Characterizing short and long term iron stress responses in iron deficiency tolerant and susceptible soybean (Glycine max L. Merr.)

2020 United States Department Agriculture (USDA) Foreign Agricultural Service (FAO) Commodities: Soybeans. https://www.fas.usda.gov/commodities/soybeans. Froechlich, 1981, Agronomic performance of soybeans with differing levels of iron deficiency chlorosis on calcareous soil, Crop Sci, 438, 10.2135/cropsci1981.0011183X002100030021x Hansen, 2003, Iron deficiency of soybean in the upper Midwest and associated soil properties, Agron. J., 95, 1595, 10.2134/agronj2003.1595 Bloom, 2011, Soil nitrate is a causative factor in iron deficiency chlorosis in soybeans, Soil Sci. Soc. Am. J., 75, 2233, 10.2136/sssaj2010.0391 Inskeep, 1986, Effects of soil moisture on soil pCO2, soil solution bicarbonate, and iron chlorosis in soybeans, Soil Sci. Soc. Am. J., 50, 946, 10.2136/sssaj1986.03615995005000040024x Hansen, 2004, Iron deficiency of soybean in the North Central US and associated soil properties, Soil Sci. Plant Nutr., 50, 983, 10.1080/00380768.2004.10408564 García, 2011, A new model involving ethylene, nitric oxide and Fe to explain the regulation of Fe-acquisition genes in Strategy I plants, Plant Physiol. Biochem., 49, 537, 10.1016/j.plaphy.2011.01.019 Liu, 2016, Roles of chemical signals in regulation of the adaptive responses to iron deficiency, Plant Signal Behav, 11, 10.1080/15592324.2016.1179418 Wild, 2016, Tissue-specific regulation of gibberellin signaling fine-tunes Arabidopsis iron-deficiency responses, Dev. Cell, 37, 190, 10.1016/j.devcel.2016.03.022 Shen, 2016, Involvement of endogenous salicylic acid in iron-deficiency responses in Arabidopsis, J. Exp. Bot., 67, 4179, 10.1093/jxb/erw196 Gayomba, 2015, Local and systemic signaling of iron status and its interactions with homeostasis of other essential elements, Front. Plant Sci., 6, 716, 10.3389/fpls.2015.00716 Pii, 2016, Modulation of Fe acquisition process by Azospirillum brasilense in cucumber plants, Environ. Exp. Bot., 130, 216, 10.1016/j.envexpbot.2016.06.011 Zanin, 2019, Humic substances contribute to plant iron nutrition acting as chelators and biostimulants. Front, Plant Sci, 10 Hirayama, 2018, The putative peptide gene FEP1 regulates iron deficiency response in Arabidopsis, Plant Cell Physiol, 59, 1739, 10.1093/pcp/pcy145 Xiong, 2013, Molecular evidence for phytosiderophore-induced improvement of iron nutrition of peanut intercropped with maize in calcareous soil, Plant Cell Environ, 36, 1888, 10.1111/pce.12097 Astolfi, 2020, Single and combined Fe and S deficiency differentially modulate root exudate composition in tomato: a double strategy for Fe acquisition?, Inter. J. Mol. Sci., 21, 4038, 10.3390/ijms21114038 Assefa, 2020, Deconstructing the genetic architecture of iron deficiency chlorosis in soybean using genome-wide approaches, BMC Plant Biol, 20, 42, 10.1186/s12870-020-2237-5 Atwood, 2014, Replication protein A subunit 3 and the iron efficiency response in soybean, Plant Cell Environ, 37, 213, 10.1111/pce.12147 Moran Lauter, 2014, Identification of candidate genes involved in early iron deficiency chlorosis signaling in soybean (Glycine max) roots and leaves, BMC Genomics, 15, 702, 10.1186/1471-2164-15-702 Moran Lauter, 2020, Examining short-term responses to a long-term problem: RNA-seq analyses of iron deficiency chlorosis tolerant soybean, Int. J. Mol. Sci., 21, 3591, 10.3390/ijms21103591 Stein, 2012, Use of natural variation reveals core genes in the transcriptome of iron-deficient Arabidopsis thaliana roots, J. Exp. Bot., 63, 1039, 10.1093/jxb/err343 O'Rourke, 2020, Dynamic gene expression changes in response to micronutrient, macronutrient, and multiple stress exposures in soybean, Funct. Integr. Genom., 20, 321, 10.1007/s10142-019-00709-9 O'Rourke, 2007, Microarray analysis of iron deficiency chlorosis in near-isogenic soybean lines, BMC Genom., 8, 476, 10.1186/1471-2164-8-476 O'Rourke, 2007, Recovering from iron deficiency chlorosis in near-isogenic soybeans: a microarray study, Plant Physiol. Biochem., 45, 287, 10.1016/j.plaphy.2007.03.008 O'Rourke, 2009, Integrating microarray analysis and the soybean genome to understand the soybeans iron deficiency response, BMC Genomics, 10, 376, 10.1186/1471-2164-10-376 Bernard, 1975, Genetic stocks available, Soybean Genet. Newsletter, 2, 57 Chaney, 1992, Detailed method to screen dicot cultivars for resistance to Fe-chlorosis using FeDTPA and biocarbonate in nutrient solutions, J. Plant Nutr., 15, 15 Peiffer, 2012, Identification of candidate genes underlying an iron efficiency quantitative trait locus in soybean, Plant Physiol., 158, 1745, 10.1104/pp.111.189860 Lin, 2000, Nutrient solution screening of Fe chlorosis resistance in soybean evaluated by molecular characterization, J. Plant Nutri., 23, 1915, 10.1080/01904160009382153 Andrews, S. FastQC: A quality control tool for high throughput sequence data. https://www.bioinformatics.babraham.ac.uk/projects/fastqc/. The FASTX-Toolkit. FASTQ/A short-reads pre-processing tools. http://hannonlab.cshl.edu/fastx_toolkit/. Version 0.0.13. Sickle- a windowed adaptive trimming tool for FASTQ files using quality. https://github.com/najoshi/sickle. Version 1.33. Trapnell, 2009, TopHat: discovering splice junctions with RNA-Seq, Bioinformatics, 25, 1105, 10.1093/bioinformatics/btp120 Schmutz, 2010, Genome sequence of the palaeopolyploid soybean, Nature, 463, 178, 10.1038/nature08670 Li, 2009, The sequence alignment /map format and SAMtools, Bioinformatics, 25, 2078, 10.1093/bioinformatics/btp352 2018 Morgan, 2010 Lawrence, 2009, Rtracklayer: an R package for interfacing with genome browsers, Bioinformatics, 25, 1841, 10.1093/bioinformatics/btp328 Lawrence, 2013, Software for computing and annotating genomic ranges, PLoS Comput. Biol., 10.1371/journal.pcbi.1003118 Wickham, 2009 Robinson, 2010, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, 26, 139, 10.1093/bioinformatics/btp616 Everaert, 2017, Benchmarking of RNA-sequencing analysis workflows using whole-transcriptome RT-qPCR expression data, Sci. Rep., 7, 1, 10.1038/s41598-017-01617-3 The SoyBase genome annotation report page. http://soybase.org/genomeannotation.index.php. Version Wm82.a2.v2. Apweiler, 2004, UniProt: the universal protein knowledgebase, Nucleic Acids Res, 32, D115, 10.1093/nar/gkh131 The Arabidopsis Information Resource version 10. http://arabidopsis.org. Altschul, 1997, Gapped BLAST and PSI-BLAST: a new generation of protein database search programs, Nucleic Acids Res, 25, 3389, 10.1093/nar/25.17.3389 Berardini, 2004, Functional annotation of the Arabidopsis genome using controlled vocabularies, Plant Physiol, 135, 745, 10.1104/pp.104.040071 Fisher, 1966, 248 Bonferroni, 1935, Calcolo delle assicurazioni su gruppi di teste, Studi in Onore del Professore Salvatore Ortu Carboni, 47 Wang, 2010, SoyDB: a knowledge database of soybean transcription factors, BMCPlant Biol, 10, 14 Frith, 2004, Detection of functional DNA motifs via statistical over-representation, Nucleic Acids Res, 32, 1372, 10.1093/nar/gkh299 Mathelier, 2015, JASPAR 2016: a major expansion and update of the open-access database of transcription factor binding profiles, Nucleic Acids Res, 44, D110, 10.1093/nar/gkv1176 Lin, 1998, Field and nutrient solution tests measure similar mechanisms controlling iron deficiency chlorosis in soybean, Crop Sci, 38, 254, 10.2135/cropsci1998.0011183X003800010043x Vasconcelos, 2014, Morpho-physiological parameters affecting iron deficiency chlorosis in soybean (Glycine max L.), Plant Soil, 374, 161, 10.1007/s11104-013-1842-6 Liu, 2010, Histone methylation in higher plants, Annu. Rev. Plant Biol., 395, 10.1146/annurev.arplant.043008.091939 Lachner, 2001, Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins, Nature, 410, 116, 10.1038/35065132 Xie, 2010, Role of the stomatal development regulators FLP/MYB88 in abiotic stress responses, Plant J, 64, 731, 10.1111/j.1365-313X.2010.04364.x Pillitteri, 2007, Breaking the silence: three bHLH proteins direct cell-fate decisions during stomatal development, Bioessays, 29, 861, 10.1002/bies.20625 Ohashi-Ito, 2006, Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development, Plant Cell, 18, 2493, 10.1105/tpc.106.046136 Guo, 2009, Dof5. 6/HCA2, a Dof transcription factor gene, regulates interfascicular cambium formation and vascular tissue development in Arabidopsis, Plant Cell, 21, 3518, 10.1105/tpc.108.064139 Uberti-Manassero, 2012, The class I protein AtTCP15 modulates plant development through a pathway that overlaps with the one affected by CIN-like TCP proteins, J. Exp. Botany, 63, 809, 10.1093/jxb/err305 Li, 2005, Arabidopsis TCP20 links regulation of growth and cell division control pathways, Proc. Natl. Acad. Sci. U. S. A., 102, 12978, 10.1073/pnas.0504039102 Wang, 2007, Iron deficiency-mediated stress regulation of four subgroup Ib BHLH genes in Arabidopsis thaliana, Planta, 226, 897, 10.1007/s00425-007-0535-x Lorenzo, 2004, Jasmonate-insensitive1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis, Plant Cell, 16, 1938, 10.1105/tpc.022319 Persak, 2014, Dominant repression by Arabidopsis transcription factor MYB44 causes oxidative damage and hypersensitivity to abiotic stress, Int. J. Mol. Sci., 15, 2517, 10.3390/ijms15022517 Ülker, 2007, The WRKY70 transcription factor of Arabidopsis influences both the plant senescence and defense signaling pathways, Planta, 226, 125, 10.1007/s00425-006-0474-y Liu, 2013, Overexpression of Arachis hypogaeaNAC3 in tobacco enhances dehydration and drought tolerance by increasing superoxide scavenging, Plant Physiol. Biochem., 70, 354, 10.1016/j.plaphy.2013.05.018 Kasajima, 2010, WRKY6 is involved in the response to boron deficiency in Arabidopsis thaliana, Physiol. Plant., 139, 80, 10.1111/j.1399-3054.2010.01349.x Peng, 2012, Constitutive expression of rice WRKY30 gene increases the endogenous jasmonic acid accumulation, PR gene expression and resistance to fungal pathogens in rice, Planta, 236, 1485, 10.1007/s00425-012-1698-7 Gao, 2011, Low oleic acid-derived repression of jasmonic acid-inducible defense responses requires the WRKY50 and WRKY51 proteins, Plant Physiol, 155, 464, 10.1104/pp.110.166876 Fernández-Calvo, 2011, The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses, Plant Cell, 23, 701, 10.1105/tpc.110.080788 Zhao, 2011, The Arabidopsis Myb genes MYR1 and MYR2 are redundant negative regulators of flowering time under decreased light intensity, Plant J, 66, 502, 10.1111/j.1365-313X.2011.04508.x Oh, 2011, A dual role for MYB60 in stomatal regulation and root growth of Arabidopsis thaliana under drought stress, Plant Mol. Biol., 77, 91, 10.1007/s11103-011-9796-7 Mittler, 2006, Gain-and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress, FEBS Lett., 580, 6537, 10.1016/j.febslet.2006.11.002 Long, 2010, The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots, Plant Cell, 22, 2219, 10.1105/tpc.110.074096 Yin, 2005, A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis, Cell, 120, 249, 10.1016/j.cell.2004.11.044 Koyama, 2013, A regulatory cascade involving class II ETHYLENE RESPONSE FACTOR transcriptional repressors operates in the progression of leaf senescence, Plant Physiol, 162, 991, 10.1104/pp.113.218115 He, 2015, TCP2 positively regulates HY5/HYH and photomorphogenesis in Arabidopsis, J. Exp. Bot., 775 Huq, 2004, Phytochrome-interacting factor 1 is a critical bHLH regulator of chlorophyll biosynthesis, Science, 305, 1937, 10.1126/science.1099728 Holm, 2002, Two interacting bZIP proteins are direct targets of COP1-mediated control of light-dependent gene expression in Arabidopsis, Genes Dev, 16, 1247, 10.1101/gad.969702 Chen, 2016, Shoot-to-root mobile transcription factor HY5 coordinates plant carbon and nitrogen acquisition, Curr. Biol., 26, 640, 10.1016/j.cub.2015.12.066 Son, 2012, Ethylene-responsive element-binding factor 5, ERF5, is involved in chitin-induced innate immunity response, Mol. Plant Microbe Interact., 25, 48, 10.1094/MPMI-06-11-0165 Pan, 2012, An ethylene response factor (ERF5) promoting adaptation to drought and salt tolerance in tomato, Plant Cell Rep, 31, 349, 10.1007/s00299-011-1170-3 Moffat, 2012, ERF5 and ERF6 play redundant roles as positive regulators of JA/Et-mediated defense against Botrytis cinerea in Arabidopsis, PLoS One, 7, e35995, 10.1371/journal.pone.0035995 Kalde, 2003, Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways, Mol. Plant Microbe Interact., 16, 295, 10.1094/MPMI.2003.16.4.295 Wu, 2003, Repression of gene expression by Arabidopsis HD2 histone deacetylases, Plant J, 34, 241, 10.1046/j.1365-313X.2003.01714.x Grasser, 2004, HMGB6 from Arabidopsis thaliana specifies a novel type of plant chromosomal HMGB protein, Biochemistry, 43, 1309, 10.1021/bi035931c Kim, 2014, Arabidopsis VIM proteins regulate epigenetic silencing by modulating DNA methylation and histone modification in cooperation with MET1, Mol. Plant, 7, 1470, 10.1093/mp/ssu079 Gentry, 2014, Remodelling chromatin to shape development of plants, Exp. Cell Res., 321, 40, 10.1016/j.yexcr.2013.11.010 Shultz, 2007, Genome-wide analysis of the core DNA replication machinery in the higher plants Arabidopsis and rice, Plant Physiol, 144, 1697, 10.1104/pp.107.101105 Chandran, 2014, Atypical E2F transcriptional repressor DEL1 acts at the intersection of plant growth and immunity by controlling the hormone salicylic acid, Cell Host Microbe, 15, 506, 10.1016/j.chom.2014.03.007 Zhao, 2013, Arabidopsis thaliana AHL family modulates hypocotyl growth redundantly by interacting with each other via the PPC/DUF296 domain, Proc. Natl. Acad. Sci. U. S. A, 110, 4688, 10.1073/pnas.1219277110 Ding, 2009, Transgenic expression of MYB15 confers enhanced sensitivity to abscisic acid and improved drought tolerance inArabidopsis thaliana, J. Genet. Genomics, 36, 17, 10.1016/S1673-8527(09)60003-5 Colangelo, 2004, The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response, Plant Cell, 16, 3400, 10.1105/tpc.104.024315 Andriankaja, 2014, Transcriptional coordination between leaf cell differentiation and chloroplast development established by TCP20 and the subgroup Ib bHLH transcription factors, Plant Mol. Biol., 85, 233, 10.1007/s11103-014-0180-2 Guan, 2014, Nitrate foraging by Arabidopsis roots is mediated by the transcription factor TCP20 through the systemic signaling pathway, Proc. Natl. Acad. Sci. U. S. A, 111, 15267, 10.1073/pnas.1411375111 Stec, 2013, Genomic heterogeneity and structural variation in soybean near isogenic lines, Front. Plant Sci., 4, 104, 10.3389/fpls.2013.00104 Charlson, 2005, Molecular marker Satt481 is associated with iron deficiency chlorosis resistance in a soybean breeding population, Crop Sci, 46, 2394, 10.2135/cropsci2004.0510 Feng, 2018, Soybean TCP transcription factors: Evolution, classification, protein interaction and stress and hormone responsiveness, Plant Physiol. Biochem., 127, 129, 10.1016/j.plaphy.2018.03.020 Zhang, 2003, Knockout analysis of Arabidopsis transcription factors TGA2, TGA5, and TGA6 reveals their redundant and essential roles in systemic acquired resistance, Plant Cell, 15, 2647, 10.1105/tpc.014894 Herrera-Vásquez, 2020 Cui, 2018, Four IVa bHLH transcription factors are novel interactors of FIT and mediate JA inhibition of iron uptake in Arabidopsis, Mol. Plant, 11, 1166, 10.1016/j.molp.2018.06.005 Valentinuzzi, 2020, Root-shoot-root Fe translocation in cucumber plants grown in a heterogeneous Fe provision, Plant Sci, 293, 10.1016/j.plantsci.2020.110431 Nakagami, 2020, The atypical E2F transcription factor DEL1 modulates growth–defense tradeoffs of host plants during root-knot nematode infection, Sci. Rep., 10, 8836, 10.1038/s41598-020-65733-3 Danisman, 2012, Arabidopsis class I and class II TCP transcription factors regulate jasmonic acid metabolism and leaf development antagonistically, Plant Physiol, 159, 1511, 10.1104/pp.112.200303 Kim, 2014, The Arabidopsis immune adaptor SRFR1 interacts with TCP transcription factors that redundantly contribute to effector-triggered immunity, Plant J, 78, 978, 10.1111/tpj.12527 Schwarz, 2020, Putative cis-regulatory elements predict iron deficiency responses in Arabidopsis roots, Plant Physiol, 182, 1420, 10.1104/pp.19.00760