigami A, Sokabe M, Kojima I, Sato S, Kato T, Tabata S, Iida K, Terashima A, Nakano M, Ikeda M, Yamanaka T, Iida H (2007) Arabidopsis plasma membrane protein crucial for Ca2+ influx and touch sensing in roots. Proc Natl Acad Sci USA 104:3639–3644
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 52:464–469
Nakano M, Iida K, Nyunoya H, Iida H (2011) Determination of structural regions important for Ca(2+) uptake activity in Arabidopsis MCA1 and MCA2 expressed in yeast. Plant Cell Physiol 52:1915–1930
Nordberg GF, Jin T, Kong Q, Ye T, Cai S, Wang Z, Zhuang F, Wu X (1997) Biological monitoring of cadmium exposure and renal effects in a population group residing in a polluted area in China. Sci Total Environ 199:111–114
Oda K, Otani M, Uraguchi S, Akihiro T, Fujiwara T (2011) Rice ABCG43 is Cd inducible and confers Cd tolerance on yeast. Biosci Biotechnol Biochem 75:1211–1213
Qiao Z, Brechenmacher L, Smith B, Strout GW, Mangin W, Taylor C, Russell SD, Stacey G, Libault M (2017) The GmFWL1 (FW2.2-like) nodulation gene encodes a plasma membrane microdomain-associated protein. Plant Cell Environ 40:1442–1455. https://doi.org/10.1111/pce.12941
Rodda MS, Li G, Reid RJ (2011) The timing of grain Cd accumulation in rice plants: the relative importance of remobilisation within the plant and root Cd uptake post-flowering. Plant Soil 347:105–114
Sasaki A, Yamaji N, Yokosho K, Ma J (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24:2155–2167
Satoh-Nagasawa N, Mori M, Nakazawa N, Kawamoto T, Nagato Y, Sakurai K, Takahashi H, Watanabe A, Akagi H (2011) Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol 53:213–224
Satoh-Nagasawa N, Mori M, Sakurai K, Takahashi H, Watanabe A, Akagi H (2013) Functional relationship heavy metal P-type ATPases (OsHMA2 and OsHMA3) of rice (Oryza sativa) using RNAi. Plant Biotechnol 30:511–515
Shimo H, Ishimaru Y, An G, Yamakawa T, Nakanishi H, Nishizawa NK (2011) Low cadmium (LCD), a novel gene related to cadmium tolerance and accumulation in rice. J Exp Bot 62:5727–5734
Sobrino-Plata J, Meyssen D, Cuypers A, Escobar C, Hernández LE (2014) Glutathione is a key antioxidant metabolite to cope with mercury and cadmium stress. Plant Soil 377:369–381
Song WY, Martinoia E, Lee J, Kim D, Kim DY, Vogt E, Shim D, Choi KS, Hwang I, Lee Y (2004) A novel family of cys-rich membrane proteins mediates cadmium resistance in Arabidopsis. Plant Physiol 135:1027–1039
Song WY, Choi KS, Kim do Y, Geisler M, Park J, Vincenzetti V, Schellenberg M, Kim SH, Lim YP, Noh EW, Lee Y, Martinoia E (2010) Arabidopsis PCR2 is a zinc exporter involved in both zinc extrusion and long-distance zinc transport. Plant Cell 22:2237–2252
Song W-Y, Lee H-S, Jin S-R, Ko D, Martinoia E, Lee Y, An G, Ahn S-N (2015) Rice PCR1 influences grain weight and Zn accumulation in grains. Plant Cell Environ 38:2327–2339
Su C, Jiang L, Zhang W (2014) A review on heavy metal contamination in the soil worldwide: situation, impact and remediation techniques. Environ Skept Crit 3:24
Szczypka MS, Wemmie JA, Moye-Rowley WS, Thiele DJ (1994) Yeast metal resistance protein similar to human cystic fibrosis transmembrane conductance regulator (CFTR) and multidrug resistance-associated protein. J Biol Chem 269:22853–22857
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 6:1813–1816
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 62:4843–4850
Takahashi R, Bashir K, Ishimaru Y, Nishizawa N, Nakanishi H (2012) The role of heavy-metal ATPases, HMAs, in zinc and cadmium transport in rice. Plant Signal Behav 7:1605–1607
Thomine S, Lelièvre F, Debarbieux E, Schroeder JI, Barbier-Brygoo H (2003) AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J 34:685–695
Ueno D, Yamaji N, Kono I, Huang C, Ando T, Yano M, Ma JF (2010) Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci USA 107:16500–16505
Uraguchi S, Fujiwara T (2012) Cadmium transport and tolerance in rice: perspectives for reducing grain cadmium accumulation. Rice 5:1–8
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 108:20959–20964
Vert G, Grotz N, Dédaldéchamp F, Gaymard F, Guerinot M, Briat J, Curie C (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1223–1233
Voelker C, Schmidt D, Mueller-Roeber B, Czempinski K (2006) Members of the Arabidopsis AtTPK/KCO family form homomeric vacuolar channels in planta. Plant J 48:296–306
Waadt R, Schmidt LK, Lohse M, Hashimoto K, Bock R, Kudla J (2008) Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J 56:505–516
Wang F, Wang M, Liu Z, Shi Y, Han T, Ye Y, Gong N, Sun J, Zhu C (2015a) Different responses of low grain-Cd-accumulating and high grain-Cd-accumulating rice cultivars to Cd stress. Plant Physiol Biochem 96:261–269
Wang Y, Zeng H, Zhou X, Huang F, Peng W, Liu L, Xiong W, Shi X, Luo M (2015b) Transformation of rice with large maize genomic DNA fragments containing high content repetitive sequences. Plant Cell Rep 34:1049–1061
Williams LE, Mills RF (2005) P1B-ATPases—an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci 10:491–502
Wolnik KA, Fricke FL, Capar SG, Braude GL, Meyer MW, Satzger RD, Bonnin E (1983) Elements in major raw agricultural crops in the United States. 1. Cadmium and lead in lettuce, peanuts, potatoes, soybeans, sweet corn, and wheat. J Agric Food Chem 31:1240–1244
Xu J, Xiong WT, Cao BB, Yan TZ, Luo T, Fan TT, Luo MZ (2013) Molecular characterization and functional analysis of “fruit-weight 2.2-like” gene family in rice. Planta 238:643–655
Yamanaka T, Nakagawa Y, Mori K, Nakano M, Imamura T, Kataoka H, Terashima A, Iida K, Kojima I, Katagiri T, Shinozaki K, Iida H (2010) MCA1 and MCA2 that mediate Ca2+ uptake have distinct and overlapping roles in Arabidopsis. Plant Physiol 152:1284–1296
Yang M, Zhang Y, Zhang L, Hu J, Zhang X, Lu K, Dong H, Wang D, Zhao F-J, Huang C-F, Lian X (2014) OsNRAMP5 contributes to manganese translocation and distribution in rice shoots. J Exp Bot 65:4849–4861
Yuan L, Yang S, Liu B, Zhang M, Wu K (2012) Molecular characterization of a rice metal tolerance protein, OsMTP1. Plant Cell Rep 31:67–79
Zhou J, Goldsbrough PB (1994) Functional homologs of fungal metallothionein genes from Arabidopsis. Plant Cell 6:875–884
Zimeri AM, Dhankher OP, McCaig B, Meagher RB (2005) The plant MT1 metallothioneins are stabilized by binding cadmiums and are required for cadmium tolerance and accumulation. Plant Mol Biol 58:839–855
Acknowledgements
We thank Dr. Dennis J Thiele (Duke University School of Medicine) for kindly providing the Cd-sensitive ycf1 mutant and Professor Jian Xu (National University of Singapore) for providing the pM999 vectors. We also thank Dr. Tao Luo (Nanchang University) and Tingting Fan (Humboldt-Universitat zu Berlin) for technical assistance. This work was supported by the National Natural Science Foundation of China (Grant no. 31671268).
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Xiong, W., Wang, P., Yan, T. et al. The rice “fruit-weight 2.2-like” gene family member OsFWL4 is involved in the translocation of cadmium from roots to shoots. Planta 247, 1247–1260 (2018). https://doi.org/10.1007/s00425-018-2859-0
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DOI: https://doi.org/10.1007/s00425-018-2859-0