Abstract
The Lesion Simulating Disease (LSD) genes encode a family of zinc finger proteins that are reported to play an important role in the hypersensitive response and programmed cell death (PCD) that are caused by biotic and abiotic stresses. In the present study, 117 putative LSD family members were identified in Viridiplantae. Genes with one, two, or three conserved LSD domains were identified. Proteins with three LSD domains were highly represented in the species analyzed and were present in basal organisms. Proteins with two LSD domains were identified only in the Embryophyte clade, and proteins possessing one LSD domain were highly represented in grass species. Expression analyses of Glycine max LSD (GmLSD) genes were performed by real-time quantitative polymerase chain reaction. The results indicated that GmLSD genes are not ubiquitously expressed in soybean organs and that their expression patterns are instead organ-dependent. The expression of the majority of GmLSD genes is modulated in soybean during Phakopsora pachyrhizi infection. In addition, the expression of some GmLSD genes is modulated in plants under dehydration stress. These results suggest the involvement of GmLSD genes in the response of soybean to both biotic and abiotic stresses.







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References
Almeida BB, da Silva WG, Moreira MA, de Barros EG (2011) In silico characterization and expression analysis of the multigene family encoding the Bowman–Birk protease inhibitor in soybean. Mol Biol Rep 39:327–334
Almeida HO, Barbosa MO, Marques AE, Pereira THA, Júnior MJM, Tessarollo NG, Games PD, de Barros EG, Stolf-Moreira R, Marcelino-Guimarães FC, Abdelnoor RV, Pereira PRG, Baracat-Pereira MC (2012) Differentially regulated induced resistance marker enzymes in soybean genotypes resistant and susceptible to Asian soybean rust. Pesq Agrop Brasileira 47:163–172
Aroca R, Porcel R, Ruiz-Lozano JM (2011) Regulation of root water uptake under abiotic stress conditions. J Exp Bot 63:43–57
Aviv DH, Rusterucci C, Holt BF III, Dietrich RA, Parker JE, Dangl JL (2002) Runaway cell death, but not basal disease resistance, in lsd1 is SA- and NIM1/NPR1-dependent. Plant J 29:381–391
Bhatti KH, Xu C, Wu J, He C (2008) Overexpression of rice OsLOL2 gene confers disease resistance in tobacco to Pseudomonas syringae pv. tabaci. Prog Nat Sci 18:807–812
Bromfield KR, Hartwig EE (1980) Resistance to soybean rust and mode of inheritance. Crop Sci 20:254–255
Bromfield KR, Melching JS (1982) Sources of specific resistance to soybean rust. Phytopathology 72:706
Cagliari A, Turchetto-Zolet AC, Maraschin FS, Loss G, Margis R, Margis-Pinheiro M (2011) The evolutionary history of CBF transcription factors: gene duplication of CCAAT-binding factors NF-Y in plants. In: Friedberg F (ed) Gene duplication. InTech, Rijeka, pp. 1–27
Coll NS, Vercammen D, Smidler A, Clover C, Van Breusegem F, Dangl JL, Epple P (2010) Arabidopsis type I metacaspases control cell death. Science 330:1393–1397
Dietrich RA, Delaney TP, Uknes SJ, Ward ER, Ryals JA, Dangl JL (1994) Arabidopsis mutants simulating disease resistance response. Cell 77:565–577
Dietrich RA, Richberg MH, Schmidt R, Dean C, Dangl JL (1997) A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death. Cell 88:685–694
Dubos C, Plomion C (2003) Identification of water-deficit responsive genes in maritime pine (Pinus pinaster Ait.) roots. Plant Mol Biol 51:249–262
Epple P, Mack AA, Morris VR, Dangl JL (2003) Antagonistic control of oxidative stress-induced cell death in Arabidopsis by two related, plant-specific zinc finger proteins. Proc Natl Acad Sci USA 100:6831–6836
Fehr WR, Caviness CE (1977) Stages on soybean development. Iowa State University, Ames, IA
Garcia A, Calvo ES, de Souza Kiihl RA, Harada A, Hiromoto DM, Vieira LG (2008) Molecular mapping of soybean rust (Phakopsora pachyrhizi) resistance genes: discovery of a novel locus and alleles. Theor Appl Genet 117:545–553
Goellner K, Loehrer M, Langenbach C, Conrath U, Koch E, Schaffrath U (2010) Phakopsora pachyrhizi, the causal agent of Asian soybean rust. Mol Plant Pathol 11:169–177
Hartwig EE (1986) Identification of a fourth major gene conferring resistance to soybean rust. Crop Sci 26:1135–1136
Hartwig EE, Bromfield KR (1983) Relationships among three genes conferring specific resistance to rust in soybeans. Crop Sci 23:237–239
He S, Huang K, Zhang X, Yu X, Huang P, An C (2011a) The LSD1-type zinc finger motifs of Pisum sativa LSD1 Are a novel nuclear localization signal and interact with Importin Alpha. PLoS One 6:e22131
He S, Tan G, Liu Q, Huang K, Ren J, Zhang X, Yu X, Huang P, An C (2011b) The LSD1-interacting protein GILP is a LITAF domain protein that negatively regulates hypersensitive cell death in Arabidopsis. PLoS One 6:e18750
Huang X, Li Y, Zhang X, Zuo J, Yang S (2010) The Arabidopsis LSD1 gene plays an important role in the regulation of low temperature-dependent cell death. New Phytol 187:301–312
Hunt MD, Delaney TP, Dietrich RA, Weymann KB, Dangl JL, Ryals JA (1997) Salicylate-independent lesion formation in Arabidopsis lsd mutants. Mol Plant Microbe Interact 10:531–536
Jabs T, Dietrich RA, Dangl JL (1996) Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273:1853–1856
Jian B, Liu B, Bi Y, Hou W, Wu C, Han T (2008) Validation of internal control for gene expression study in soybean by quantitative real-time PCR. BMC Mol Biol 9:1–14
Jung CH, Wong CE, Singh MB, Bhalla PL (2012) Comparative genomic analysis of soybean flowering genes. PLoS One 7:e38250
Kakumanu A, Ambavaram MM, Klumas C, Krishnan A, Batlang U, Myers E, Grene R, Pereira A (2012) Effects of drought on gene expression in maize reproductive and leaf meristem tissue revealed by RNA-Seq. Plant Physiol 160:846–867
Kaminaka H, Nake C, Epple P, Dittgen J, Schutze K, Chaban C, Holt BF III, Merkle T, Schafer E, Harter K, Dangl JL (2006) bZIP10-LSD1 antagonism modulates basal defense and cell death in Arabidopsis following infection. EMBO J 25:4400–4411
Kim KS, Unfried JR, Hyten DL, Frederick RD, Hartman GL, Nelson RL, Song Q, Diers BW (2012) Molecular mapping of soybean rust resistance in soybean accession PI 561356 and SNP haplotype analysis of the Rpp1 region in diverse germplasm. Theor Appl Genet 125:1339–1352
Kliebenstein DJ, Dietrich RA, Martin AC, Last RL, Dangl JL (1999) LSD1 regulates salicylic acid induction of copper zinc superoxide dismutase in Arabidopsis thaliana. Mol Plant Microbe Interact 12:1022–1026
Kulcheski FR, de Oliveira LF, Molina LG, Almerão MP, Rodrigues FA, Marcolino J, Barbosa JF, Stolf-Moreira R, Nepomuceno AL, Marcelino-Guimarães FC, Abdelnoor RV, Nascimento LC, Carazzolle MF, Pereira GA, Margis R (2011) Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genomics 12:307–324
Ledrera R, Marino D, Larrainzar E, Gonzales EM, Aresse-Igor C (2007) Reduced carbon availability to bacteroids and elevated ureides in nodules, but not in shoots, are involved in the Nitrogen fixation response to early drought in soybean. Plant Physiol 145:539–546
Li S, Smith JR, Ray JD, Frederick RD (2012) Identification of a new soybean rust resistance gene in PI 567102B. Theor Appl Genet 125:133–142
Libault M, Thibivilliers S, Bilgin DD, Radwan O, Benitez M, Clough SJ, Stacey G (2008) Identification of four soybean reference genes for gene expression normalization. The Plant Genome 1:44–54
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDC T Method. Methods 25:402–408
Manavalan LP, Guttikonda SK, Tran LS, Nguyen HT (2009) Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol 50:1260–1276
Martins PK, Jordão BK, Yamanaka N, Farias JRB, Beneventi MA, Binneck E, Fuganti R, Stolf R, Nepomuceno AL (2008) Differential gene expression and mitotic cell analysis of the drought tolerant soybean (Glycine max L. Merrill Fabales, Fabaceae) cultivar MG/BR46 (Conquista) under two water deficit induction systems. Genet Mol Biol 31:512–521
Mateo A, Muhlenbock P, Rusterucci C, Chang CC, Miszalski Z, Karpinska B, Parker JE, Mullineaux PM, Karpinski S (2004) LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiol 136:2818–2830
McLean RJ, Byth DE (1980) Inheritance of resistance to rust (Phakopsora pachyrhizi) in soybeans. Aust J Agric Res 31:951–956
Meckel L, Egli DB, Phillips RE, Radcliffe D, Leggett JE (1984) Effect of moisture stress on seed growth in soybeans. Agron J 75:1027–1031
Mehrotra R, Kiran K, Chaturvedi CP, Ansari SA, Lodhi N, Sawant, Tuli R (2005) Effect of copy number and spacing of the ACGT and GT cis elements on transient expression of minimal promoter in plants. J Genet 84:183–187
Mochida K, Yoshida T, Sakurai T, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2009) In silico analysis of transcription factor repertoire and prediction of stress responsive transcription factors in soybean. DNA Res 16:353–369
Muhlenbock P, Plaszczyca M, Mellerowicz E, Karpinski S (2007) Lysigenous aerenchyma formation in Arabidopsis is controlled by Lesion Simulating Disease1. Plant Cell 19:3819–3830
Muhlenbock P, Szechynska-Hebda M, Plaszczyca M, Baudo M, Mateo A, Mullineaux PM, Parker JE, Karpinska B, Karpinski S (2008) Chloroplast signaling and Lesion Simulating Disease1 regulate crosstalk between light acclimation and immunity in Arabidopsis. Plant Cell 20:2339–2356
Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148
Oya T, Nepomuceno AL, Neumaier N, Farias JRB, Tobita S, Ito O (2004) Drought tolerance characteristics of Brazilian soybean cultivars—evaluation and characterization of drought tolerance of various Brazilian soybean cultivars in the field. Plant Prod Sci 7:129–137
Panthee DR, Yuan JS, Wright DL, Marois JJ, Mailhot D, Stewart CN Jr (2007) Gene expression analysis in soybean in response to the causal agent of Asian soybean rust (Phakopsora pachyrhizi Sydow) in an early growth stage. Funct Integr Genomics 7:291–301
Porcel R, Ruiz-Lozano JM (2004) Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. J Exp Bot 55:1743–1750
Requejo R, Hurd TR, Costa NJ, Murphy MP (2010) Cysteine residues exposed on protein surfaces are the dominant intramitochondrial thiol and may protect against oxidative damage. FEBS J 277:1465–1480
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, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183
Schneider KT, van de Mortel M, Bancroft TJ, Braun E, Nettleton D, Nelson RT, Frederick RD, Baum TJ, Graham MA, Whitham SA (2011) Biphasic gene expression changes elicited by Phakopsora pachyrhizi in soybean correlate with fungal penetration and haustoria formation. Plant Physiol 157:355–371
Shi J, Zhang L, An H, Wu C, Guo X (2011) GhMPK16, a novel stress-responsive group D MAPK gene from cotton, is involved in disease resistance and drought sensitivity. BMC Mol Biol 12:22–36
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 28:2731–2739
Thibaud-Nissen F, Ouyang S, Buell CR (2009) Identification and characterization of pseudogenes in the rice gene complement. BMC Genomics 10:317–329
Tran LS, Mochida K (2010) Functional genomics of soybean for improvement of productivity in adverse conditions. Funct Integr Genomics 10:447–462
van de Mortel M, Recknor JC, Graham MA, Nettleton D, Dittman JD, Nelson RT, Godoy CV, Abdelnoor RV, Almeida AM, Baum TJ, Whitham SA (2007) Distinct biphasic mRNA changes in response to Asian soybean rust infection. Mol Plant Microbe Interact 20:887–899
Walther D, Brunnemann R, Selbig J (2007) The regulatory code for transcriptional response diversity and its relation to genome structural properties in A. thaliana. PLoS Genet 3:e11
Wang L, Pei Z, Tian Y, He C (2005) OsLSD1, a rice zinc finger protein, regulates programmed cell death and callus differentiation. Mol Plant Microbe Interact 18:375–384
Wang Z, Hobson N, Galindo L, Zhu S, Shi D, McDill J, Yang L, Hawkins S, Neutelings G, Datla R, Lambert G, Galbraith DW, Grassa CJ, Geraldes A, Cronk QC, Cullis C, Dash PK, Kumar PA, Cloutier S, Sharpe AG, Wong GK, Wang J, Deyholos MK (2012) The genome of flax (Linum usitatissimum) assembled de novo from short shotgun sequence reads. Plant J 72:461–473
Weymann K, Hunt M, Uknes S, Neuenschwander U, Lawton K, Steiner HY, Ryals J (1995) Suppression and restoration of lesion formation in Arabidopsis lsd mutants. Plant Cell 7:2013–2022
Wiebke-Strohm B, Pasquali G, Margis-Pinheiro M, Bencke M, Bucker-Neto L, Becker-Ritt AB, Martinelli AH, Rechenmacher C, Polacco JC, Stolf R, Marcelino FC, Abdelnoor RV, Homrich MS, Del Ponte EM, Carlini CR, De Carvalho MC, Bodanese-Zanettini MH (2012) Ubiquitous urease affects soybean susceptibility to fungi. Plant Mol Biol 79:75–87
Xu C, He C (2007) The rice OsLOL2 gene encodes a zinc finger protein involved in rice growth and disease resistance. Mol Genet Genomics 278:85–94
Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803
Yeh SH, Lin CS, Wu FH, Wang AY (2011) Analysis of the expression of BohLOL1, which encodes an LSD1-like zinc finger protein in Bambusa oldhamii. Planta 234:1179–1189
Yi J, Derynck MR, Chen L, Dhaubhadel S (2010) Differential expression of CHS7 and CHS8 genes in soybean. Planta 231:741–753
Zhang XC, Wang Z, Zhang X, Le MH, Sun J, Xu D, Cheng J, Stacey G (2012) Evolutionary dynamics of protein domain architecture in plants. BMC Evol Biol 12:6–17
Zhu L, Zhang Y, Zhang W, Yang S, Chen JQ, Tian D (2009) Patterns of exon–intron architecture variation of genes in eukaryotic genomes. BMC Genomics 10:47–58
Zou C, Lehti-Shiu MD, Thomashow M, Shiu SH (2009) Evolution of stress-regulated gene expression in duplicate genes of Arabidopsis thaliana. PLoS Genet 5:e1000581
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This work was supported by grants from the GENOSOJA/CNPq and BIOTECSUR II/MCT.
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Fig. S1
Relative expression levels of the GmLSD genes in each different organ of the Conquista Brazilian soybean cultivar. The values are the means of three biological replicates with four technical replicates each. The means that are labeled identically (with a letter) do not differ significantly (Tukey comparison test, p < 0.05). ACTII, CYP2 and metalloprotease reference genes were used as internal controls to normalize for the amount of mRNA present in each sample. In each organ, the gene with the lowest transcript level was used to normalize the transcript levels of the other genes. To allow a better comparison of groups of genes that exhibited large differences in their expression levels, some graphs of fold-change are shown in log2 scale, and this is indicated at the y axis. ND: no detected (PDF 40 kb)
Table S1
Summary of the GmLSD gene RT-qPCR primer sequences (PDF 51 kb)
Table S2
Species, acronym, locus and EST identified for the 117 LSD genes (PDF 149 kb)
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Cabreira, C., Cagliari, A., Bücker-Neto, L. et al. The Lesion Simulating Disease (LSD) gene family as a variable in soybean response to Phakopsora pachyrhizi infection and dehydration. Funct Integr Genomics 13, 323–338 (2013). https://doi.org/10.1007/s10142-013-0326-3
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DOI: https://doi.org/10.1007/s10142-013-0326-3


