Identification of candidate genes involved in early iron deficiency chlorosis signaling in soybean (Glycine max) roots and leaves

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Moran Lauter, Adrienne N ^a   Peiffer, Gregory A ^a   Yin, Tengfei ^b   Whitham, Steven A ^c   Cook, Dianne ^b   Shoemaker, Randy C ^a,c   Graham, Michelle A ^a,c  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b Iowa State University   (United States)

^c IOWA STATE UNIVERSITY   (United States)

Author keywords

Glycine max; Iron deficiency chlorosis; RNA Seq; Soybean

Indexed keywords

IRON; NITRATE; PLANT DNA; PLANT RNA; TRANSCRIPTION FACTOR; PROTEIN BINDING;

ARTICLE; CHLOROSIS; CONTROLLED STUDY; CROP IMPROVEMENT; CULTURE MEDIUM; DNA REPLICATION; GENE EXPRESSION; GENE IDENTIFICATION; HYDROPONICS; IRON DEFICIENCY; IRON TRANSPORT; NONHUMAN; PLANT GENE; PLANT LEAF; PLANT ROOT; RNA SEQUENCE; SIGNAL TRANSDUCTION; SOYBEAN; BINDING SITE; DEFICIENCY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; METABOLISM; MULTIGENE FAMILY; PHYSIOLOGICAL STRESS; PLANT DISEASE; TIME;

GLYCINE MAX;

BINDING SITES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; HOMEOSTASIS; IRON; MULTIGENE FAMILY; PLANT DISEASES; PLANT LEAVES; PLANT ROOTS; PROTEIN BINDING; SIGNAL TRANSDUCTION; SOYBEANS; STRESS, PHYSIOLOGICAL; TIME FACTORS; TRANSCRIPTION FACTORS;

EID: 84906927262     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-702     Document Type: Article

References (143)

1. Hansen NC, Jolley VD, Naeve SL, Goos RJ. Iron deficiency of soybean in the north central US and associated soil properties. Soil Sci Plant Nutr 2004, 50(7):983-987.
2. Aust SD, Morehouse LA, Thomas CE. Role of metals in oxygen radical reactions. J Free Radic Biol Med 1985, 1(1):3-25.
3. Marschner H. Mineral Nutrition of Higher Plants 1995, London; San Diego: Academic Press, 2.
4. Robinson NJ, Procter CM, Connolly EL, Guerinot ML. A ferric-chelate reductase for iron uptake from soils. Nature 1999, 397(6721):694-697.
5. Colangelo EP, Guerinot ML. The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 2004, 16(12):3400-3412.
6. Vert G, Grotz N, Dedaldechamp F, Gaymard F, Guerinot ML, Briat JF, Curie C. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 2002, 14(6):1223-1233.
7. Vert GA, Briat JF, Curie C. Dual regulation of the Arabidopsis high-affinity root iron uptake system by local and long-distance signals. Plant Physiol 2003, 132(2):796-804.
8. Enomoto Y, Goto F. Long-distance signaling of iron deficiency in plants. Plant Signal Behav 2008, 3(6):396-397.
9. Garcia MJ, Suarez V, Romera FJ, Alcantara E, Perez-Vicente R. A new model involving ethylene, nitric oxide and Fe to explain the regulation of Fe-acquisition genes in Strategy I plants. Plant Physiol Biochem 2011, 49(5):537-544.
10. Bernard RL. Genetic stocks available. Soybean Genetic Newsletter 1975, 2:57-74.
11. Atwood SE, O'Rourke JA, Peiffer GA, Yin T, Majumder M, Zhang C, Cianzio SR, Hill JH, Cook D, Whitham SA, Shoemaker RC, Graham MA. Replication protein A subunit 3 and the iron efficiency response in soybean. Plant Cell Environ 2014, 37(1):213-234.
12. O'Rourke JA, Charlson DV, Gonzalez DO, Vodkin LO, Graham MA, Cianzio SR, Grusak MA, Shoemaker RC. Microarray analysis of iron deficiency chlorosis in near-isogenic soybean lines. BMC Genomics 2007, 8:476.
13. O'Rourke JA, Nelson RT, Grant D, Schmutz J, Grimwood J, Cannon S, Vance CP, Graham MA, Shoemaker RC. Integrating microarray analysis and the soybean genome to understand the soybeans iron deficiency response. BMC Genomics 2009, 10:376.
14. Peiffer GA, King KE, Severin AJ, May GD, Cianzio SR, Lin SF, Lauter NC, Shoemaker RC. Identification of candidate genes underlying an iron efficiency quantitative trait locus in soybean. Plant Physiol 2012, 158(4):1745-1754.
15. Wang J, McClean PE, Lee R, Goos RJ, Helms T. Association mapping of iron deficiency chlorosis loci in soybean (Glycine max L. Merr.) advanced breeding lines. Theor Appl Genet 2008, 116(6):777-787.
16. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, et al. Genome sequence of the palaeopolyploid soybean. Nature 2010, 463(7278):178-183.
17. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26(1):139-140.
18. Wickham H. Ggplot2: Elegant Graphics for Data Analysis. Use R! 2009, New York: Series Springer.
19. Cook D, Hofmann H, Lee E, Yan H, Nikolau B, Wurtele E. Exploring gene expression data, using plots. J Data Sci 2007, 5:151-182.
20. Apweiler R, Bairoch A, Wu CH, Barker WC, Boeckmann B, Ferro S, Gasteiger E, Huang H, Lopez R, Magrane M, Martin MJ, Natale DA, O'Donovan C, Redaschi N, Yeh LS. UniProt: the Universal Protein knowledge base. Nucleic Acids Res 2004, 32(Database issue):D115-119.
21. Rietz S, Dermendjiev G, Oppermann E, Tafesse FG, Effendi Y, Holk A, Parker JE, Teige M, Scherer GF. Roles of Arabidopsis patatin-related phospholipases a in root development are related to auxin responses and phosphate deficiency. Mol Plant 2010, 3(3):524-538.
22. Herzog M, Dorne AM, Grellet F. GASA, a gibberellin-regulated gene family from Arabidopsis thaliana related to the tomato GAST1 gene. Plant Mol Biol 1995, 27(4):743-752.
23. Chen LQ, Qu XQ, Hou BH, Sosso D, Osorio S, Fernie AR, Frommer WB. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 2012, 335(6065):207-211.
24. Rea G, Metoui O, Infantino A, Federico R, Angelini R. Copper amine oxidase expression in defense responses to wounding and Ascochyta rabiei invasion. Plant Physiol 2002, 128(3):865-875.
25. Moller SG, Urwin PE, Atkinson HJ, McPherson MJ. Nematode-induced expression of atao1, a gene encoding an extracellular diamine oxidase associated with developing vascular tissue. Physiol Mol Plant Phatol 1998, 53(2):73-79.
26. Zhao MG, Chen L, Zhang LL, Zhang WH. Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol 2009, 151(2):755-767.
27. Shapiro AD. Nitric oxide signaling in plants. Vitam Horm 2005, 72:339-398.
28. Carretero-Paulet L, Ahumada I, Cunillera N, Rodriguez-Concepcion M, Ferrer A, Boronat A, Campos N. Expression and molecular analysis of the Arabidopsis DXR gene encoding 1-deoxy-D-xylulose 5-phosphate reductoisomerase, the first committed enzyme of the 2-C-methyl-D-erythritol 4-phosphate pathway. Plant Physiol 2002, 129(4):1581-1591.
29. Kim MJ, Ciani S, Schachtman DP. A peroxidase contributes to ROS production during Arabidopsis root response to potassium deficiency. Mol Plant 2010, 3(2):420-427.
30. Llorente F, Lopez-Cobollo RM, Catala R, Martinez-Zapater JM, Salinas J. A novel cold-inducible gene from Arabidopsis, RCI3, encodes a peroxidase that constitutes a component for stress tolerance. Plant J 2002, 32(1):13-24.
31. Borges A, Tsai SM, Caldas DG. Validation of reference genes for RT-qPCR normalization in common bean during biotic and abiotic stresses. Plant Cell Rep 2012, 31(5):827-838.
32. Hawkins TJ, Deeks MJ, Wang P, Hussey PJ. The evolution of the actin binding NET superfamily. Front Plant Sci 2014, 5:254.
33. Zhang Z, Barlow JN, Baldwin JE, Schofield CJ. Metal-catalyzed oxidation and mutagenesis studies on the iron(II) binding site of 1-aminocyclopropane-1-carboxylate oxidase. Biochemistry 1997, 36(50):15999-16007.
34. Singh K, Singla-Pareek SL, Pareek A. Dissecting out the crosstalk between salinity and hormones in roots of Arabidopsis. OMICS 2011, 15(12):913-924.
35. Yamaguchi-Shinozaki K, Shinozaki K. The plant hormone abscisic acid mediates the drought-induced expression but not the seed-specific expression of rd22, a gene responsive to dehydration stress in Arabidopsis thaliana. Mol Gen Genet 1993, 238(1-2):17-25.
36. Kumar K, Rao KP, Biswas DK, Sinha AK. Rice WNK1 is regulated by abiotic stress and involved in internal circadian rhythm. Plant Signal Behav 2011, 6(3):316-320.
37. Wang H, Liu D, Sun J, Zhang A. Asparagine synthetase gene TaASN1 from wheat is up-regulated by salt stress, osmotic stress and ABA. J Plant Physiol 2005, 162(1):81-89.
38. Lisso J, Schroder F, Mussig C. EXO modifies sucrose and trehalose responses and connects the extracellular carbon status to growth. Front Plant Sci 2013, 4:219.
39. Goujon T, Sibout R, Pollet B, Maba B, Nussaume L, Bechtold N, Lu F, Ralph J, Mila I, Barriere Y, Lapierre C, Jouanin L. A new Arabidopsis thaliana mutant deficient in the expression of O-methyltransferase impacts lignins and sinapoyl esters. Plant Mol Biol 2003, 51(6):973-989.
40. Kajikawa M, Fujibe T, Uraguchi S, Miwa K, Fujiwara T. Expression of the Arabidopsis borate efflux transporter gene, AtBOR4, in rice affects the xylem loading of boron and tolerance to excess boron. Biosci Biotechnol Biochem 2011, 75(12):2421-2423.
41. Langowski L, Ruzicka K, Naramoto S, Kleine-Vehn J, Friml J. Trafficking to the outer polar domain defines the root-soil interface. Curr Biol 2010, 20(10):904-908.
42. Cooper W, Bouzayen M, Hamilton A, Barry C, Rossall S, Grierson D. Use of transgenic plants to study the role of ethylene and polygalacturonase during infection of tomato fruit by Colletotrichum gloeosporioides. Plant Pathol 1998, 47(3):308-316.
43. Hamilton AJ, Lycett GW, Grierson D. Antisense gene that inhibits synthesis of the hormone ethylene in transgenic plants. Nature 1990, 346(6281):284-287.
44. Henriques R, Jasik J, Klein M, Martinoia E, Feller U, Schell J, Pais MS, Koncz C. Knock-out of Arabidopsis metal transporter gene IRT1 results in iron deficiency accompanied by cell differentiation defects. Plant Mol Biol 2002, 50(4-5):587-597.
45. Severin AJ, Peiffer GA, Xu WW, Hyten DL, Bucciarelli B, O'Rourke JA, Bolon YT, Grant D, Farmer AD, May GD, Vance CP, Shoemaker RC, Stupar RM. An integrative approach to genomic introgression mapping. Plant Physiol 2010, 154(1):3-12.
46. Stec AO, Bhaskar PB, Bolon YT, Nolan R, Shoemaker RC, Vance CP, Stupar RM. Genomic heterogeneity and structural variation in soybean near isogenic lines. Front Plant Sci 2013, 4:104.
47. Lin S, Cianzio S, Shoemaker R. Mapping genetic loci for iron deficiency chlorosis in soybean. Mol Breed 1997, 3(3):219-229.
48. Lin SF, Grant D, Cianzio S, Shoemaker R. Molecular characterization of iron deficiency chlorosis in soybean. J Plant Nutr 2000, 23(11-12):1929-1939.
49. Mamidi S, Chikara S, Goos RJ, Hyten DL, Annam D, Moghaddam SM, Lee RK, Cregan PB, McClean PE. Genome-wide association analysis identifies candidate genes associated with iron deficiency chlorosis in soybean. Plant Genome-Us 2011, 4(3):154-164.
50. Bauer S, Grossmann S, Vingron M, Robinson PN. Ontologizer 2.0--a multifunctional tool for GO term enrichment analysis and data exploration. Bioinformatics 2008, 24(14):1650-1651.
51. Kobayashi T, Nishizawa NK. Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol 2012, 63:131-152.
52. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25(17):3389-3402.
53. Graham MA, Ramirez M, Valdes-Lopez O, Lara M, Tesfaye M, Vance CP, Hernandez G. Identification of candidate phosphorus stress induced genes in Phaseolus vulgaris through clustering analysis across several plant species. Funct Plant Biol 2006, 33(8):789-797.
54. Wang Z, Libault M, Joshi T, Valliyodan B, Nguyen HT, Xu D, Stacey G, Cheng J. SoyDB: a knowledge database of soybean transcription factors. BMC Plant Biol 2010, 10:14.
55. Lee SJ, Kang JY, Park HJ, Kim MD, Bae MS, Choi HI, Kim SY. DREB2C interacts with ABF2, a bZIP protein regulating abscisic acid-responsive gene expression, and its overexpression affects abscisic acid sensitivity. Plant Physiol 2010, 153(2):716-727.
56. Yoon HK, Kim SG, Kim SY, Park CM. Regulation of leaf senescence by NTL9-mediated osmotic stress signaling in Arabidopsis. Mol Cell 2008, 25(3):438-445.
57. Kim JH, Nguyen NH, Jeong CY, Nguyen NT, Hong SW, Lee H. Loss of the R2R3 MYB, AtMyb73, causes hyper-induction of the SOS1 and SOS3 genes in response to high salinity in Arabidopsis. J Plant Physiol 2013, 170(16):1461-1465.
58. Cheng MC, Liao PM, Kuo WW, Lin TP. The arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiol 2013, 162(3):1566-1582.
59. Yang Z, Tian L, Latoszek-Green M, Brown D, Wu K. Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant Mol Biol 2005, 58(4):585-596.
60. Kim MJ, Park MJ, Seo PJ, Song JS, Kim HJ, Park CM. Controlled nuclear import of the transcription factor NTL6 reveals a cytoplasmic role of SnRK2.8 in the drought-stress response. Biochem J 2012, 448(3):353-363.
61. Zhu H, Li GJ, Ding L, Cui X, Berg H, Assmann SM, Xia Y. Arabidopsis extra large G-protein 2 (XLG2) interacts with the Gbeta subunit of heterotrimeric G protein and functions in disease resistance. Mol Plant 2009, 2(3):513-525.
62. Nakata M, Mitsuda N, Herde M, Koo AJ, Moreno JE, Suzuki K, Howe GA, Ohme-Takagi M. A bHLH-type transcription factor, ABA-INDUCIBLE BHLH-TYPE TRANSCRIPTION FACTOR/JA-ASSOCIATED MYC2-LIKE1, acts as a repressor to negatively regulate jasmonate signaling in arabidopsis. Plant Cell 2013, 25(5):1641-1656.
63. Robatzek S, Somssich IE. A new member of the Arabidopsis WRKY transcription factor family, AtWRKY6, is associated with both senescence- and defence-related processes. Plant J 2001, 28(2):123-133.
64. Chen YF, Li LQ, Xu Q, Kong YH, Wang H, Wu WH. The WRKY6 transcription factor modulates PHOSPHATE1 expression in response to low Pi stress in Arabidopsis. Plant Cell 2009, 21(11):3554-3566.
65. Kasajima I, Ide Y, Yokota Hirai M, Fujiwara T. WRKY6 is involved in the response to boron deficiency in Arabidopsis thaliana. Physiol Plant 2010, 139(1):80-92.
66. Frith MC, Fu Y, Yu L, Chen JF, Hansen U, Weng Z. Detection of functional DNA motifs via statistical over-representation. Nucleic Acids Res 2004, 32(4):1372-1381.
67. Wingender E, Dietze P, Karas H, Knuppel R. TRANSFAC: a database on transcription factors and their DNA binding sites. Nucleic Acids Res 1996, 24(1):238-241.
68. Cheong YH, Chang HS, Gupta R, Wang X, Zhu T, Luan S. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 2002, 129(2):661-677.
69. Ghanashyam C, Jain M. Role of auxin-responsive genes in biotic stress responses. Plant Signal Behav 2009, 4(9):846-848.
70. He JX, Gendron JM, Sun Y, Gampala SS, Gendron N, Sun CQ, Wang ZY. BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 2005, 307(5715):1634-1638.
71. Li XP, Tian AG, Luo GZ, Gong ZZ, Zhang JS, Chen SY. Soybean DRE-binding transcription factors that are responsive to abiotic stresses. Theor Appl Genet 2005, 110(8):1355-1362.
72. Shin J, Park E, Choi G. PIF3 regulates anthocyanin biosynthesis in an HY5-dependent manner with both factors directly binding anthocyanin biosynthetic gene promoters in Arabidopsis. Plant J 2007, 49(6):981-994.
73. Solano R, Nieto C, Avila J, Canas L, Diaz I, Paz-Ares J. Dual DNA binding specificity of a petal epidermis-specific MYB transcription factor (MYB.Ph3) from Petunia hybrida. EMBO J 1995, 14(8):1773-1784.
74. Dang HQ, Tran NQ, Tuteja R, Tuteja N. Promoter of a salinity and cold stress-induced MCM6 DNA helicase from pea. Plant Signal Behav 2011, 6(7):1006-1008.
75. Lindermayr C, Sell S, Muller B, Leister D, Durner J. Redox regulation of the NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide. Plant Cell 2010, 22(8):2894-2907.
76. Despres C, Chubak C, Rochon A, Clark R, Bethune T, Desveaux D, Fobert PR. The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. Plant Cell 2003, 15(9):2181-2191.
77. Kobayashi Y, Murata M, Minami H, Yamamoto S, Kagaya Y, Hobo T, Yamamoto A, Hattori T. Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. Plant J 2005, 44(6):939-949.
78. Kang JY, Choi HI, Im MY, Kim SY. Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 2002, 14(2):343-357.
79. Sell S, Hehl R. Functional dissection of a small anaerobically induced bZIP transcription factor from tomato. Eur J Biochem 2004, 271(22):4534-4544.
80. Wei W, Huang J, Hao YJ, Zou HF, Wang HW, Zhao JY, Liu XY, Zhang WK, Ma B, Zhang JS, Chen SY. Soybean GmPHD-type transcription regulators improve stress tolerance in transgenic Arabidopsis plants. PLoS One 2009, 4(9):e7209.
81. Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L. MYB transcription factors in Arabidopsis. Trends Plant Sci 2010, 15(10):573-581.
82. Ding Z, Li S, An X, Liu X, Qin H, Wang D. Transgenic expression of MYB15 confers enhanced sensitivity to abscisic acid and improved drought tolerance in Arabidopsis thaliana. J Genet Genomics 2009, 36(1):17-29.
83. Blanchet E, Annicotte JS, Lagarrigue S, Aguilar V, Clape C, Chavey C, Fritz V, Casas F, Apparailly F, Auwerx J, Fajas L. E2F transcription factor-1 regulates oxidative metabolism. Nat Cell Biol 2011, 13(9):1146-1152.
84. Mariconti L, Pellegrini B, Cantoni R, Stevens R, Bergounioux C, Cella R, Albani D. The E2F family of transcription factors from Arabidopsis thaliana. Novel and conserved components of the retinoblastoma/E2F pathway in plants. J Biol Chem 2002, 277(12):9911-9919.
85. Manavella PA, Dezar CA, Ariel FD, Drincovich MF, Chan RL. The sunflower HD-Zip transcription factor HAHB4 is up-regulated in darkness, reducing the transcription of photosynthesis-related genes. J Exp Bot 2008, 59(11):3143-3155.
86. Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K. DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 2002, 290(3):998-1009.
87. Osnato M, Stile MR, Wang Y, Meynard D, Curiale S, Guiderdoni E, Liu Y, Horner DS, Ouwerkerk PB, Pozzi C, Muller KJ, Salamini F, Rossini L. Cross talk between the KNOX and ethylene pathways is mediated by intron-binding transcription factors in barley. Plant Physiol 2010, 154(4):1616-1632.
88. Kawaoka A, Kaothien P, Yoshida K, Endo S, Yamada K, Ebinuma H. Functional analysis of tobacco LIM protein Ntlim1 involved in lignin biosynthesis. Plant J 2000, 22(4):289-301.
89. Yang S, Sweetman JP, Amirsadeghi S, Barghchi M, Huttly AK, Chung WI, Twell D. Novel anther-specific myb genes from tobacco as putative regulators of phenylalanine ammonia-lyase expression. Plant Physiol 2001, 126(4):1738-1753.
90. Dixon RA, Paiva NL. Stress-induced phenylpropanoid metabolism. Plant Cell 1995, 7(7):1085-1097.
91. Faria JA, Reis PA, Reis MT, Rosado GL, Pinheiro GL, Mendes GC, Fontes EP. The NAC domain-containing protein, GmNAC6, is a downstream component of the ER stress- and osmotic stress-induced NRP-mediated cell-death signaling pathway. BMC Plant Biol 2011, 11:129.
92. Mukherjee K, Choudhury AR, Gupta B, Gupta S, Sengupta DN. An ABRE-binding factor, OSBZ8, is highly expressed in salt tolerant cultivars than in salt sensitive cultivars of indica rice. BMC Plant Biol 2006, 6:18.
93. Grotewold E, Athma P, Peterson T. Alternatively spliced products of the maize P gene encode proteins with homology to the DNA-binding domain of myb-like transcription factors. Proc Natl Acad Sci U S A 1991, 88(11):4587-4591.
94. Styles ED, Ceska O. Genetic-control of flavonoid synthesis in Maize. Can J Genet Cytol 1977, 19(2):289-302.
95. Woo HR, Kim JH, Kim J, Lee U, Song IJ, Lee HY, Nam HG, Lim PO. The RAV1 transcription factor positively regulates leaf senescence in Arabidopsis. J Exp Bot 2010, 61(14):3947-3957.
96. Le DT, Nishiyama R, Watanabe Y, Mochida K, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS. Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress. DNA Res 2011, 18(4):263-276.
97. Reddy AS, Ali GS, Celesnik H, Day IS. Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 2011, 23(6):2010-2032.
98. Fan W, Dong X. In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis. Plant Cell 2002, 14(6):1377-1389.
99. Journot-Catalino N, Somssich IE, Roby D, Kroj T. The transcription factors WRKY11 and WRKY17 act as negative regulators of basal resistance in Arabidopsis thaliana. Plant Cell 2006, 18(11):3289-3302.
100. Stein RJ, Waters BM. Use of natural variation reveals core genes in the transcriptome of iron-deficient Arabidopsis thaliana roots. J Exp Bot 2012, 63(2):1039-1055.
101. Waters BM, McInturf SA, Stein RJ. Rosette iron deficiency transcript and microRNA profiling reveals links between copper and iron homeostasis in Arabidopsis thaliana. J Exp Bot 2012, 63(16):5903-5918.
102. Buckhout TJ, Yang TJ, Schmidt W. Early iron-deficiency-induced transcriptional changes in Arabidopsis roots as revealed by microarray analyses. BMC Genomics 2009, 10:147.
103. Yang TJ, Lin WD, Schmidt W. Transcriptional profiling of the Arabidopsis iron deficiency response reveals conserved transition metal homeostasis networks. Plant Physiol 2010, 152(4):2130-2141.
104. Hermans C, Vuylsteke M, Coppens F, Craciun A, Inze D, Verbruggen N. Early transcriptomic changes induced by magnesium deficiency in Arabidopsis thaliana reveal the alteration of circadian clock gene expression in roots and the triggering of abscisic acid-responsive genes. New Phytol 2010, 187(1):119-131.
105. Kim SA, Punshon T, Lanzirotti A, Li L, Alonso JM, Ecker JR, Kaplan J, Guerinot ML. Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 2006, 314(5803):1295-1298.
106. Rodriguez-Celma J, Pan IC, Li W, Lan P, Buckhout TJ, Schmidt W. The transcriptional response of Arabidopsis leaves to Fe deficiency. Front Plant Sci 2013, 4:276.
107. Waters BM, Chu HH, Didonato RJ, Roberts LA, Eisley RB, Lahner B, Salt DE, Walker EL. Mutations in Arabidopsis yellow stripe-like1 and yellow stripe-like3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds. Plant Physiol 2006, 141(4):1446-1458.
108. DiDonato RJ, Roberts LA, Sanderson T, Eisley RB, Walker EL. Arabidopsis Yellow Stripe-Like2 (YSL2): a metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes. Plant J 2004, 39(3):403-414.
109. Long TA, Tsukagoshi H, Busch W, Lahner B, Salt DE, Benfey PN. The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. Plant Cell 2010, 22(7):2219-2236.
110. Roppolo D, De Rybel B, Tendon VD, Pfister A, Alassimone J, Vermeer JE, Yamazaki M, Stierhof YD, Beeckman T, Geldner N. A novel protein family mediates Casparian strip formation in the endodermis. Nature 2011, 473(7347):380-383.
111. Hosmani PS, Kamiya T, Danku J, Naseer S, Geldner N, Guerinot ML, Salt DE. Dirigent domain-containing protein is part of the machinery required for formation of the lignin-based Casparian strip in the root. PNAS 2013, 110(35):14498-14503.
112. Lee Y, Rubio MC, Alassimone J, Geldner N. A mechanism for localized lignin deposition in the endodermis. Cell 2013, 153(2):402-412.
113. Roschzttardtz H, Conejero G, Divol F, Alcon C, Verdeil JL, Curie C, Mari S. New insights into Fe localization in plant tissues. Front Plant Sci 2013, 4:350.
114. Schmid NB, Giehl RF, Doll S, Mock HP, Strehmel N, Scheel D, Kong X, Hider RC, von Wiren N. Feruloyl-CoA 6'-Hydroxylase1-dependent coumarins mediate iron acquisition from alkaline substrates in Arabidopsis. Plant Physiol 2014, 164(1):160-172.
115. Rodriguez-Celma J, Lin WD, Fu GM, Abadia J, Lopez-Millan AF, Schmidt W. Mutually exclusive alterations in secondary metabolism are critical for the uptake of insoluble iron compounds by Arabidopsis and Medicago truncatula. Plant Physiol 2013, 162(3):1473-1485.
116. Fourcroy P, Siso-Terraza P, Sudre D, Saviron M, Reyt G, Gaymard F, Abadia A, Abadia J, Alvarez-Fernandez A, Briat JF. Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency. New Phytol 2014, 201(1):155-167.
117. Garcia MJ, Lucena C, Romera FJ, Alcantara E, Perez-Vicente R. Ethylene and nitric oxide involvement in the up-regulation of key genes related to iron acquisition and homeostasis in Arabidopsis. J Exp Bot 2010, 61(14):3885-3899.
118. Lin Z, Zhong S, Grierson D. Recent advances in ethylene research. J Exp Bot 2009, 60(12):3311-3336.
119. Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 1993, 72(3):427-441.
120. Penninckx IA, Eggermont K, Terras FR, Thomma BP, De Samblanx GW, Buchala A, Metraux JP, Manners JM, Broekaert WF. Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell 1996, 8(12):2309-2323.
121. Cooper CE. Nitric oxide and iron proteins. Biochim Biophys Acta 1999, 1411(2-3):290-309.
122. Hey SJ, Byrne E, Halford NG. The interface between metabolic and stress signalling. Ann Bot 2010, 105(2):197-203.
123. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 2008, 30(2):214-226.
124. Henriques R, Magyar Z, Monardes A, Khan S, Zalejski C, Orellana J, Szabados L, de la Torre C, Koncz C, Bogre L. Arabidopsis S6 kinase mutants display chromosome instability and altered RBR1-E2F pathway activity. EMBO J 2010, 29(17):2979-2993.
125. Schroder F, Lisso J, Lange P, Mussig C. The extracellular EXO protein mediates cell expansion in Arabidopsis leaves. BMC Plant Biol 2009, 9:20.
126. Schroder F, Lisso J, Mussig C. EXORDIUM-LIKE1 promotes growth during low carbon availability in Arabidopsis. Plant Physiol 2011, 156(3):1620-1630.
127. Schroder F, Lisso J, Mussig C. Expression pattern and putative function of EXL1 and homologous genes in Arabidopsis. Plant Signal Behav 2012, 7(1):22-27.
128. Xiong Y, McCormack M, Li L, Hall Q, Xiang C, Sheen J. Glucose-TOR signalling reprograms the transcriptome and activates meristems. Nature 2013, 496(7444):181-186.
129. Froehlich DM, Fehr WR. Agronomic performance of soybeans with differing levels of iron-deficiency chlorosis on calcareous soil. Crop Sci 1981, 21(3):438-441.
130. Helms TC, Scott RA, Schapaugh WT, Goos RJ, Franzen DW, Schlegel AJ. Soybean iron-deficiency chlorosis tolerance and yield decrease on calcareous soils. Agron J 2010, 102(2):492-498.
131. Chaney RLCBA, Bell PF, Angle JS. Detailed method to screen dicot cultivars for resistance to Fe-chlorosis using FeDTPA and biocarbonate in nutrient solutions. J Plant Nutr 1992, 15:2063-2083.
132. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25(9):1105-1111.
133. Li HHB, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup The Sequence alignment/map (SAM) format and SAMtools. Bioinformatics 2009, 25:2078-2079. 1000 Genome Project Data Processing Subgroup.
134. Morgan M, Pages H. Rsamtools: Binary alignment (BAM), variant call (BCF), or tabix file import. R package 2010, version 1(4.3).
135. Lawrence M, Gentleman R, Carey V. rtracklayer: an R package for interfacing with genome browsers. Bioinformatics 2009, 25(14):1841-1842.
136. Lawrence M, Huber W, Pages H, Aboyoun P, Carlson M, Gentleman R, Morgan MT, Carey VJ. Software for computing and annotating genomic ranges. PLoS Comput Biol 2013, 9(8):e1003118.
137. Robinson MD, Smyth GK. Moderated statistical tests for assessing differences in tag abundance. Bioinformatics 2007, 23(21):2881-2887.
138. Robinson MD, Smyth GK. Small-sample estimation of negative binomial dispersion, with applications to SAGE data. Biostatistics 2008, 9(2):321-332.
139. McCarthy DJ, Chen Y, Smyth GK. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res 2012, 40(10):4288-4297.
140. Berardini TZ, Mundodi S, Reiser L, Huala E, Garcia-Hernandez M, Zhang P, Mueller LA, Yoon J, Doyle A, Lander G, Moseyko N, Yoo D, Xu I, Zoeckler B, Montoya M, Miller N, Weems D, Rhee SY. Functional annotation of the Arabidopsis genome using controlled vocabularies. Plant Physiol 2004, 135(2):745-755.
141. Grossmann S, Bauer S, Robinson PN, Vingron M. Improved detection of overrepresentation of Gene-Ontology annotations with parent child analysis. Bioinformatics 2007, 23(22):3024-3031.
142. Fisher RA. The Design of Experiments 1966, Edinburgh: London: Oliver & Boyd, 8.
143. Bonferroni CE. Ill Calcolo delle assicurazioni su gruppi di teste. Studi in Onore del Professore Salvatore Ortu Carboni 1935, 13-60.