Full paper

You have full text access to this OnlineOpen article

Molecular characterization of the submergence response of the Arabidopsis thaliana ecotype Columbia

  1. Seung Cho Lee1,
  2. Angelika Mustroph2,
  3. Rashmi Sasidharan3,4,
  4. Divya Vashisht3,4,
  5. Ole Pedersen5,
  6. Teruko Oosumi1,
  7. Laurentius A.C.J. Voesenek3,4,
  8. Julia Bailey-Serres1

Article first published online: 13 JAN 2011

DOI: 10.1111/j.1469-8137.2010.03590.x

Issue

New Phytologist

New Phytologist

Special Issue: Plant anaerobiosis

Volume 190, Issue 2, pages 457–471, April 2011

Additional Information

How to Cite

Lee, S. C., Mustroph, A., Sasidharan, R., Vashisht, D., Pedersen, O., Oosumi, T., Voesenek, L. A.C.J. and Bailey-Serres, J. (2011), Molecular characterization of the submergence response of the Arabidopsis thaliana ecotype Columbia. New Phytologist, 190: 457–471. doi: 10.1111/j.1469-8137.2010.03590.x

Author Information

  1. 1

    Department of Botany and Plant Sciences, University of California, Riverside, CA 92521, USA

  2. 2

    Department of Plant Physiology, University of Bayreuth, Universitaetsstrasse 30, 95440 Bayreuth, Germany

  3. 3

    Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, the Netherlands

  4. 4

    Centre for Biosystems Genomics, 6708 PB Wageningen, the Netherlands

  5. 5

    Freshwater Biological Laboratory, Department of Biology, University of Copenhagen, Helsingørsgade 51, DK-3400 Hillerød, Denmark

*Author for correspondence: Julia Bailey-Serres Tel: +1 951 827 3738 Email: serres@ucr.edu

Publication History

  1. Issue published online: 28 MAR 2011
  2. Article first published online: 13 JAN 2011
  3. Received: 19 September 2010, Accepted: 8 November 2010

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article with Supporting Information (HTML) Get PDF (1268K)

References

  • Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R et al. 2003. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653–657.
  • Baena-González E. 2010. Energy signaling in the regulation of gene expression during stress. Molecular Plant 3: 300–313.
  • Baena-González E, Rolland F, Thevelein JM, Sheen J. 2007. A central integrator of transcription networks in plant stress and energy signalling. Nature 448: 938–942.
  • Bailey-Serres J, Voesenek LACJ. 2008. Flooding stress: acclimations and genetic diversity. Annual Review of Plant Biology 59: 313–339.
  • Bailey-Serres J, Voesenek LACJ. 2010. Life in the balance: a signaling network controlling survival of flooding. Current Opinion in Plant Biology 13: 489–494.
  • Branco-Price C, Kaiser KA, Jang CJ, Larive CK, Bailey-Serres J. 2008. Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. Plant Journal 56: 743–755.
    Direct Link:
  • Branco-Price C, Kawaguchi R, Ferriera R, Bailey-Serres J. 2005. Genome-wide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation. Annals of Botany 96: 647–660.
  • Chen X, Pierik R, Peeters AJM, Poorter H, Visser EJ, Huber H, de Kroon H, Voesenek LACJ. 2010. Endogenous ABA as a key switch for natural variation in flooding-induced shoot elongation. Plant Physiology 154: 969–977.
  • Christianson JA, Llewellyn DJ, Dennis ES, Wilson IW. 2010a. Global gene expression responses to waterlogging in roots and leaves of cotton (Gossypium hirsutum L.). Plant & Cell Physiology 51: 21–37.
  • Christianson JA, Llewellyn DJ, Dennis ES, Wilson IW. 2010b. Comparisons of early transcriptome responses to low-oxygen environments in three dicotyledonous plant species. Plant Signaling & Behavior 5: 1–4.
  • Colmer TD, Flowers TJ. 2008. Flooding tolerance in halophytes. New Phytologist 179: 964–974.
    Direct Link:
  • Colmer TD, Voesenek LACJ. 2009. Flooding tolerance: suites of plant traits in variable environments. Functional Plant Biology 36: 665–681.
  • Cosgrove DJ. 2005. Growth of the plant cell wall. Nature Reviews Molecular Cell Biology 6: 850–861.
  • 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. Annals of Botany 103: 269–280.
  • Dubini A, Mus F, Seibert M, Grossman AR, Posewitz MC. 2009. Flexibility in anaerobic metabolism as revealed in a mutant of Chlamydomonas reinhardtii lacking hydrogenase activity. Journal of Biological Chemistry 284: 7201–7213.
  • Fukao T, Bailey-Serres J. 2008. Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice. Proceedings of the National Academy of Sciences, USA 105: 16814–16819.
  • Fukao T, Harris T, Bailey-Serres J. 2009. Evolutionary analysis of the Sub1 gene cluster that confers submergence tolerance to domesticated rice. Annals of Botany 103: 143–150.
  • Fukao T, Xu K, Ronald PC, Bailey-Serres J. 2006. A variable cluster of ethylene response factor–like genes regulates metabolic and developmental acclimation responses to submergence in rice. The Plant Cell 18: 2021–2034.
  • Gautier L, Cope L, Bolstad BM, Irizarry RA. 2004. Affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20: 307–315.
  • Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biology 5: R80.
  • Gibon Y, Bläsing OE, Palacios-Rojas N, Pankovic D, Hendriks JH, Fisahn J, Höhne M, Günther M, Stitt M. 2004. Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. Plant Journal 39: 847–862.
    Direct Link:
  • Graf A, Schlereth A, Stitt M, Smith AM. 2010. Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proceedings of the National Academy of Sciences, USA 107: 9458–9463.
  • Hattori Y, Nagai K, Furukawa S, Song XJ, Kawano R, Sakakibara H, Wu J, Matsumoto T, Yoshimura A, Kitano H et al. 2009. The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460: 1026–1030.
  • Hinz M, Wilson IW, Yang J, Buerstenbinder K, Llewellyn D, Dennis ES, Sauter M, Dolferus R. 2010. Arabidopsis RAP2.2: an ethylene response transcription factor that is important for hypoxia survival. Plant Physiology 153: 757–772.
  • Horan K, Jang C, Bailey-Serres J, Mittler R, Shelton C, Harper JF, Zhu JK, Cushman JC, Gollery M, Girke T. 2008. Annotating genes of known and unknown function by large-scale coexpression analysis. Plant Physiology 147: 41–57.
  • Huang S, Colmer TD, Millar AH. 2008. Does anoxia tolerance involve altering the energy currency towards PPi? Trends in Plant Science 13: 221–227.
  • Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. 2003. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Research 31: e15.
  • Jung KH, Seo YS, Walia H, Cao P, Fukao T, Canlas PE, Amonpant F, Bailey-Serres J, Ronald PC. 2010. The submergence tolerance regulator Sub1A mediates stress-responsive expression of AP2/ERF transcription factors. Plant Physiology 152: 1674–1692.
  • Kende H, Bradford KJ, Brummell DA, Cho HT, Cosgrove DJ, Fleming AJ, Gehring C, Lee Y, McQueen-Mason S, Rose JKC et al. 2004. Nomenclature for members of the expansin superfamily of genes and proteins. Plant Molecular Biology 55: 311–314.
  • 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. The Plant Cell 14: 2481–2494.
  • 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 Physiology 149: 461–473.
  • 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 Physiology 144: 218–231.
  • Lee KW, Chen PW, Lu CA, Chen S, Ho TH, Yu SM. 2009. Coordinated responses to oxygen and sugar deficiency allow rice seedlings to tolerate flooding. Science Signaling 2: ra61.
  • Licausi F, van Dongen JT, Giuntoli B, Novi G, Santaniello A, Geigenberger P, Perata P. 2010. HRE1 and HRE2, two hypoxia-inducible ethylene response factors, affect anaerobic responses in Arabidopsis thaliana. Plant Journal 62: 302–315.
    Direct Link:
  • Liu F, Vantoai T, Moy LP, Bock G, Linford LD, Quackenbush J. 2005. Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis. Plant Physiology 137: 1115–1129.
  • Liu WM, Mei R, Di X, Ryder TB, Hubbell E, Dee S, Webster TA, Harrington CA, Ho MH, Baid J et al. 2002. Analysis of high density expression microarrays with signed-rank call algorithms. Bioinformatics 18: 1593–1599.
  • 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 Physiology 137: 1130–1138.
  • Millenaar FF, Cox MC, van Berkel YE, Welschen RA, Pierik R, Voesenek LACJ, Peeters AJM. 2005. Ethylene-induced differential growth of petioles in Arabidopsis. Analyzing natural variation, response kinetics, and regulation. Plant Physiology 137: 998–1008.
  • Mommer L, Pedersen O, Visser EJW. 2004. Acclimation of a terrestrial plant to submergence facilitates gas exchange: a microelectrode study. Plant, Cell & Environment 27: 1281–1287.
    Direct Link:
  • Mommer L, Wolters-Arts M, Andersen C, Visser E, Pedersen O. 2007. Submergence-induced leaf acclimation in terrestrial species varying in flooding tolerance. New Phytologist 176: 337–345.
    Direct Link:
  • 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 highlights conserved and plant-specific responses. Plant Physiology 152: 1484–1500.
  • Mustroph A, Zanetti ME, Jang CJ, Holtan HE, Repetti PP, Galbraith DW, Girke T, Bailey-Serres J. 2009. Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis. Proceedings of the National Academy of Sciences, USA 106: 18843–18848.
  • 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 Physiology 151: 306–322.
  • Paul AL, Ferl RJ. 1991. In vivo footprinting reveals unique cis-elements and different modes of hypoxic induction in maize Adh1 and Adh2. The Plant Cell 3: 159–168.
  • Pérez-Rodríguez P, Riaño-Pachón DM, Corrêa LG, Rensing SA, Kersten B, Mueller-Roeber B. 2010. PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Research 38: D822–D827.
  • Pierik R, Millenaar FF, Peeters AJ, Voesenek LACJ. 2005. New perspectives in flooding research: the use of shade avoidance and Arabidopsis thaliana. Annals of Botany 96: 533–540.
  • Qiao H, Chang KN, Yazaki J, Ecker JR. 2009. Interplay between ethylene, ETP1/ETP2 F-box proteins, and degradation of EIN2 triggers ethylene responses in Arabidopsis. Genes and Development 23: 512–521.
  • Ramonell KM, Kuang A, Porterfield DM, Crispi ML, Xiao Y, McClure G, Musgrave ME. 2001. Influence of atmospheric oxygen on leaf structure and starch deposition in Arabidopsis thaliana. Plant, Cell & Environment 24: 419–428.
    Direct Link:
  • Revsbech NP. 1989. An oxygen microsensor with a guard cathode. Limnology and Oceanography 34: 474–478.
  • Rocha M, Licausi F, Araújo WL, Nunes-Nesi A, Sodek L, Fernie AR, van Dongen JT. 2010. Glycolysis and the TCA-cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiology 152: 1501–1513.
  • Rose JKC, Braam J, Fry SC, Nishitani K. 2002. The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant & Cell Physiology 43: 1421–1435.
  • Sasidharan R, Chinnappa CC, Staal M, Elzenga JT, Yokoyama R, Nishitani K, Voesenek LACJ, Pierik R. 2010. Light quality-mediated petiole elongation in Arabidopsis during shade avoidance involves cell wall modification by XTHs. Plant Physiology 154: 978–990.
  • Smith AM, Stitt M. 2007. Coordination of carbon supply and plant growth. Plant Cell and Environment 30: 1126–1149.
    Direct Link:
  • Smyth GK. 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Statistical Applications in Genetics and Molecular Biology 3: Article 3.
  • Stepanova AN, Yun J, Likhacheva AV, Alonso JM. 2007. Multilevel interactions between ethylene and auxin in Arabidopsis roots. The Plant Cell 19: 2169–2185.
  • Tadege M, Dupuis I, Kuhlemeier C. 1999. Ethanolic fermentation: new functions for an old pathway. Trends in Plant Science 4: 320–325.
  • Usadel B, Bläsing OE, Gibon Y, Retzlaff K, Höhne M, Günther M, Stitt M. 2008. Global transcript levels respond to small changes of the carbon status during progressive exhaustion of carbohydrates in Arabidopsis rosettes. Plant Physiology 146: 1834–1861.
  • Vashisht D, Hesselink A, Pierik R, Ammerlaan JMH, Bailey-Serres J, Visser EJW, Pedersen O, van Zanten M, Vreugdenhil D, Jamar DCL et al. 2011. Natural variation of submergence tolerance among Arabidopsis thaliana accessions. New Phytologist 190: 299–310.
    Direct Link:
  • Voesenek LACJ, Bailey-Serres J. 2009. Genetics of high-rise rice. Nature 460: 959–960.
  • Voesenek LACJ, Colmer TD, Pierik R, Millenaar FF, Peeters AJM. 2006. How plants cope with complete submergence. New Phytologist 170: 213–226.
    Direct Link:
  • Vreeburg RAM, Benschop JJ, Peeters AJM, Colmer TD, Ammerlaan AHM, Staal M, Elzenga TM, Staals RHJ, Darley CP, McQueen-Mason SJ et al. 2005. Ethylene regulates fast apoplastic acidification and expansin A transcription during submergence-induced petiole elongation in Rumex palustris. Plant Journal 43: 597–610.
    Direct Link:
  • 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: 705–708.
  • Zabalza A, van Dongen JT, Froehlich A, Oliver SN, Faix B, Gupta KJ, Schmälzlin E, Igal M, Orcaray L, Royuela M et al. 2009. Regulation of respiration and fermentation to control the plant internal oxygen concentration. Plant Physiology 149: 1087–1098.
View Full Article with Supporting Information (HTML) Get PDF (1268K)