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Global gene expression responses to waterlogging in leaves of rape seedlings

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Abstract

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Waterlogging stress caused a decrease of leaf chlorophyll content and premature leaf senescence, which are associated with dramatic changes in gene expression profiles in the aerial leaves of root-waterlogged rape seedlings.

Abstract

Soil waterlogging is a serious constraint to crop production. We investigated the physiological responses of rape (Brassica napus L.) seedlings to waterlogging stress and analyzed global gene transcription responses in the aerial leaves of waterlogged rape seedlings. Seedlings of ‘Tammi’ and ‘Youngsan’ cultivars were subjected to waterlogging for 3 and 6 days and recovery for 5 days. Waterlogging stress caused a significant decrease in leaf chlorophyll content and premature senescence of the leaves. Maximal quantum efficiency of PSII (F v/F m) decreased in the waterlogged seedlings compared with the control plants. To evaluate whether the observed physiological changes in the leaves are associated with the differential regulation of gene expression in response to waterlogging stress, we analyzed the global transcriptional profile of leaves of ‘Tammi’ seedlings that were exposed to waterlogging for a short period (36 and 72 h). SolexaQA RNA-seq analysis revealed that a total of 4,484 contigs (8.5 %) of all contigs assayed (52,747) showed a twofold change in expression after 36 h of the start of waterlogging and 9,659 contigs (18.3 %) showed a twofold change after 72 h. Major genes involved in leaf photosynthesis, including light reactions and carbon-fixing reactions, were downregulated, while a number of genes involved in the scavenging of reactive oxygen species, degradation (proteins, starch, and lipids), premature senescence, and abiotic stress tolerance were upregulated. Transcriptome analysis data suggested that the aerial leaves of waterlogged rape seedlings respond to hypoxia by regulating the expression of diverse genes in the leaves.

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References

  • Ahsan N, Lee D-G, Lee S-H, Kang KY, Bahk JD, Choi MS, Lee I-J, Renaut J, Lee B-H (2007) A comparative proteomic analysis of tomato leaves in response to waterlogging stress. Physiol Plant 131:555–570

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Apse MP, Sottosanto JB, Blumwald E (2003) Vacuolar cation/H+ exchange, ion homeostasis, and leaf development are altered in a T-DNA insertional mutant of AtNHX1, the Arabidopsis vacuolar Na+/H+ antiporter. Plant J 36:229–239

    Article  CAS  PubMed  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25–29

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bailey-Serres J, Chang R (2005) Sensing and signalling in response to oxygen deprivation in plants and other organisms. Ann Bot (Lond) 96:507–518

    Article  CAS  Google Scholar 

  • Boru G, Vantoai T, Alves J, Hua D, Knee M (2003) Responses of soybean to oxygen deficiency and elevated root-zone carbon dioxide concentration. Ann Bot 91:447–453

    Article  CAS  PubMed  Google Scholar 

  • Branco-Price C, Kawaguchi R, Ferreira R, Bailey-Serres J (2005) Genome-wide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation. Ann Bot 96:647–660

    Article  CAS  PubMed  Google Scholar 

  • Camilo CM, Gomes SL (2010) Transcriptional response to hypoxia in the aquatic fungus Blastocladiella emersonii. Eukaryot Cell 9(6):915–925

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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(1):21–37

    Article  CAS  PubMed  Google Scholar 

  • Cominelli E, Galbiati M, Vavasseur A, Conti L, Sala T, Vuylsteke M, Leonhardt N, Dellaporta SL, Tonelli C (2005) A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Curr Biol 15:1196–1200

    Article  CAS  PubMed  Google Scholar 

  • Cox MP, Peterson DA, Biggs PJ (2010) SolexaQA: at-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinformatics 11:485

    Article  PubMed Central  PubMed  Google Scholar 

  • Desimone M, Henke A, Wagner E (1996) Oxidative stress induces partial degradation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in isolated chloroplasts of Barley. Plant Physiol 111:789–796

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dolferus R, de Bruxelles GL, Dennis ES, Peacock WJ (1994) Regulation of the Arabidopsis Adh gene by anaerobic and other environmental stresses. Ann Bot 74:301–308

    Article  CAS  Google Scholar 

  • Drew MC (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annu Rev Plant Physiol Plant Mol Biol 48:223–250

    Article  CAS  PubMed  Google Scholar 

  • Geigenberger P (2003) Response of plant metabolism to too little oxygen. Curr Opin Plant Biol 6(3):247–256

    Article  CAS  PubMed  Google Scholar 

  • Henderson JN, Hazra S, Dunkle AM, Salvucci ME, Wachter RM (2013) Biophysical characterization of higher plant Rubisco activase. Biochim Biophys Acta 1834(1):87–97

    Article  CAS  PubMed  Google Scholar 

  • Jackson MB (1990) Hormones and developmental change in plants subjected to submergence or soil waterlogging. Aquatic Bot 38:49–72

    Article  CAS  Google Scholar 

  • 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 culture. Plant Cell 14:2481–2494

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kreuzwieser J, Hauberg J, Howell KA, Carroll A, Rennenberg H, Millar AH, Whelan J (2009) Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol 149:461–473

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ku Y-G, Park W, Bang J-K, Jang Y-S, Kim Y-B, Bae H-J, Suh M-C, Ahn S-J (2009) Physiological response, fatty acid composition and yield component of Brassica napus L. under short-term waterlogging. J Bio Environ Control 18(2):142–147

    Google Scholar 

  • Kumar A, Taylor MA, Mad Arif SA, Davies HV (1996) Potato plants expressing antisense and sense S-adenosylmethionine decarboxylase (SAMDC) transgenes show altered levels of polyamines and ethylene: antisense plants display abnormal phenotypes. Plant J 9(2):147–158

    Article  CAS  Google Scholar 

  • Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 144:218–231

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Le Provost G, Sulmon C, Frigerio JM, Bode′ne`s C, Kremer A, Plomion C (2012) Role of waterlogging-responsive genes in shaping interspecific differentiation between two sympatric oak species. Tree Physiol 32:119–134

    Article  PubMed  Google Scholar 

  • Liu F, Vantoai T, Moy L, Bock G, Linford LD, Quackenbush J (2005) Global transcription profiling reveals novel insights into hypoxic response in Arabidopsis. Plant Physiol 137:1115–1129

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Manzur ME, Grimoldi AA, Insausti P, Striker GG (2009) Escape from water or remain quiescent? Lotus tenuis changes its strategy depending on depth of submergence. Ann Bot 104:1163–1169

    Article  CAS  PubMed  Google Scholar 

  • McFarlane NM, Ciavarella TA, Smith K (2003) The effect of waterlogging on growth, photosynthesis and biomass allocation in perennial ryegrass (Lolium perenne L.) genotypes with contrasting root development. J Agric Sci 141:241–248

    Article  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Method 5(7):621–628

    Article  CAS  Google Scholar 

  • Parent C, Capelli N, Berger A, Crèvecoeur M, Dat JF (2008) An overview of plant responses to soil waterlogging. Plant Stress 2:20–27

    Google Scholar 

  • Prakash TR, Swamy PM, Suguna P, Reddanna P (1990) Characterization and behaviour of 15-lipoxygenase during peanut cotyledonary senescence. Biochem Biophys Res Commun 30(172):462–470

    Article  Google Scholar 

  • Roxas VP, Lodhi SA, Garrett DK, Mahan JR, Allen RD (2000) Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physiol 41(11):1229–1234

    Article  CAS  PubMed  Google Scholar 

  • Shiu OY, Oetiker JH, Yip WK, Yang SF (1998) The promoter of LE-ACS7, an early flooding-induced 1-aminocyclopropane-1-carboxylate synthase gene of the tomato, is tagged by a Sol3 transposon. Proc Natl Acad Sci USA 95:10334–10339

    Article  CAS  PubMed  Google Scholar 

  • Subbaiah CC, Sachs MM (2003) Molecular and cellular adaptations of maize to flooding stress. Ann Bot 90:119–127

    Article  Google Scholar 

  • Trought MCT, Drew MC (1980) The development of waterlogging damage in wheat seedlings (Triticum aestivum L.) I. Shoot and root growth in relation to changes in concentration of dissolved gases and solutes in the soil solutions. Plant Soil 54:77–94

    Article  CAS  Google Scholar 

  • van den Berg AK, Perkins TD (2004) Evaluation of a portable chlorophyll meter to estimate chlorophyll and nitrogen contents in sugar maple (Acer saccharum Marsh.) leaves. For Ecol Manage 200:113–117

    Article  Google Scholar 

  • Wang L, Zhang Y, Qi X, Li D, Wei W, Zhang X (2012) Global gene expression responses to waterlogging in roots of sesame (Sesamum indicum L.). Acta Physiol Plant 34:2241–2249

    Article  Google Scholar 

  • Yordanova RY, Popova LP (2001) Photosynthetic response of barley plants to soil flooding. Photosynthetica 39:515–520

    Article  Google Scholar 

  • Yordanova R, Christov K, Popova L (2004) Antioxidative enzymes in barley plants subjected to soil flooding. Environ Exp Bot 51:93–101

    Article  CAS  Google Scholar 

  • Zhang J, Davies WJ (1987) ABA in roots and leaves of flooded pea plants. J Exp Bot 38:649–659

    Article  CAS  Google Scholar 

  • Zhou W, Zhao D, Lin X (1997) Effects of waterlogging on nitrogen accumulation and alleviation of waterlogging damage by application of nitrogen fertilizer and mixtalol in winter rape (Brassica napus L.). J Plant Growth Regul 16:47–53

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by a grant from Rural Development Administration (Project No: PJ008761). The authors would like to thank Song-Hee Bae for her invaluable contributions to this research.

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Correspondence to Yong-Hwa Lee.

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Communicated by Y.-I. Park.

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Lee, YH., Kim, KS., Jang, YS. et al. Global gene expression responses to waterlogging in leaves of rape seedlings. Plant Cell Rep 33, 289–299 (2014). https://doi.org/10.1007/s00299-013-1529-8

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  • DOI: https://doi.org/10.1007/s00299-013-1529-8

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