Home LiteratureArticle Details
PMID: 24077074 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Root transcript profiling of two Rorippa species reveals gene clusters associated with extreme submergence tolerance.

Plant physiology ·Vol. 163 ·No. 3 ·2013-11-00 ·Pages 1277-92

Sasidharan R, Mustroph A, Boonman A, Akman M, Ammerlaan AM, Breit T, Schranz ME, Voesenek LA, van Tienderen PH

Abstract

Complete submergence represses photosynthesis and aerobic respiration, causing rapid mortality in most terrestrial plants. However, some plants have evolved traits allowing them to survive prolonged flooding, such as species of the genus Rorippa, close relatives of Arabidopsis (Arabidopsis thaliana). We studied plant survival, changes in carbohydrate and metabolite concentrations, and transcriptome responses to submergence of two species, Rorippa sylvestris and Rorippa amphibia. We exploited the close relationship between Rorippa species and the model species Arabidopsis by using Arabidopsis GeneChip microarrays for whole-genome transcript profiling of roots of young plants exposed to a 24-h submergence treatment or air. A probe mask was used based on hybridization of genomic DNA of both species to the arrays, so that weak probe signals due to Rorippa species/Arabidopsis mismatches were removed. Furthermore, we compared Rorippa species microarray results with those obtained for roots of submerged Arabidopsis plants. Both Rorippa species could tolerate deep submergence, with R. sylvestris surviving much longer than R. amphibia. Submergence resulted in the induction of genes involved in glycolysis and fermentation and the repression of many energy-consuming pathways, similar to the low-oxygen and submergence response of Arabidopsis and rice (Oryza sativa). The qualitative responses of both Rorippa species to submergence appeared roughly similar but differed quantitatively. Notably, glycolysis and fermentation genes and a gene encoding sucrose synthase were more strongly induced in the less tolerant R. amphibia than in R. sylvestris. A comparison with Arabidopsis microarray studies on submerged roots revealed some interesting differences and potential tolerance-related genes in Rorippa species.

MeSH Terms
Adaptation, Physiological/genetics,physiology Arabidopsis/genetics,metabolism Floods Fructose/metabolism Gene Expression Regulation, Plant Gene Ontology Genes, Plant/genetics Glucose/metabolism Glycolysis/genetics Molecular Sequence Data Multigene Family Oligonucleotide Array Sequence Analysis Photosynthesis/genetics Plant Proteins/genetics,metabolism Plant Roots/genetics,metabolism Reverse Transcriptase Polymerase Chain Reaction Rorippa/classification,genetics,metabolism Species Specificity Starch/metabolism Sucrose/metabolism Transcriptome Water/physiology
Chemicals
Plant Proteins Water Fructose Sucrose Starch Glucose
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Sasidharan Rashmi
Plant Ecophysiology, Institute for Environmental Biology, Utrecht University 3584CH, Utrecht, The Netherlands.
Mustroph Angelika
Boonman Alex
Akman Melis
Ammerlaan Ankie M H
Breit Timo
Schranz M Eric
Voesenek Laurentius A C J
van Tienderen Peter H
References (61)
61 references, click to expand
  1. Transcript and metabolite profiling of the adaptive response to mild decreases in oxygen concentration in the roots of arabidopsis plants.
    Ann Bot. 2009 Jan;103(2):269-80 PMID: 18660497
  2. Bioconductor: open software development for computational biology and bioinformatics.
    Genome Biol. 2004;5(10):R80 PMID: 15461798
  3. Low levels of pyrophosphate in transgenic potato plants expressing E. coli pyrophosphatase lead to decreased vitality under oxygen deficiency.
    Ann Bot. 2005 Sep;96(4):717-26 PMID: 16027130
  4. OXYGEN DEFICIENCY AND ROOT METABOLISM: Injury and Acclimation Under Hypoxia and Anoxia.
    Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:223-250 PMID: 15012263
  5. Flooding stress: acclimations and genetic diversity.
    Annu Rev Plant Biol. 2008;59:313-39 PMID: 18444902
  6. Natural variation of submergence tolerance among Arabidopsis thaliana accessions.
    New Phytol. 2011 Apr;190(2):299-310 PMID: 21108648
  7. Comparisons of early transcriptome responses to low-oxygen environments in three dicotyledonous plant species.
    Plant Signal Behav. 2010 Aug;5(8):1006-9 PMID: 20724824
  8. Fermentation metabolism in roots of wheat seedlings after hypoxic pre-treatment in different anoxic incubation systems.
    J Plant Physiol. 2007 Apr;164(4):394-407 PMID: 16616971
  9. A central integrator of transcription networks in plant stress and energy signalling.
    Nature. 2007 Aug 23;448(7156):938-42 PMID: 17671505
  10. Expression profile analysis of the low-oxygen response in Arabidopsis root cultures.
    Plant Cell. 2002 Oct;14(10):2481-94 PMID: 12368499
  11. Comparative genomics in the Brassicaceae: a family-wide perspective.
    Curr Opin Plant Biol. 2007 Apr;10(2):168-75 PMID: 17300984
  12. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository.
    Nucleic Acids Res. 2002 Jan 1;30(1):207-10 PMID: 11752295
  13. Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization.
    Nature. 2011 Oct 23;479(7373):419-22 PMID: 22020282
  14. Transcript profiling of the anoxic rice coleoptile.
    Plant Physiol. 2007 May;144(1):218-31 PMID: 17369434
  15. Cross-kingdom comparison of transcriptomic adjustments to low-oxygen stress highlights conserved and plant-specific responses.
    Plant Physiol. 2010 Mar;152(3):1484-500 PMID: 20097791
  16. Introgressive hybridization in Rorippa (Brassicaceae): gene flow and its consequences in natural and anthropogenic habitats.
    Mol Ecol. 2001 Aug;10(8):2013-22 PMID: 11555244
  17. Sucrose synthase activity does not restrict glycolysis in roots of transgenic potato plants under hypoxic conditions
    Planta. 1999 Nov;210(1):41-9 PMID: 10592031
  18. Ethylene--and oxygen signalling--drive plant survival during flooding.
    Plant Biol (Stuttg). 2013 May;15(3):426-35 PMID: 23574304
  19. Does anoxia tolerance involve altering the energy currency towards PPi?
    Trends Plant Sci. 2008 May;13(5):221-7 PMID: 18439868
  20. A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice.
    Plant Cell. 2006 Aug;18(8):2021-34 PMID: 16816135
  21. Summaries of Affymetrix GeneChip probe level data.
    Nucleic Acids Res. 2003 Feb 15;31(4):e15 PMID: 12582260
  22. Cell identity mediates the response of Arabidopsis roots to abiotic stress.
    Science. 2008 May 16;320(5878):942-5 PMID: 18436742
  23. GO::TermFinder--open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes.
    Bioinformatics. 2004 Dec 12;20(18):3710-5 PMID: 15297299
  24. A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes.
    New Phytol. 2006;170(2):239-60 PMID: 16608451
  25. Using genomic DNA-based probe-selection to improve the sensitivity of high-density oligonucleotide arrays when applied to heterologous species.
    Plant Methods. 2005 Nov 09;1(1):10 PMID: 16280083
  26. Molecular characterization of the submergence response of the Arabidopsis thaliana ecotype Columbia.
    New Phytol. 2011 Apr;190(2):457-71 PMID: 21231933
  27. Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis.
    Plant Physiol. 2005 Mar;137(3):1115-29 PMID: 15734912
  28. Aquatic adventitious roots of the wetland plant Meionectes brownii can photosynthesize: implications for root function during flooding.
    New Phytol. 2011 Apr;190(2):311-9 PMID: 21062289
  29. Organ-specific analysis of the anaerobic primary metabolism in rice and wheat seedlings. I: Dark ethanol production is dominated by the shoots.
    Planta. 2006 Dec;225(1):103-14 PMID: 16845530
  30. Insights into hypoxic systemic responses based on analyses of transcriptional regulation in Arabidopsis.
    PLoS One. 2011;6(12):e28888 PMID: 22194941
  31. Arabidopsis thaliana mutant that develops as a light-grown plant in the absence of light.
    Cell. 1989 Sep 8;58(5):991-9 PMID: 2776216
  32. Structure and expression profile of the sucrose synthase multigene family in Arabidopsis.
    J Exp Bot. 2004 Feb;55(396):397-409 PMID: 14739263
  33. Tolerance of crop plants to oxygen deficiency stress: fermentative activity and photosynthetic capacity of entire seedlings under hypoxia and anoxia.
    Physiol Plant. 2003 Apr;117(4):508-520 PMID: 12675741
  34. Comparative analysis between plant species of transcriptional and metabolic responses to hypoxia.
    New Phytol. 2011 Apr;190(2):472-87 PMID: 21244431
  35. A genome-wide analysis of the effects of sucrose on gene expression in Arabidopsis seedlings under anoxia.
    Plant Physiol. 2005 Mar;137(3):1130-8 PMID: 15734908
  36. Enhanced low oxygen survival in Arabidopsis through increased metabolic flux in the fermentative pathway.
    Plant Physiol. 2003 Jul;132(3):1292-302 PMID: 12857811
  37. How plants cope with complete submergence.
    New Phytol. 2006;170(2):213-26 PMID: 16608449
  38. Annotating genes of known and unknown function by large-scale coexpression analysis.
    Plant Physiol. 2008 May;147(1):41-57 PMID: 18354039
  39. Different flooding responses in Rorippa amphibia and Rorippa sylvestris, and their modes of expression in F1 hybrids.
    New Phytol. 2008;180(1):229-239 PMID: 18631292
  40. Microarray challenges in ecology.
    Trends Ecol Evol. 2007 May;22(5):273-9 PMID: 17296243
  41. Metabolic repression of transcription in higher plants.
    Plant Cell. 1990 Oct;2(10):1027-38 PMID: 2136626
  42. Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia.
    Plant Physiol. 2009 Jan;149(1):461-73 PMID: 19005089
  43. HRE1 and HRE2, two hypoxia-inducible ethylene response factors, affect anaerobic responses in Arabidopsis thaliana.
    Plant J. 2010 Apr;62(2):302-15 PMID: 20113439
  44. The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl.
    Genes Dev. 1997 Nov 15;11(22):2983-95 PMID: 9367981
  45. Genome-wide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation.
    Ann Bot. 2005 Sep;96(4):647-60 PMID: 16081496
  46. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.
    Methods. 2001 Dec;25(4):402-8 PMID: 11846609
  47. Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana.
    Plant J. 2008 Dec;56(5):743-55 PMID: 18665916
  48. Stimulation of glycolysis in anaerobic elongation of pondweed (Potamogeton distinctus) turions.
    J Exp Bot. 2002 Sep;53(376):1847-56 PMID: 12177122
  49. Analysis of the sucrose synthase gene family in Arabidopsis.
    Plant J. 2007 Mar;49(5):810-28 PMID: 17257168
  50. Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis.
    Proc Natl Acad Sci U S A. 2009 Nov 3;106(44):18843-8 PMID: 19843695
  51. Evidence of neutral transcriptome evolution in plants.
    New Phytol. 2008;180(3):587-593 PMID: 18801004
  52. The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water.
    Nature. 2009 Aug 20;460(7258):1026-30 PMID: 19693083
  53. Arabidopsis roots and shoots have different mechanisms for hypoxic stress tolerance.
    Plant Physiol. 1999 Jan;119(1):57-64 PMID: 9880346
  54. Life in the balance: a signaling network controlling survival of flooding.
    Curr Opin Plant Biol. 2010 Oct;13(5):489-94 PMID: 20813578
  55. Wait or escape? Contrasting submergence tolerance strategies of Rorippa amphibia, Rorippa sylvestris and their hybrid.
    Ann Bot. 2012 Jun;109(7):1263-76 PMID: 22499857
  56. Linear models and empirical bayes methods for assessing differential expression in microarray experiments.
    Stat Appl Genet Mol Biol. 2004;3:Article3 PMID: 16646809
  57. A discussion of statistical methods for design and analysis of microarray experiments for plant scientists.
    Plant Cell. 2006 Sep;18(9):2112-21 PMID: 16968907
  58. Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants.
    Nature. 2011 Oct 23;479(7373):415-8 PMID: 22020279
  59. The submergence tolerance regulator Sub1A mediates stress-responsive expression of AP2/ERF transcription factors.
    Plant Physiol. 2010 Mar;152(3):1674-92 PMID: 20107022
  60. Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice.
    Nature. 2006 Aug 10;442(7103):705-8 PMID: 16900200
  61. Comparison of gene expression in segregating families identifies genes and genomic regions involved in a novel adaptation, zinc hyperaccumulation.
    Mol Ecol. 2006 Sep;15(10):3045-59 PMID: 16911220
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
1532-2548
Published
2013-11-00
Epub
2013-00-27
Pages
1277-92
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC3813650
Subset
IM
Databases
GENBANK
JQ582800, JQ582801, KF042825, KF042826, KF042827, KF042828, KF042829, KF042831, KF042832, KF042833, KF042834, KF042835, KF042836, KF042837, KF042838, KF042839, KF042842, KF042843, KF042844, KF042845, KF042846, KF042847, KF042848, KF042850, KF042851
GEO
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com