Physiological and transcriptomic characterization of submergence and reoxygenation responses in soybean seedlings

Plant Cell and Environment

Volumn 37, Issue 10, 2014, Pages 2350-2365

  Tamang, Bishal G ^a   Magliozzi, Joseph O ^a   Maroof, M A Saghai ^a   Fukao, Takeshi ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

Affymetrix microarray; Flooding; Genome scale gene expression analysis; Glycine max; Group VII Ethylene Responsive Factors

Indexed keywords

GLYCINE MAX;

ADENOSINE TRIPHOSPHATE; CARBOHYDRATE; OXYGEN; PLANT RNA; TRANSCRIPTOME; WATER;

ADAPTATION; ANTIBODY SPECIFICITY; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; LIPID PEROXIDATION; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY; PLANT; PLANT ROOT; SEEDLING; SIGNAL TRANSDUCTION; SOYBEAN;

ADAPTATION, PHYSIOLOGICAL; ADENOSINE TRIPHOSPHATE; CARBOHYDRATES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; LIPID PEROXIDATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN SPECIFICITY; OXIDATIVE STRESS; OXYGEN; PLANT ROOTS; PLANT SHOOTS; RNA, PLANT; SEEDLING; SIGNAL TRANSDUCTION; SOYBEANS; TRANSCRIPTOME; WATER;

EID: 84908226731     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12277     Document Type: Article

References (74)

1. Andrews D.L., Drew M.C., Johson J.R. & Cobb B.G. (1994) The response of maize seedlings of different ages to hypoxic and anoxic stress. Plant Physiology 105, 53-60.
2. Bacanamwo M. & Purcell L.C. (1999) Soybean root morphological and anatomical traits associated with acclimation to flooding. Crop Science 39, 143-149.
3. Bailey-Serres J. & Voesenek L.A.C.J. (2010) Life in the balance: a signaling network controlling survival of flooding. Currrent Opinion in Plant Biology 13, 489-494.
4. Bailey-Serres J., Fukao T., Gibbs D.J., Holdsworth M.J., Lee S.C., Licausi F., .. van Dongen J.T. (2012a) Making sense of low oxygen sensing. Trends in Plant Science 17, 129-138.
5. Bailey-Serres J., Lee S.C. & Brinton E. (2012b) Waterproofing crops: effective flooding survival strategies. Plant Physiology 160, 1698-1709.
6. Baxter-Burrell A., Yang Z., Springer P.S. & Bailey-Serres J. (2002) RopGAP4-dependent Rop GTPase rheostat control of Arabidopsis oxygen deprivation tolerance. Science 296, 2026-2028.
7. Branco-Price C., Kaiser K.A., Jang C.J., Larive C.K. & Bailey-Serres J. (2008) Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. The Plant Journal 56, 743-755.
8. Carvalho B.S. & Irizarry R.A. (2010) A framework for oligonucleotide microarray preprocessing. Bioinformatics (Oxford, England) 26, 2363-2367.
9. Christianson J.A., Llewellyn D.J., Dennis E.S. & Wilson I.W. (2010) Global gene expression responses to waterlogging in roots and leaves of cotton (Gossypium hirsutum L.). Plant and Cell Physiology 51, 21-37.
10. Colmer T.D., Winkel A. & Pedersen O. (2011) A perspective on underwater photosynthesis in submerged terrestrial wetland plants. AoB Plants 2011, plr030.
11. Ella E.S., Kawano N. & Ito O. (2003) Importance of active oxygen-scavenging system in the recovery of rice seedlings after submergence. Plant Science 165, 85-93.
12. FAOSTAT. (2012) Retrieved from http://faostat.fao.org.
13. Fukao T. & Bailey-Serres J. (2004) Plant responses to hypoxia - is survival a balancing act? Trends in Plant Sciences 9, 449-456.
14. 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 of the United States of America 105, 16814-16819.
15. Fukao T. & Xiong L. (2013) Genetic mechanisms conferring adaptation to submergence and drought in rice: simple or complex? Current Opinion in Plant Biology 16, 196-204.
16. Fukao T., Kennedy R.A., Yamasue Y. & Rumpho M.E. (2003) Genetic and biochemical analysis of anaerobically-induced enzymes during seed germination of Echinochloa crus-galli varieties tolerant and intolerant to anoxia. Journal of Experimental Botany 386, 1421-1429.
17. Fukao T., Xu K., Ronald P.C. & 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.
18. Fukao T., Yeung E. & Bailey-Serres J. (2011) The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice. The Plant Cell 23, 412-427.
19. Fukao T., Yeung E. & Bailey-Serres J. (2012) The submergence tolerance gene SUB1A delays leaf senescence under prolonged darkness through hormonal regulation in rice. Plant Physiology 160, 1795-1807.
20. Gentleman R.C., Carey V.J., Bates D.M., Bolstad B., Dettling M., Dudoit S., .. Zhang J. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biology 5, R80.
21. Gibbs D.J., Lee S.C., Isa N.M., Gramuglia S., Fukao T., Bassel G.W., .. Holdsworth M.J. (2011) Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature 479, 415-418.
22. Gladish D.K., 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. Annals of Botany 97, 895-902.
23. Hashiguchi A., Sakata K. & Komatsu S. (2009) Proteome analysis of early-stage soybean seedlings under flooding stress. Journal of Proteome Research 8, 2058-2069.
24. Hattori Y., Nagai K., Furukawa S., Song X.J., Kawano R., Sakakibara H., .. Ashikari M. (2009) The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460, 1026-1030.
25. Hinz M., Wilson I.W., Yang J., Buerstenbinder K., Llewellyn D., Dennis E.S., .. Dolferus R. (2010) Arabidopsis RAP2.2: an ethylene response transcription factor that is important for hypoxia survival. Plant Physiology 153, 757-772.
26. Hirayama T. & Shinozaki K. (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. The Plant Journal 61, 1041-1052.
27. Hodges D.M., DeLong J.M., Forney C.F. & Prange R.K. (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207, 604-611.
28. Huynh L.N., Vantoai T., Streeter J. & Banowetz G. (2005) Regulation of flooding tolerance of SAG12:ipt Arabidopsis plants by cytokinin. Journal of Experimental Botany 56, 1397-1407.
29. Ismond K.P., Dolferus R., De Pauw M., Dennis E.S. & Good A.G. (2003) Enhanced low oxygen survival in Arabidopsis through increased metabolic flux in the fermentative pathway. Plant Physiology 132, 1292-1302.
30. Johnson J., Cobb B.G. & Drew M.C. (1989) Hypoxic induction of anoxia tolerance in root tips of Zea mays. Plant Physiology 91, 837-841.
31. Kawano N., Ella E., Ito O., Yamauchi Y. & Tanaka K. (2002) Metabolic changes in rice seedlings with different submergence tolerance after desubmergence. Environmental and Experimental Botany 47, 195-203.
32. Koch K.E., Ying Z., Wu Y. & Avigen W.T. (2000) Multiple paths of sugar-sensing and a sugar/oxygen overlap for genes of sucrose and ethanol metabolism. Journal of Experimental Botany 51, 417-427.
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. Journal of Proteome Research 8, 4766-4778.
34. Komatsu S., Deschamps T., Hiraga S., Kato M., Chiba M., Hashiguchi A., .. Yasue H. (2011) Characterization of a novel flooding stress-responsive alcohol dehydrogenase expressed in soybean roots. Plant Molecular Biology 77, 309-322.
35. Kreuzwieser J., Hauberg J., Howell K.A., Carroll A., Rennenberg H., Millar A.H. & Whelan J. (2009) Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiology 149, 461-473.
36. Le D.T., Aldrich D.L., Valliyodan B., Watanabe Y., Ha C.V., Nishiyama R., .. Nguyen H.T. (2012) Evaluation of candidate reference genes for normalization of quantitative RT-PCR in soybean tissues under various abiotic stress conditions. PLoS ONE 7, e46487.
37. Lee S.C., Mustroph A., Sasidharan R., Vashisht D., Pedersen O., Oosumi T., .. Bailey-Serres J. (2011) Molecular characterization of the submergence response of the Arabidopsis thaliana ecotype Columbia. The New Phytologist 190, 457-471.
38. Licausi F., van Dongen J.T., 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. The Plant Journal 62, 302-315.
39. Licausi F., Kosmacz M., Weits D.A., Giuntoli B., Giorgi F.M., Voesenek L.A., .. van Dongen J.T. (2011) Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature 479, 419-422.
40. Linkemer G., Board J.E. & Musgrave M.E. (1998) Waterlogging effects on growth and yield components in late-planted soybean. Crop Science 38, 1576-1584.
41. Livak K.J. & Schmittgen T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods (San Diego, Calif.) 25, 402-408.
42. Manzur M.E., Grimoldi A.A., Insausti P. & Striker G.G. (2009) Escape from water or remain quiescent? Lotus tenuis changes its strategy depending on depth of submergence. Annals of Botany 104, 1163-1169.
43. Mommer L., Pons T.L., Wolters-Arts M., Venema J.H. & Visser E.J. (2005) Submergence-induced morphological, anatomical, and biochemical responses in a terrestrial species affect gas diffusion resistance and photosynthetic performance. Plant Physiology 139, 497-508.
44. Mustroph A., Zanetti M.E., Jang C.J., Holtan H.E., Repetti P.P., Galbraith D.W., .. 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 of the United States of America 106, 18843-18848.
45. Mustroph A., Lee S.C., Oosumi T., Zanetti M.E., Yang H., Ma K., .. 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.
46. Nakano T., Suzuki K., Fujimura T. & Shinshi H. (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiology 140, 411-432.
47. Nakazono M., Tsuji H., Li Y., Saisho D., Arimura S., TsuTsumi N. & Hirai A. (2000) Expression of a gene encoding mitochondrial aldehyde dehydrogenase in rice increases under submerged conditions. Plant Physiology 124, 587-598.
48. 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. Journal of Proteome Research 9, 3989-4002.
49. Nanjo Y., Maruyama K., Yasue H., Yamaguchi-Shinozaki K., Shinozaki K. & Komatsu S. (2011) Transcriptional responses to flooding stress in roots including hypocotyl of soybean seedlings. Plant Molecular Biology 77, 129-144.
50. Nanjo Y., Skultety L., Uvackova L., Klubicova K., Hajduch M. & Komatsu S. (2012) Mass spectrometry-based analysis of proteomic changes in the root tips of flooded soybean seedlings. Journal of Proteome Research 11, 372-385.
51. Nanjo Y., Nakamura T. & Komatsu S. (2013) Identification of indicator proteins associated with flooding injury in soybean seedlings using label-free quantitative proteomics. Journal of Proteome Research 12, 4785-4798.
52. Newman K.D. & VanToai T.T. (1992) Molecular characterization of the soybean alcohol dehydrogenase gene family amplified in vitro by the polymerase chain reaction. Plant Physiology 100, 489-495.
53. Nguyen V.T., Vuong T.D., VanToai T., Lee J.D., Wu X., Mian M.A.R., .. Nguyen H.T. (2012) Mapping of quantitative trait loci associated with resistance to and flooding tolerance in soybean. Crop Science 52, 2481-2493.
54. Peña-Castro J.M., van Zanten M., Lee S.C., Patel M.R., Voesenek L.A.J.C., Fukao T. & Bailey-Serres J. (2011) Expression of rice SUB1A and SUB1C transcription factor in Arabidopsis uncovers flowering inhibition as a submergence tolerance mechanism. The Plant Journal 67, 434-446.
55. Porra R.J. (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophyll a and b. Photosynthesis Research 73, 149-156.
56. Rahman M., Grover A., Peacock W.J., Dennis E.S. & Ellis M.H. (2001) Effects of manipulation of pyruvate decarboxylase and alcohol dehydrogenase levels on the submergence tolerance of rice. Australian Journal of Plant Physiology 28, 1231-1241.
57. Russell D.A., Wong D.M.L. & Sachs M.M. (1990) The anaerobic response of soybean. Plant Physiology 92, 401-407.
58. Schmittgen T.D. & Livak K.J. (2008) Analyzing real-time PCR data by the comparative CT method. Nature Protocols 3, 1101-1108.
59. Schwartz D. (1969) Alcohol dehydrogenase in maize: genetic basis for multiple isozymes. Science 164, 585-586.
60. Shimamura S., Yamamoto R., Nakamura T., Shimada S. & Komatsu S. (2010) Stem hypertrophic lenticels and secondary aerenchyma enable oxygen transport to roots of soybean in flooded soil. Annals of Botany 106, 277-284.
61. Smyth G.K. (2004) Liner models and empirical bayes methods for assessing differential expression in microarray experiments. Statistical Application in Genetics and Molecular Biology 3, Article 3, 1-25.
62. Steffens B., Kovalev A., Gorb S.N. & Sauter M. (2012) Emerging roots alter epidermal cell fate through mechanical and reactive oxygen species signaling. The Plant Cell 24, 3296-3306.
63. Subbaiah C.C. & Sachs M.M. (2003) Molecular and cellular adaptation of maize to flooding stress. Annals of Botany 90, 119-127.
64. 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. Molecular Biology and Evolution 28, 2731-2739.
65. Thimm O., Bläsing O., Gibon Y., Nagel A., Meyer S., Krüger P., .. Stitt M. (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. The Plant Journal 37, 914-939.
66. Thomas A.L., Guerreiro S.M. & Sodek L. (2005) Aerenchyma formation and recovery from hypoxia of the flooded root system of nodulated soybean. Annals of Botany 96, 1191-1198.
67. Tsuji H., Meguro N., Suzuki Y., Tsutsumi N., Hirai A. & Nakazono M. (2003) Induction of mitochondrial aldehyde dehydrogenase by submergence facilitates oxidation of acetaldehyde during re-aeration in rice. FEBS Letters 546, 369-373.
68. Usadel B., Nagel A., Steinhauser D., Gibon Y., Blasing O.E., Redestig H., .. Stitt M. (2006) PageMan: an interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments. BMC Bioinformatics 7, 535.
69. VanToai T.T., Beuerlein J.E., Schmitthenner A.F. & St. Martin S.K. (1994) Genetic variability for flooding tolerance in soybeans. Crop Science 34, 1112-1115.
70. VanToai T.T., St. Martin S.K., Chase K., Boru G., Schnipke V., Schmitthenner A.F. & Lark K.G. (2001) Identification of a QTL associated with tolerance of soybean to soil waterlogging. Crop Science 41, 1247-1252.
71. Vidoz M.L., Loreti E., Mensuali A., Alpi A. & Perata P. (2010) Hormonal interplay during adventitious root formation in flooded tomato plants. The Plant Journal 63, 551-562.
72. Wuebker E.F., Mullen R.E. & Koehler K. (2001) Flooding and temperature effects on soybean germination. Crop Science 41, 1857-1861.
73. Xu K., Xu X., Fukao T., Canlas P., Maghirang-Rodriguez R., Heuer S., .. Mackill D.J. (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442, 705-708.
74. Zeng Y., Wu Y., Avigen W.T. & Koch K.E. (1999) Rapid repression of maize invertases by low oxygen. Invertase/sucrose synthase balance, sugar signaling potential, and seedling survival. Plant Physiology 121, 599-608.