Type 4 metallothionein genes are involved in regulating Zn ion accumulation in late embryo and in controlling early seedling growth in Arabidopsis

Plant, Cell and Environment

Volumn 35, Issue 4, 2012, Pages 770-789

  Ren, Yujun ^a   Liu, Yang ^a   Chen, Hongyu ^a   Li, Gang ^a   Zhang, Xuelian ^a   Zhao, Jie ^a  

^a WUHAN UNIVERSITY   (China)

Author keywords

ABA; AtMT4a; AtMT4b; GA

Indexed keywords

ABSCISIC ACID; ARABIDOPSIS PROTEIN; ATMT4A, PROTEIN, ARABIDOPSIS; COPPER; GIBBERELLIC ACID; GIBBERELLIN; METALLOTHIONEIN; PHYTOHORMONE; ZINC;

ABSCISIC ACID; BIOACCUMULATION; CATION; CYTOPLASM; DICOTYLEDON; EMBRYONIC DEVELOPMENT; FUNCTIONAL ROLE; GENE EXPRESSION; GENETIC ANALYSIS; GERMINATION; SEEDLING EMERGENCE; ZINC;

ARABIDOPSIS; ARTICLE; BIOMASS; COTYLEDON; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHENOTYPE; PLANT GROWTH; PLANT ROOT; PLANT SEED; PRENATAL DEVELOPMENT; PROMOTER REGION; SEEDLING; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOMASS; COPPER; COTYLEDON; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; GERMINATION; GIBBERELLINS; HYPOCOTYL; METALLOTHIONEIN; MUTATION; PHENOTYPE; PLANT GROWTH REGULATORS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; SEEDLING; SEEDS; SIGNAL TRANSDUCTION; ZINC;

ARABIDOPSIS; EMBRYOPHYTA; TRACHEOPHYTA;

EID: 84857997111     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2011.02450.x     Document Type: Article

References (85)

1. An Z.G., Li C.J., Zu Y.G., Du Y.J., Andreas W., Roland G. & Thomas R. (2006) Expression of BjMT2, a metallothionein 2 from Brassica juncea, increases copper and cadmium tolerance in Escherichia coli and Arabidopsis thaliana, but inhibits root elongation in Arabidopsis thaliana seedlings. Journal of Experimental Botany 57, 3575-3582.
2. Audran C., Liotenberg S., Gonneau M., North H., Frey A., Tap-Waksman K., Vartnanian N. & Marion-Poll A. (2001) Localization and expression of zeaxanthin epoxidase mRNA in Arabidopsis in response to draught stress and during seed development. Australian Journal of Plant Physiology 28, 1161-1173.
3. Bausher M., Shatters R., Chaparro J., Dang P., Hunter W. & Niedz R. (2003) An expressed sequence tag (EST) set from Citrus sinensis L. Osbeck whole seedlings and the implications of further perennial source investigations. Plant Science 165, 415-422.
4. Bi Y.M., Zhang Y., Signorelli T., Zhao R. & Rothstein S. (2005) Genetic analysis of Arabidopsis GATA transcription factor gene family reveals a nitrate-inducible member important for chlorophyll synthesis and glucose sensitivity. The Plant Journal 44, 680-692.
5. Blindauer C.A., Harrison M.D., Robinson A.K., Parkinson J.A., Bowness P.W., Sadler P.J. & Robinson N.J. (2002) Multiple bacteria encode metallothioneins and SmtA-like zinc fingers. Molecular Microbiology 45, 1421-1432.
6. Cakmak I. (2000) Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytologist 146, 185-205.
7. Charbonnel-Campaa L., Lauge B. & Combes D. (2000) Isolation of a type 2 metallothionein like gene preferentially expressed in the tapetum in Zea mays. Gene 254, 199-208.
8. Chatthai M., Kaukinen K.H., Tranbarger T.J., Gupta P.K. & Misra S. (1997) The isolation of a novel metallothionein-related cDNA expressed in somatic and zygotic embryos of Douglas-fir: regulation by ABA, osmoticum and metal ions. Plant Molecular Biology 34, 243-254.
9. Chatthai M., Osusky M., Osuska L., Yevtushenko D. & Misra S. (2004) Functional analysis of a Douglas-fir metallothionein-like gene promoter: transient assays in zygotic and somatic embryos and stable transformation in transgenic tobacco. Planta 220, 118-128.
10. Cheng W.H., Endo A., Zhou L., etal. (2002) A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. The Plant Cell 14, 2723-2743.
11. Chyan C.L., Lee T.T.T., Liu C.P., Yang Y.C., Tzen J.T. & Chou W.M. (2005) Cloning and expression of a seed-specific metallothionein-like protein from sesame. Bioscience, Biotechnology, and Biochemistry 69, 2319-2325.
12. Cobbett C.S. & Goldsbrough P.B. (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annual Review of Plant Biology 53, 159-182.
13. Coyle P., Zalewski P.Z., Philcox J.C., Forves I.J., Ward A.D., Lincoln S.F., Mahadevan I. & Rofe A.M. (1994) Measurement of zinc in hepatocytes by using a flurenscent probe, zinquin: relationship to metallothionein and intracellular zinc. Biochemical Journal 303, 781-786.
14. Dong J.Z. & Dunstan D.I. (1996) Expression of abundant mRNAs during somatic embryogenesis of white spruce [Picea glauca (Moench) Voss]. Planta 199, 459-466.
15. Evans K.M., Gatehouse J.A., Lindsay W.P., Shi J., Tommey A.M. & Robison N.J. (1992) Expression of the pea metallothionein-like gene PsMTA in Escherichia coli and Arabidopsis thaliana and analysis of trace-metal ion accumulation implications for PsMTA function. Plant Molecular Biology 20, 1019-1028.
16. Figueira A., Kido E.A. & Almeida R.S. (2001) Identification sugarcane expressed sequences associated with nutrient transporters and peptide metal chelators. Genetics and Molecular Biology 24, 207-220.
17. Finkelstein R.R., Gampala S.S. & Rock C.D. (2002) Abscisic acid signaling in seeds and seedlings. The Plant Cell 14 (Suppl.), s15-s45.
18. Foley R.C. & Singh K.B. (1994) Isolation of a Vicia faba metallothionein-like gene expression in foliar trichomes. Plant Molecular Biology 26, 435-444.
19. Freisinger E. (2008) Plant MTs - long neglected members of the metallothionein superfamily. Dalton Transactions 47, 6663-6675.
20. Giacomelli L., Rudella A. & van Wijk K.J. (2006) High light response of the thylakoid proteome in Arabidopsis wild type and the ascorbate-deficient mutant vtc2-2. A comparative proteomics study. Plant Physiology 141, 685-701.
21. Giritch A., Ganal M., Stephan U.W. & Baumlein H. (1998) Structure, expression and chromosome localization of the metallothionein-like gene family of tomato. Plant Molecular Biology 37, 701-714.
22. Goldberg R.B., de Paiva G. & Yadegari R. (1994) Plant embryogenesis: zygote to seed. Science 266, 605-614.
23. González-Guzmán M., Apostolova N., Bellés J.M., Barrero J.M., Piqueras P., Ponce M.R., Micol J.L., Serrano R. & Rodríguez P.L. (2002) The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde. The Plant Cell 14, 1833-1846.
24. Grotz N., Fox T., Connolly E., Park W., Guerinot M.L. & Eide D. (1998) Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proceedings of the National Academy of Sciences of the United States of America 95, 7220-7224.
25. Guo W.J., Bundithya W. & Goldsbrough P.B. (2003) Characterization of the Arabidopsis metallothionein gene family: tissue-specific expression and induction during senescence and in response to copper. New Phytologist 159, 369-381.
26. Guo W.J., Metha M. & Goldsbrough P.B. (2008) Examining the specific contribution of individual Arabidopsis metallothioneins to copper distribution and metal tolerance. Plant Physiology 146, 1697-1706.
27. Gutierrez L., Wuytswinkel O.V., Castelain M. & Bellini C. (2007) Combined networks regulating seed maturation. Trends in Plant Science 12, 294-300.
28. Hajduch M., Hearne L.B., Miernyk J.A., Casteel J.E., Joshi T., Agrawal G.K., Song Z., Zhou M., Xu D. & Thelen J.J. (2010) Systems analysis of seed filling in Arabidopsis: using general linear modeling to assess concordance of transcript and protein expression. Plant Physiology 152, 2078-2087.
29. Hamer D.H. (1986) Metallothionein. Annual Review of Biochemistry 55, 913-951.
30. Hänsch R. & Mendel R.R. (2009) Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Current Opinion in Plant Biology 12, 259-266.
31. Hasler D.W., Jensen L.T., Zerbe O., Winge D.R. & Vašák M. (2000) Effect of the two conserved pralines of human growth inhibitory factors (metalothionein-3) on its biological activity and structure fluctuation: comparison with a mutant protein. Biochemistry 39, 14567-14575.
32. 2+ complexes. Journal of the American Chemical Society 125, 3889-3895.
33. Hsieh H.M., Liu W.K. & Huang P.C. (1995) A novel stress-inducible metallothionein-like gene from rice. Plant Molecular Biology 28, 381-389.
34. Iuchi S., Kobayashi M., Taji T., Naramoto M., Seki M., Kato T., Tabata S., Kakubari Y., Yamaguchi-Shinozaki K. & Shinozaki K. (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. The Plant Journal 27, 325-333.
35. Kagi J.H.R. (1991) Overview of metallothionein. Methods in Enzymology 205, 613-626.
36. 2+ metallothionein genes are conspicuously expressed during embryogenesis. European Journal of Biochemistry 209, 971-976.
37. Kong X.P., Pan J.W., Zhang M.Y., Xing X., Zhou Y., Liu Y., Li D.P. & Li D.Q. (2011) ZmMKK4, a novel group C mitogen-activated protein kinase in Maize (Zea mays), confers salt and cold tolerance in transgenic Arabidopsis. Plant, Cell & Environment 34, 1291-1303.
38. Krämer U. & Clemens S. (2005) Functions and homeostasis of zinc, copper, and nickel in plants. Topics in Current Genetics 14, 215-271.
39. Kucera B., Cohn M.A. & Leubner-Metzger G. (2005) Plant hormone interactions during seed dormancy release and germination. Seed Science research 15, 281-307.
40. Kushiro T., Okamoto M., Nakabayashi K., Yamagishi K., Kitamura S., Asami T., Hirai N., Koshiba T., Kamiya Y. & Nambara E. (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8'-hydroxylases: key enzymes in ABA catabolism. EMBO Journal 23, 1647-1656.
41. C protein is a zinc-containing metallothionein. Biochemistry and Cell Biology 33, 1001-1005.
42. Lefebvre V., North H., Frey A., Sotta B., Seo M., Okamoto M., Nambara E. & Marion-Poll A. (2006) Functional analysis of Arabidopsis NCED6 and NCED9 genes indicated that ABA synthesized in the endosperm is involved in the induction of seed dormancy. The Plant Journal 45, 309-319.
43. Leszczyszyn O.I., Schmid R. & Blindauer C.A. (2007) Toward a property/function relationship for metallothioneins: histidine coordination and unusual cloister composition in a zinc-metallothionein from plants. Proteins 68, 922-935.
44. Leszczyszyn O.I., White C.R. & Blindauer C.A. (2010) The isolated Cys2His2 site in EC metallothionein mediates metal-specific protein folding. Molecular Biosystems 6, 1592-1603.
45. Ma M., Lau P.S., Jia Y.T., Tsang W.K., Lam S.K.S., Tam N.F.Y. & Wong Y.S. (2003) The isolation and characterization of type 1 metallothionein (MT) cDNA from a heavy-metal-tolerant plant, Festuca rubra cv. Merlin. Plant Science 164, 51-60.
46. Matsumura H., Nirasawa S. & Terauchi R. (1999) Transcript profiling in rice (Oryza sativa L.) seedling using serial analysis of gene expression (SAGE). The Plant Journal 20, 719-726.
47. Mitchum M.G., Yamaguchi S., Hanada A., Kuwahara A., Yoshioka Y., Kato T., Tabata S., Kamiya Y. & Sun T.P. (2006) Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. The Plant Journal 45, 804-818.
48. Moyle R., Fairbairn D.J., Ripi J., Crowe M. & Botella J.R. (2005) Developing pineapple fruit has a small transcriptome dominated by metallothionein. Journal of Experimental Botany 56, 101-112.
49. Murphy A., Zhou J.M., Goldsbrough P.B. & Taiz L. (1997) Purification and immunological identification of metallothioneins 1 and 2 from Arabidopsis thaliana. Plant Physiology 113, 1293-1301.
50. Nambara E. & Marion-Poll A. (2003) ABA action and interactions in seeds. Trends in Plant Science 8, 213-217.
51. Nawy T., Lee J.Y., Colinas J., Wang J.Y., Thongrod S.C., Birnbaum K. & Benfey P.N. (2005) Transcriptional profile of the Arabidopsis root quiescent center. The Plant Cell 17, 1908-1925.
52. Oh E., Yamaguchi S., Kamiya Y., Bae G., Chung W. & Choi G. (2006) Light activates the degradation of PIL5 protein to promote seed germination through gibberellin in Arabidopsis. The Plant Journal 47, 124-139.
53. Okamoto M., Kuwahara A., Seo M., Kushiro T., Asami T., Hirai N., Kamiya Y., Koshiba T. & Nambara E. (2006) CYP707A1 and CYP707A2, which encode abscisic acid 8'-hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiology 141, 97-107.
54. Öz G., Pountney D.L. & Armitage I.M. (1998) NMR spectroscopic studies of I =1/2 metal ions in biological systems. Biochemistry and Cell Biology 76, 223-234.
55. C-1 metallothionein: evidence supporting two separate metal thiolate clusters. Journal of Biological Inorganic Chemistry 12, 377-391.
56. Puig S. & Peñarrubia L. (2009) Placing metal micronutrients in context: transport and distribution in plants. Current Opinion in Plant Biology 12, 299-306.
57. Ren Y.J. & Zhao J. (2009) Functional analysis of the rice metallothionein gene OsMT2b promoter in transgenic Arabidopsis plants and rice germinated embryos. Plant Science 176, 528-538.
58. Reynolds T.L. & Crawford R.L. (1996) Changes in abundance of an abscisic acid-responsive, early cystein-labeled metallothionein transcript during pollen embryogenesis in bread wheat (Triticum aestivum). Plant Molecular Biology 32, 823-829.
59. Richard O., Pineau C., Loubet S., Chalies C., Vile D., Marques L. & Berthomieu P. (2011) Arabidopsis thaliana species revealed a low contribution of Zn translocation to Zn tolerance and a new role for Zn in lateral root development. Plant, Cell & Environment 34, 1065-1078.
60. Rock C.D. & Zeevaart J.A. (1991) The ABA mutant of Arabidopsis thaliana is impaired in epoxy-carotenoid biosynthesis. Proceedings of the National Academy of Sciences of the United States of America 88, 7496-7499.
61. Roosens N.H., Bernard C., Leplae R. & Verbruggen N. (2004) Evidence for copper homeostasis function of metallothionein (MT3) in the hyperaccumulator Thlaspi caerulescens. FEBS Letters 577, 9-16.
62. Saiga S., Furumizu C., Yokoyama R., Kurata T., Sato S., Kato T., Tabata S., Suzuki M. & Komeda Y. (2008) The Arabidopsis OBERON1 and OBERON2 genes encode plant homeodomain finger proteins and are required for apical meristem maintenance. Development 135, 1751-1759.
63. Sakamoto W., Zaltsman A., Adam Z. & Takahashi Y. (2003) Coordinated regulation and complex formation of yellow variegated1 and yellow variegated2, chloroplastic FtsH metalloproteases involved in the repair cycle of photosystem II in Arabidopsis thylakoid membranes. The Plant Cell 15, 2843-2855.
64. Santos-Mendoza M., Dubreucq B., Baud S., Parcy F., Caboche M. & Lepiniec L. (2008) Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. The Plant Journal 54, 608-620.
65. Seo M. & Koshiba T. (2002) Complex regulation of ABA biosynthesis in plants. Trends in Plant Science 7, 41-48.
66. Seo M., Koiwai H., Akaba S., Komano T., Oritani T., Kamiya Y. & Koshiba T. (2000a) Abscisic aldehyde oxidase in leaves of Arabidopsis thaliana. The Plant Journal 23, 481-488.
67. Seo M., Peeters A.J., Koiwai H., Oritani T., Marion-Poll A., Zeevaart J.A., Koornneef M., Kamiya Y. & Koshiba T. (2000b) The Arabidopsis aldehyde oxidase 3 (AAO3) gene product catalyzes the final step in abscisic acid biosynthesis in leaves. Proceedings of the National Academy of Sciences of the United States of America 97, 12908-12913.
68. Seo M., Aoki H., Koiwai H., Kamiya Y., Nambara E. & Koshiba T. (2004) Comparative studies on the Arabidopsis aldehyde oxidase (AAO) gene family revealed a major role of AAO3 in ABA biosynthesis in seeds. Plant and Cell Physiology 45, 1694-1703.
69. Seo M., Hanada A., Kuwahara A., etal. (2006) Regulation of hormone metabolism in Arabidopsis seeds: phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. The Plant Journal 48, 354-366.
70. Tanz S.K., Tetu S.G., Vella N.G. & Ludwig M. (2009) Loss of the transit peptide and an increase in gene expression of an ancestral chloroplastic carbonic anhydrase were instrumental in the evolution of the cytosolic C4 cabonic anhydrase in flaveria. Plant Physiology 150, 1515-1529.
71. Thomas J.C., Perron M., Larose P.C. & Smigocki A.C. (2005) Cytokinin and the regulation of a tobacco metallothionein-like gene during copper stress. Physiologia Plantarum 123, 262-271.
72. Vilaine F., Palauqui J.C., Amselem J., Kusiak C., Lemoine R. & Dinant S. (2003) Toward deciphering phloem: a transcriptome analysis of the phloem of Apium graveolens. The Plant Journal 36, 67-81.
73. 35 homologs in plants. Plant Physiology 140, 624-636.
74. White C.N. & Rivin C.J. (1995) Characterization and expression of a cDNA encoding a seed-specific metallothionein in maize. Plant Physiology 108, 831-832.
75. White J., Pacey-Miller T., Crawford A., Cordeiro G., Barbary D., Bundock P. & Henry R. (2006) Abundant transcripts of malting barley identified by serial analysis of gene expression (SAGE). Plant Biotechnology Journal 4, 289-301.
76. Wobus U. & Webber H. (1999) Seed maturation: genetic programmes and control signals. Current Opinion in Plant Biology 2, 33-38.
77. Wong H.L., Sakamoto T., Kawasaki T., Umemura K. & Shimamoto K. (2004) Down-regulation of metallothionein, a reactive oxygen scavenger, by the small GTPase OsRac1 in rice. Plant Physiology 135, 1447-1456.
78. Xue T.T., Li X.Z., Zhu W., Wu C.G., Yang G.D. & Zheng C.C. (2009) Cotton metallothionein GhMT3a, a reactive oxygen species scavenger, increased tolerance against abiotic stress in transgenic tobacco and yeast. Journal of Experimental Botany 60, 339-349.
79. Yamaguchi S., Smith M.W., Brown R.G.S., Kamiya Y. & Sun T.P. (1998) Phytochrome regulation and differential expression of gibberellin 3β-hydroxylase genes in germinating Arabidopsis seeds. The Plant Cell 10, 2115-2126.
80. Yamauchi Y., Takeda-Kamiya N., Hanada A., Ogawa M., Kuwahara A., Seo M., Kamiya Y. & Yamaguchi S. (2007) Contribution of gibberellin deactivation by AtGA2ox2 to the suppression of germination of dark-imbibed Arabidopsis thaliana seeds. Plant and Cell Physiology 48, 555-561.
81. Yang Z., Wu Y.R., Li Y., Ling H.Q. & Chu C.C. (2009) OsMT1a, a type 1 metallothionein, plays the pivotal role in zinc homeostasis and drought tolerance in rice. Plant Molecular Biology 70, 219-229.
82. Yuan J., Chen D., Ren Y.J., Zhang X.L. & Zhao J. (2008) Characteristic and expression analysis of a metallothionein gene, OsMT2b, down-regulated by cytokinin suggest functions in root development and seed embryo germination of rice (Oryza sativa L.). Plant Physiology 146, 1637-1650.
83. Zhang X.L., Ren Y.J. & Zhao J. (2008) Roles of extensins in cotyledon primordium formation and shoot apical meristem activity in Nicotiana tabacum. Journal of Experimental Botany 59, 4045-4058.
84. Zhou G.K., Xu Y.F., Li J., Yang L.Y. & Liu J.Y. (2006) Molecular analyses of the metallothionein gene family in rice (Oryza sativa L.). Journal of Biochemistry and Molecular Biology 39, 595-606.
85. Zhou J.M. & Goldsbrough P.B. (1995) Structure, organization and expression of the metallothionein gene family in Arabidopsis. Molecular and General Genetics 248, 318-328.