Nicotianamine synthase gene family as central components in heavy metal and phytohormone response in maize

Functional and Integrative Genomics

Volumn 13, Issue 2, 2013, Pages 229-239

  Zhou, Mei Liang ^a,b   Qi, Lei Peng ^a   Pang, Jun Feng ^b   Zhang, Qian ^a   Lei, Zhi ^b   Tang, Yi Xiong ^b   Zhu, Xue Mei ^a   Shao, Ji Rong ^a   Wu, Yan Min ^b  

^a SICHUAN AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Biofortification; CuRE; Heavy metals; Nicotianamine synthase; Salicylic acid

Indexed keywords

ABSCISIC ACID; HEAVY METAL; JASMONIC ACID; PHYTOHORMONE; SALICYLIC ACID;

ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ENVIRONMENTAL STRESS; GENE EXPRESSION; GENE IDENTIFICATION; GENE MAPPING; GENETIC ANALYSIS; HORMONE RESPONSE; MAIZE; MOLECULAR PHYLOGENY; NICOTIANAMINE SYNTHASE 1 GENE; NICOTIANAMINE SYNTHASE 10 GENE; NICOTIANAMINE SYNTHASE 2 GENE; NICOTIANAMINE SYNTHASE 3 GENE; NICOTIANAMINE SYNTHASE 4 GENE; NICOTIANAMINE SYNTHASE 5 GENE; NICOTIANAMINE SYNTHASE 6 GENE; NICOTIANAMINE SYNTHASE 7 GENE; NICOTIANAMINE SYNTHASE 8 GENE; NICOTIANAMINE SYNTHASE 9 GENE; NICOTIANAMINE SYNTHASE GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT DEVELOPMENT; PLANT GENE; PLANT GENOME; PLANT LEAF; PRIORITY JOURNAL; PROTOPLAST; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RICE; STRUCTURE ANALYSIS;

ALKYL AND ARYL TRANSFERASES; BIOCATALYSIS; CYTOPLASM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; METALS, HEAVY; MODELS, MOLECULAR; MULTIGENE FAMILY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN SPECIFICITY; PHYLOGENY; PLANT GROWTH REGULATORS; PROMOTER REGIONS, GENETIC; PROTEIN TRANSPORT; S-ADENOSYLMETHIONINE; STRESS, PHYSIOLOGICAL; STRUCTURAL HOMOLOGY, PROTEIN; ZEA MAYS;

ARABIDOPSIS; ZEA MAYS;

EID: 84878755053     PISSN: 1438793X     EISSN: 14387948     Source Type: Journal    
DOI: 10.1007/s10142-013-0315-6     Document Type: Article

References (52)

1. Benedetti CE, Xie D, Turner JG (1995) COI1-dependent expression of an Arabidopsis vegetative storage protein in flowers and siliques and in response to coronatine or methyl jasmonate. Plant Physiol 109:567-572
2. Boter M, Ruiz-Rivero O, Abdeen A, Prat S (2004) Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Genes Dev 18:1577-1591
3. Brown RL, Kazan K, McGrath KC, Maclean DJ, Manners JM (2003) A role for the GCC-box in jasmonate-mediated activation of the PDF1.2 gene of Arabidopsis. Plant Physiol 132:1020-1032
4. De Vleesschauwer D, Yang Y, Vera Cruz C, Höfte M (2010) Abscisic acid-induced resistance against the brown spot pathogen Cochliobolus miyabeanus in rice involves MAPK-mediated repression of ethylene signaling. Plant Physiol 152:2036-2052
5. Doehlemann G, van der Linde K, Assmann D, Schwammbach D, Hof A, Mohanty A, Jackson D, Kahmann R (2009) Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathog 5:e1000290
6. Douchkov D, Gryczka C, Stephan UW, Hell R, Baumlein H (2005) Ectopic expression of nicotianamine synthase genes results in improved iron accumulation and increased nickel tolerance in transgenic tobacco. Plant Cell Environ 28:365-374
7. Dreyfus C, Lemaire D, Mari S, Pignol D, Arnoux P (2009) Crystallographic snapshots of iterative substrate translocations during nicotianamine synthesis in archaea. Proc Natl Acad Sci USA 22:16180-16184
8. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2:953-971
9. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205-227
10. He P, Shan L, Sheen J (2007) The use of protoplasts to study innate immune responses. Methods Mol Biol 354:1-9
11. Hell R, Stephan UW (2003) Iron uptake, trafficking and homeostasis in plants. Planta 216:541-551
12. Herbik A, Koch G, Mock HP, Dushkov D, Czihal A, Thielmann J, Stephan UW, Bäumlein H (1999) Isolation, characterization, and cDNA cloning of nicotianamine synthase from barley. A key enzyme for iron homeostasis in plants. Eur J Biochem 265:231-239
13. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297-300
14. Higuchi K, Suzuki K, Nakanishi H, Yamaguchi H, Nishizawa NK, Mori S (1999) Cloning of nicotianamine synthase genes, novel genes involved in the biosynthesis of phytosiderophores. Plant Physiol 119:471-480
15. Higuchi K, Tani M, Nakanishi H, Yoshiwara T, Goto F, Nishizawa NK, Mori S (2001) The expression of a barley HvNAS1 nicotianamine synthase gene promoter-gus fusion gene in transgenic tobacco is induced by Fe-deficiency in roots. Biosci Biotechnol Biochem 65:1692-1696
16. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41-66
17. Inoue H, Higuchi K, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2003) Three rice nicotianamine synthase genes, OsNAS1, OsNAS2 and OsNAS3, are expressed in cells involved in long-distance transport of iron and differentially regulated by iron. Plant J 36:366-381
18. Johnson AAT, Kyriacou B, Callahan DL, Carruthers L, Stangoulis J, Lombi E, Tester M (2011) Constitutive overexpression of the OsNAS gene family reveals single-gene strategies for effective iron- and zinc-biofortification of rice endosperm. PLoS One 6(9):e24476
19. Kim S, Takahashi M, Higuchi K, Tsunoda K, Nakanishi H, Yoshimura E, Mori S, Nishizawa NK (2005) Increased nicotianamine biosynthesis confers enhanced tolerance of high levels of metals, in particular nickel, to plants. Plant Cell Physiol 46:1809-1818
20. Kobayashi T, Nakayama Y, Itai RN, Nakanishi H, Yoshihara T, Mori S, Nishizawa NK (2003) Identification of novel cis-acting elements, IDE1 and IDE2, of the barley IDS2 gene promoter conferring iron deficiency-inducible, root-specific expression in heterogeneous tobacco plants. Plant J 36:780-793
21. Kobayashi T, Suzuki M, Inoue H, Itai RN, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2005) Expression of iron-acquisition related genes in iron-deficient rice is co-ordinately induced by partially conserved iron-deficiency-responsive elements. J Exp Bot 56:1305-1316
22. Kropat J, Tottey S, Birkenbihl RP, Depege N, Huijser P, Merchant S (2005) A regulator of nutritional copper signaling in Chlamydomonas is an SBP domain protein that recognizes the GTAC core of copper response element. Proc Natl Acad Sci USA 102:18730-18735
23. Lebel E, Heifetz P, Thorne L, Uknes S, Ryals J, Ward E (1998) Functional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis. Plant J 16:223-233
24. Lee S, Jeon US, Lee SJ, Kim YK, Persson DP, Husted S, Schjørring JK, Kakei Y, Masuda H, Nishizawa NK, An G (2009) Iron fortification of rice seeds through activation of the nicotianamine synthase gene. Proc Natl Acad Sci USA 106:22014-22019
25. Ling HQ, Pich A, Scholz G, Ganal MW (1996) Genetic analysis of two tomato mutants affected in the regulation of iron metabolism. Mol Gen Genet 252:87-92
26. Ling HQ, Koch G, Baumlein H, Ganal MW (1999) Map-based cloning of chloronerva, a gene involved in iron uptake of higher plants encoding nicotianamine synthase. Proc Natl Acad Sci USA 96:7098-7103
27. Lorenzo O, Piqueras R, Sanchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15:165-178
28. Mari S, Gendre D, Pianelli K, Ouerdane L, Lobinski R, Briat JF, Lebrun M, Czernic P (2006) Root-to-shoot long-distance circulation of nicotianamine and nicotianamine-nickel chelates in the metal hyperaccumulator Thlaspi caerulescens. J Exp Bot 57:4111-4122
29. Masuda H, Usuda K, Kobayashi T, Ishimaru Y, Kakei Y, Takahashi M, Higuchi K, Nakanishi H, Mori S, Nishizawa NK (2009) Overexpression of the barley nicotianamine synthase gene HvNAS1 increases iron and zinc concentrations in rice grains. Rice 2:155-166
30. Mizuno D, Higuchi K, Sakamoto T, Nakanishi H, Mori S, Nishizawa NK (2003) Three nicotianamine synthase genes isolated from maize are differentially regulated by iron nutritional status. Plant Physiol 132:1989-1997
31. Nishizawa N, Mori S (1987) The particular vesicle appearing in barley root cells and its relation to mugineic acid secretion. J Plant Nutr 10:1012-1020
32. Pianelli K, Mari S, Marques L, Lebrun M, Czernic P (2005) Nicotianamine overaccumulation confers resistance to nickel in Arabidopsis thaliana. Transgenic Res 14:739-748
33. Quinn JM, Barraco P, Eriksson M, Merchant S (2000) Coordinate copper- and oxygen-responsive Cyc6 and Cpx1 expression in Chlamydomonas is mediated by the same element. J Biol Chem 275:6080-6089
34. Ramesh SA, Choimes S, Schachtman DP (2004) Over-expression of an Arabidopsis zinc transporter in Hordeum vulgare increases short-term zinc uptake after zinc deprivation and seed zinc content. Plant Mol Biol 54:373-385
35. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425
36. Schünmann PH, Richardson AE, Vickers CE, Delhaize E (2004) Promoter analysis of the barley Pht1;1 phosphate transporter gene identifies regions controlling root expression and responsiveness to phosphate deprivation. Plant Physiol 136:4205-4214
37. Sekhon RS, Lin H, Childs KL, Hansey CN, Buell CR, de Leon N, Kaeppler SM (2011) Genome-wide atlas of transcription through maize development. Plant J 66:553-563
38. Sekhon RS, Childs KL, Santoro N, Foster CE, Buell CR, de Leon N, Kaeppler SM (2012) Transcriptional and metabolic analysis of senescence induced by preventing pollination in maize. Plant Physiol 159:1730-1744
39. Sutoh K, Yamauchi D (2003) Two cis-acting elements necessary and sufficient for gibberellin-upregulated proteinase expression in rice seeds. Plant J 34:636-645
40. Takahashi M, Terada Y, Nakai I, Nakanishi H, Yoshimura E, Mori S, Nishizawa NK (2003) Role of nicotianamine in the intracellular delivery of metals and plant reproductive development. Plant Cell 15:1263-1280
41. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. doi: 10.1093/molbev/msr121
42. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876-4882
43. Trampczynska A, Bottcher C, Clemens S (2006) The transition metal chelator nicotianamine is synthesized by filamentous fungi. FEBS Lett 580:3173-3178
44. Usuda K, Wada Y, Ishimaru Y, Kobayashi T, Takahashi M, Nakanishi H, Nagato Y, Mori S, Nishizawa NK (2008) Genetically engineered rice containing larger amounts of nicotianamine to enhance the antihypertensive effect. Plant Biotechnol J 7:87-95
45. Wirth J, Poletti S, Aeschlimann B, Yakandawala N, Drosse B, Osorio S, Tohge T, Fernie AR, Günther D, Gruissem W, Sautter C (2009) Rice endosperm iron biofortification by targeted and synergistic action of nicotianamine synthase and ferritin. Plant Biotechnol J 7:631-644
46. Zheng L, Cheng Z, Ai C, Jiang X, Bei X, Zheng Y, Glahn RP, Welch RM, Miller DD, Lei XG, Shou H (2010) Nicotianamine, a novel enhancer of rice iron bioavailability to humans. PLoS One 5:e10190
47. Zhou ML, Ma JT, Pang JF, Zhang ZL, Tang YX, Wu YM (2010a) Regulation of plant stress response by dehydration responsive element binding (DREB) transcription factors. Afr J Biotechnol 9:9255-9269
48. Zhou ML, Zhu XM, Shao JR, Wu YM, Tang YX (2010b) Transcriptional response of the terpenoid indole alkaloid pathway to the overexpression of ORCA3 along with MeJA/nitric oxide elicitation in Catharanthus roseus hairy root culture. Appl Microbiol Biotechnol 88:737-750
49. Zhou ML, Hou HL, Zhu XM, Shao JR, Wu YM, Tang YX (2011) GmMYBZ2 acts as a repressor of catharanthine biosynthesis pathway in Catharanthus roseus hairy root culture. Appl Microbiol Biotechnol 91:1095-1105
50. Zhou ML, Ma JT, Zhao YM, Wei YH, Tang YX, Wu YM (2012a) Improvement of drought and salt tolerance in Arabidopsis and Lotus corniculatus by overexpression of a novel DREB transcription factor from Populus euphratica. Gene 506:10-17
51. Zhou ML, Zhang Q, Zhou M, Sun ZM, Zhu XM, Shao JR, Tang YX, Wu YM (2012b) Genome-wide identification of genes involved in raffinose metabolism in maize. Glycobiology 22:1775-1785
52. Zuchi S, Cesco S, Varanini Z, Pinton R, Astolfi S (2009) Sulphur deprivation limits Fe-deficiency responses in tomato plants. Planta 230:85-94