Plant Molecular Biology

, Volume 77, Issue 1–2, pp 129–144 | Cite as

Transcriptional responses to flooding stress in roots including hypocotyl of soybean seedlings

  • Yohei Nanjo
  • Kyonoshin Maruyama
  • Hiroshi Yasue
  • Kazuko Yamaguchi-Shinozaki
  • Kazuo Shinozaki
  • Setsuko KomatsuEmail author


To understand the transcriptional responses to flooding stress in roots including hypocotyl of soybean seedlings, genome-wide changes in gene expression were analyzed using a soybean microarray chip containing 42,034 60-mer oligonucleotide probes. More than 6,000 of flooding-responsive genes in the roots including hypocotyl of soybean seedlings were identified. The transcriptional analysis showed that genes related to photosynthesis, glycolysis, Ser-Gly-Cys group amino acid synthesis, regulation of transcription, ubiquitin-mediated protein degradation and cell death were significantly up-regulated by flooding. Meanwhile, genes related to cell wall synthesis, secondary metabolism, metabolite transport, cell organization, chromatin structure synthesis, and degradation of aspartate family amino acid were significantly down-regulated. Comparison of the responses with other plants showed that genes encoding pyrophosphate dependent phosphofructokinase were down-regulated in flooded soybean seedlings, however, those in tolerant plants were up-regulated. Additionally, genes related to RNA processing and initiation of protein synthesis were not up-regulated in soybean, however, those in tolerant plants were up-regulated. Furthermore, we found that flooding-specific up-regulation of genes encoding small proteins which might have roles in acclimation to flooding. These results suggest that functional disorder of acclimative responses to flooding through transcriptional and post-transcriptional regulations is involved in occurring flooding injury to soybean seedlings.


Soybean Seedling Flooding Transcriptome 



Accelerated cell death


Allene oxide cyclase




Asparagine synthase


Anthocyanin 5-aromatic acyltransferase


Caffeic acid O-methyl transferase


Citrate synthase


Flooding inducible gene encoding small protein


Isocitrate dehydrogenase


Anthocyanin malonyltransferase


Malate dehydrogenase


Mildew resistance locus O


Nitrate reductase


Phosphoenolpyruvate carboxylase




Pyruvate kinase




Quantitative RT–PCR


Small open reading frames

SK1, 2

Snorkel 1, 2


Submergence 1A


Sucrose synthase


Tricarboxylic acid


Triose phosphate isomerase


Trehalose phosphate phosphatase


Trehalose phosphate synthase


UDP-gluocse pyrophosphorylase


Extra-large G-protein



We thank Dr. N Ahsan, Mr. Nouri Mohammad Zaman, Dr. Takuji Nakamura, Dr. Keito Nishizawa, Dr. Satoshi Shimamura, and Dr. Ryo Yamamoto for their helpful discussions. This work was supported by a Grant-in-Aid for Scientific Research (B) (1980015) from the Japan Society for the Promotion of Science.

Supplementary material

11103_2011_9799_MOESM1_ESM.tif (470 kb)
Supplementary Figure S1. Verification of microarray results by quantitative RT-PCR. The qRT-PCR analyses were performed with 6- and 12-h flooding treated and untreated samples to assess the microarray data. The Log2FC values of nine genes calculated from the qRT-PCR data from three biological replicates were plotted against the microarray data. A, the microarray data (white circle) and qRT-PCR (black circle) data of each gene were plotted together. B, scatter plot of microarray data versus qRT-PCR. The correlation coefficient (R2) between the two datasets is 0.954. (TIFF 470 kb)
11103_2011_9799_MOESM2_ESM.tif (3.6 mb)
Supplementary Figure S2. Overview of transcriptional changes in metabolic pathway under flooding. Log2FC values of differentially expressed genes were analyzed by use of the MapMan software. The color of each square indicates the Log2FC value of each gene. (TIFF 3697 kb)
11103_2011_9799_MOESM3_ESM.tif (922 kb)
Supplementary Figure S3. Alignment of deduced amino acid sequences of the highly inducible genes. The sequences were aligned by MAFFT multiple alignment program ver.6 (Katoh and Toh, 2008). The alignment was visualized by Jalview program 2.6.1. (Waterhouse et al., 2009). (A) alignment of amino acid sequences of FIS1, FIS2 and FIS3. B, alignment of amino acid sequences of FIS1 and Glyma12g05200.1. © alignment of amino acid sequences of FIS2, FIS16, FIS35 and FIS60. Contrast of color of shaded text indicates percent of identity. (TIFF 922 kb)
11103_2011_9799_MOESM4_ESM.tif (990 kb)
Supplementary Figure S4. In situ hybridization analysis of untreated soybean seedlings using probes for flooding inducible three genes. Bars in cotyledon panels and other panels indicate 200 μm and 1000 μm, respectively. (TIFF 990 kb)
11103_2011_9799_MOESM5_ESM.tif (1.5 mb)
Supplementary Figure S5. Root-tip death of flooded soybean seedlings. (A) Three days old seedling. (B) Flooded seedlings. The 2 days old seedlings were flooded with water for 3 days. After the 3 days of flooding treatment, the seedlings were grown on sands with normal irrigation for 2 days. Arrows indicate the region where the cell death like necrosis was observed. Bars indicate 10 mm. (TIFF 1517 kb)
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  1. Aoki T, Akashi T, Ayabe S (2000) Flavonoids of leguminous plants, structure, biological activity, and biosynthesis. J Plant Res 113:475–488CrossRefGoogle Scholar
  2. Bailey-Serres J, Voesenek LACJ (2008) Flooding stress, acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339PubMedCrossRefGoogle Scholar
  3. Banti V, Mafessoni F, Loreti E, Alpi A, Perata P (2010) The heat-inducible transcription factor hsfa2 enhances anoxia tolerance in Arabidopsis. Plant Physiol 152:1471–1483PubMedCrossRefGoogle Scholar
  4. Branco-Price C, Kawaguchi R, Ferreira RB, Bailey-Serres J (2005) Genome-wide analysis of transcripts abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation. Ann Bot 96:647–660PubMedCrossRefGoogle Scholar
  5. Branco-Price C, Kaiser KA, Jang CJH, Larive CK, Bailey-Serres J (2008) Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. Plant J 56:743–755PubMedCrossRefGoogle Scholar
  6. Chiba M, Kubo M, Miura T, Sato T, Rezaeian AH, Kiyosawa H, Ohkohchi N, Yasue H (2008) Localization of sense and antisense transcripts of Prdx2 gene in mouse tissues. Cytogenet Genome Res 121:222–231PubMedCrossRefGoogle Scholar
  7. Christianson JA, Llewellyn DJ, Dennis ES, Wilson IW (2010) Global gene expression responses to waterlogging in roots and leaves of cotton (gossypium hirsutum L.) Plant Cell Physiol 51:21–37Google Scholar
  8. Creelman RA, Mullet JE (1995) Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress. Proc Natl Acad Sci USA 92:4114–4119PubMedCrossRefGoogle Scholar
  9. Creelman RA, Tierney ML, Mullet JE (1992) Jasmonic acid/methyl jasmonate accumulate in wounded soybean hypocotyls and modulate wound gene expression. Proc Natl Acad Sci USA 89:4938–4941PubMedCrossRefGoogle Scholar
  10. Devoto A, Piffanelli P, Nilsson I, Wallin E, Panstruga R, von Heijne G, Schulze-Lefert P (1999) Topology, subcellular localization, and sequence diversity of Mlo family in plants. J Biol Chem 274:34993–35004PubMedCrossRefGoogle Scholar
  11. Ding L, Pandey S, Assmann SM (2008) Arabidopsis extra-large G proteins (XLGs) regulate root morphogenesis. Plant J 53:248–263PubMedCrossRefGoogle Scholar
  12. Drew MC, Cobb BG, Johnson JR, Andrews D, Morgan PW, Jordan W, He CJ (1994) Metabolic acclimation of root tips to oxygen deficiency. Ann Bot 74:281–286CrossRefGoogle Scholar
  13. Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70PubMedCrossRefGoogle Scholar
  14. Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371PubMedCrossRefGoogle Scholar
  15. Fennoy SL, Bailey-Serres J (1995) Post-transcriptional regulation of gene expression in oxygen-deprived roots of maize. Plant J 7:287–295CrossRefGoogle Scholar
  16. Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690PubMedCrossRefGoogle Scholar
  17. Fukao T, Bailey-Serres J (2004) Plant responses to hypoxia—is survival a balancing act? Trends Plant Sci 9:449–456PubMedCrossRefGoogle Scholar
  18. Gibbs J, Greenway H (2003) Mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Funct Plant Biol 30:1–47CrossRefGoogle Scholar
  19. Gladish DK, Xu J, Niki T (2006) Apoptosis-like programmed cell death occurs in procambium and ground meristem of pea (Pisum sativum) root tips exposed to sudden flooding. Ann Bot 97:895–902PubMedCrossRefGoogle Scholar
  20. Greenberg JT, Ausubel FM (1993) Arabidopsis mutants comprised for the control of cellular damage during pathogenesis and aging. Plant J 4:327–341PubMedCrossRefGoogle Scholar
  21. Hanada K, Zhang X, Borevitz JO, Li WH, Shiu SH (2007) A large number of novel coding small open reading frames in the intergenic regions of the Arabidopsis thaliana genome are transcribed and/or under purifying selection. Genome Res 17:632–640PubMedCrossRefGoogle Scholar
  22. Harada T, Satoh S, Yoshioka T, Ishizawa K (2007) Anoxia-enhanced expression of genes isolated by suppression subtractive hybridization from pondweed (Potamogeton distinctus A. Benn.) turions. Planta 226:1041–1052PubMedCrossRefGoogle Scholar
  23. Hashiguchi A, Sakata K, Komatsu S (2009) Proteome analysis of early-stage soybean seedlings under flooding stress. J Proteome Res 8:2058–2069PubMedCrossRefGoogle Scholar
  24. Hashimoto Y, Kondo T, Kageyama Y (2008) Lilliputians get into the limelight: novel class of small peptides genes in morphogenesis. Dev Growth Differ 50:S269–S276PubMedCrossRefGoogle Scholar
  25. Hattori Y, Nagai K, Furukawa S et al (2009) The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460:1026–1031PubMedCrossRefGoogle Scholar
  26. Huang B, Johnson JW (1995) Root respiration and carbohydrate status of two wheat genotypes in response to hypoxia. Ann Bot 75:427–432CrossRefGoogle Scholar
  27. Jackson MB, Colmer TD (2005) Response and adaptation by plants to flooding stress. Ann Bot 96:501–505PubMedCrossRefGoogle Scholar
  28. Jackson MB, Ram PC (2003) Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence. Ann Bot 91:227–241PubMedCrossRefGoogle Scholar
  29. Kastenmayer JP, Ni L, Chu A, Kitchen LE, Au WC, Yang H, Carter CD, Wheeler D, Davis RW, Boeke JD, Snyder MA, Basrai MA (2006) Functional genomics of genes with small open reading frames (sORFs) in S. cerevisiae. Genome Res 16:365–373PubMedCrossRefGoogle Scholar
  30. Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9:286–298PubMedCrossRefGoogle Scholar
  31. Kirkpatrick MT, Rupe JC, Rothrock CS (2006) Soybean response to flooded soil conditions and the association with soil borne plant pathogenic genera. Plant Dis 90:592–596CrossRefGoogle Scholar
  32. Klok EJ, Wilson IW, Wilson D, Chapman SC, Ewing RM, Somerville SC, Peacock WJ, Dolferus R, Dennis ES (2002) Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. Plant Cell 14:2481–2494PubMedCrossRefGoogle Scholar
  33. Komatsu S, Yamamoto R, Nanjo Y, Mikami Y, Yunokawa H, Sakata K (2009) A comprehensive analysis of the soybean genes and proteins expressed under flooding stress using transcriptome and proteome techniques. J Proteome Res 8:4766–4778PubMedCrossRefGoogle Scholar
  34. Komatsu S, Kobayashi Y, Nishizawa K, Nanjo Y, Furukawa K (2010) Comparative proteomics analysis of differentially expressed proteins in soybean cell wall during flooding stress. Amino Acids 39:1435–1449PubMedCrossRefGoogle Scholar
  35. Kreuzwieser J, Katharine JH, Howell A, Carroll A, Rennenberg H, Millar AH, Whelan J (2009) Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol 149:461–473PubMedCrossRefGoogle Scholar
  36. Lasanthi-Kudahettige R, Magneschi L, Loreti E, Gonzali S, Licausi F, Novi G, Beretta O, Vitulli F, Alpi A, Perata P (2007) Transcript profiling of the anoxic rice coleoptile. Plant Physiol 144:218–231PubMedCrossRefGoogle Scholar
  37. Laskowski M, Biller S, Stanley K, Kajstura T, Prusty R (2006) Expression profiling of auxin-treated Arabidopsis roots: toward a molecular analysis of lateral root emergence. Plant Cell Physiol 47:788–792PubMedCrossRefGoogle Scholar
  38. Liu F, Vantoai T, Moy LP, Bock G, Linford LD, Quackenbush J (2005) Global transcription profiling reveals comprehensive insight into hypoxic response in Arabidopsis. Plant Physiol 137:1115–1129PubMedCrossRefGoogle Scholar
  39. Loreti E, Poggi A, Novi G, Alpi A, Perata P (2005) A genome-wide analysis of the effects of sucrose on gene expression in Arabidopsis seedlings under anoxia. Plant Physiol 137:1130–1138PubMedCrossRefGoogle Scholar
  40. Moldovan D, Spriggs A, Yang J, Pogson BJ, Dennis ES, Wilson LW (2010) Hypoxia-responsive microRNAs and trans-acting small interfering RNAs in Arabidopsis. J Exp Bot 61:165–177PubMedCrossRefGoogle Scholar
  41. Mommer L, Visser EJW (2005) Underwater photosynthesis in flooded terrestrial plants: a matter of leaf plasticity. Ann Bot 96:581–589PubMedCrossRefGoogle Scholar
  42. Mustroph A, Zanetti ME, Jang CJH, Holtan HE, Repetti PP, Galbraith DW, Girke T, Bailey-Serres J (2009) Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia. Proc Natl Acad Sci USA 106:18843–18848PubMedCrossRefGoogle Scholar
  43. Mustroph A, Lee SC, Oosumi T, Zanetti ME, Yang H, Ma K, Yaghoubi-Masihi A, Fukao T, Bailey-Serres J (2010) Cross-kingdom comparison of transcriptomic adjustments to low-oxygen stress highlight conserved and plant-specific responses. Plant Physiol 152:1484–1500PubMedCrossRefGoogle Scholar
  44. Nanjo Y, Skultety L, Ashraf Y, Komatsu S (2010) Comparative proteomic analysis of early-stage soybean seedlings responses to flooding by using gel and gel-free techniques. J Proteome Res 9:3989–4002PubMedCrossRefGoogle Scholar
  45. Narsai R, Howell KA, Carroll A, Ivanova A, Millar AH, Whelan J (2009) Defining core metabolic and transcriptomic responses to oxygen availability in rice embryos and young seedlings. Plant Physiol 151:306–322PubMedCrossRefGoogle Scholar
  46. Neff MM, Chory J (1998) Genetic interactions between phytochrome A, phytochrome B, and cryptochrome 1 during Arabidopsis development. Plant Physiol 118:27–36PubMedCrossRefGoogle Scholar
  47. Ogawa T, Pan L, Kawai-Yamada M, Yu LH, Yamamura S, Koyama T, Kitajima S, Ohme-Takagi M, Sato F, Uchimiya H (2005) Functional analysis of Arabidopsis ethylene-responsive element binding protein conferring resistance to Bax and abiotic stress-induced plant cell death. Plant Physiol 138:1436–1445PubMedCrossRefGoogle Scholar
  48. Piffanelli P, Zhou F, Casais C, Orme J, Jarosch B, Schaffrath U, Collins NC, Panstruga R, Schulze-Lefert P (2002) The barley mlo modulator of defense and cell death is responsive to biotic and abiotic stress stimuli. Plant Physiol 129:1076–1085PubMedCrossRefGoogle Scholar
  49. Pnueli L, Hallak-Herr E, Rozenberg M, Cohen M, Goloubinoff P, Kaplan A, Mittler R (2002) Molecular and biochemical mechanisms associated with dormancy and drought tolerance in the desert legume Retama raetam. Plant J 31:319–330PubMedCrossRefGoogle Scholar
  50. Pružinská A, Tanner G, Anders I, Roca M, Hörtensteiner S (2003) Chlorophyll breakdown: pheophorbide a oxygenase is a Rieske-type iron-sulfur protein, encoded by the accelerated cell death 1 gene. Proc Natl Acad Sci USA 100:15259–15264PubMedCrossRefGoogle Scholar
  51. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, NJ, pp 365–386Google Scholar
  52. Russell DA, Wong DML, Sachs MM (1990) The anaerobic responses of soybean. Plant Physiol 92:401–407PubMedCrossRefGoogle Scholar
  53. Schmid M, Davison TS, Henz SR, Page UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37:501–506PubMedCrossRefGoogle Scholar
  54. Schmutz J, Cannon SB, Schlueter J et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 46:178–183CrossRefGoogle Scholar
  55. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292PubMedCrossRefGoogle Scholar
  56. Shi F, Yamamoto R, Shimamura S, Hiraga S, Nakayama N, Nakamura T, Yukawa K, Hachinohe M, Matsumoto H, Komatsu S (2008) Cytosolic ascorbate peroxidase 2 cAPX2. is involved in the soybean response to flooding. Phytochem 69:1295–1303CrossRefGoogle Scholar
  57. Steffens B, Sauter M (2010) G proteins as regulators in ethylene-mediated hypoxia signaling. Plant Signal Behav 5:375–378PubMedCrossRefGoogle Scholar
  58. Subbaiah CC, Sachs MM (2003) Molecular and cellular adaptations of maize to flooding stress. Ann Bot 90:119–127CrossRefGoogle Scholar
  59. Tran LSP, Truyen N, Quach TN, Satish K, Guttikonda SK, Aldrich DL, Kumar R, Neelakandan A, Valliyodan B, Nguyen HT (2009) Molecular characterization of stress-inducible GmNAC genes in soybean. Mol Genet Genomics 281:647–664PubMedCrossRefGoogle Scholar
  60. Umezawa T, Sakurai T, Totoki Y et al (2008) Sequencing and analysis of approximately 40,000 soybean cDNA clones from a full-length-enriched cDNA library. DNA Res 15:333–346PubMedCrossRefGoogle Scholar
  61. Usadel B, Nagel A, Thimm O et al (2005) Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of corresponding genes, and comparison with known responses. Plant Physiol 138:1195–1204PubMedCrossRefGoogle Scholar
  62. Usadel B, Poree F, Nagel A, Lohse M, Czedik-Eysenberg A, Stitt M (2009) A guide to using MapMan to visualize and compare omics data in plants: a case study in the crop species, Maize. Plant Cell Environ 32:1211–1229PubMedCrossRefGoogle Scholar
  63. van Dongen JT, Fröhlich A, Ramírez-Aguilar SJ, Schauer N, Fernie AR, Erban A, Kopka J, Clark J, Langer A, Geigenberger P (2009) Transcript and metabolite profiling of the adaptive response to mild decreases in oxygen concentration in the roots of Arabidopsis plants. Ann Bot 103:269–280PubMedCrossRefGoogle Scholar
  64. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ (2009) Jalview Version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189–1191PubMedCrossRefGoogle Scholar
  65. Weisshaar B, Jenkins GI (1998) Phenylpropanoid biosynthesis and its regulation. Curr Opin Plant Biol 1:251–257PubMedCrossRefGoogle Scholar
  66. Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442:705–708PubMedCrossRefGoogle Scholar
  67. Zhang ZX, Zou XL, Tang WH, Zheng YL (2006) Revelation on early response and molecular mechanism of submergence tolerance in maize roots by microarray and suppression subtractive hybridization. Environ Exp Bot 58:53–63CrossRefGoogle Scholar
  68. Zhang Z, Wei L, Zou X, Tao Y, Liu Z, Zheng Y (2008) Submergence-responsive microRNAs are potentially involved in the regulation of morphological and metabolic adaptations in maize root cells. Ann Bot 102:509–519PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Yohei Nanjo
    • 1
  • Kyonoshin Maruyama
    • 2
  • Hiroshi Yasue
    • 3
    • 4
  • Kazuko Yamaguchi-Shinozaki
    • 2
    • 5
  • Kazuo Shinozaki
    • 6
  • Setsuko Komatsu
    • 1
    Email author
  1. 1.National Institute of Crop ScienceTsukubaJapan
  2. 2.Biological Resources DivisionJapan International Research Center for Agricultural SciencesTsukubaJapan
  3. 3.Division of Animal ScienceNational Institute of Agricultural SciencesTsukubaJapan
  4. 4.Tsukuba GeneTechnology Laboratories Inc.TsukubaJapan
  5. 5.Graduate School of Agricultural and Life SciencesUniversity of TokyoTokyoJapan
  6. 6.Plant Science CenterRIKENYokohamaJapan

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