How unique is the low oxygen response? an analysis of the anaerobic response during germination and comparison with abiotic stress in rice and arabidopsis

Frontiers in Plant Science

Volumn 4, Issue OCT, 2013, Pages

  Narsai, Reena ^a   Whelan, James ^b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b LA TROBE UNIVERSITY   (Australia)

Author keywords

Arabidopsis; Low oxygen; Microarrays; Rice; Transcriptomes

Indexed keywords

EID: 84901022592     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00349     Document Type: Article

References (63)

1. Aguirre, J., and Lambeth, J. D. (2010). Nox enzymes from fungus to fly to fish and what they tell us about Nox function in mammals. Free Radic. Biol. Med. 49, 1342-1353. doi: 10.1016/j.freeradbiomed.2010. 07.027.
2. Bailey-Serres, J., and Voesenek, L. A. (2008). Flooding stress: acclimations and genetic diversity. Annu. Rev. Plant Biol. 59, 313-339. doi: 10.1146/annurev.arplant.59. 032607.092752.
3. Baldi, P., and Long, A. D. (2001). A Bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics 17, 509-519. doi: 10.1093/bioinformatics/17.6.509.
4. Banti, V., Giuntoli, B., Gonzali, S., Loreti, E., Magneschi, L., Novi, G., et al. (2013). Low oxygen response mechanisms in green organisms. Int. J. Mol. Sci. 14, 4734-4761. doi: 10.3390/ijms14034734.
5. Banti, V., Loreti, E., Novi, G., Santaniello, A., Alpi, A., and Perata, P. (2008). Heat acclimation and cross-tolerance against anoxia in Arabidopsis. Plant Cell Environ. 31, 1029-1037. doi: 10.1111/j.1365-3040.2008.01816.x
6. Banti, V., Mafessoni, F., Loreti, E., Alpi, A., and Perata, P. (2010). The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiol. 152, 1471-1483. doi: 10.1104/pp.109.149815.
7. Branco-Price, C., Kaiser, K. A., Jang, C. J., Larive, C. K., and Bailey-Serres, J. (2008). Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. Plant J. 56, 743-755. doi: 10.1111/j.1365- 313X.2008.03642.x
8. Catusse, J., Job, C., and Job, D. (2008). Transcriptome- and proteome- wide analyses of seed germination. C.R. Biol. 331, 815-822. doi: 10.1016/j.crvi.2008.07.023.
9. Chen, H., Lai, Z., Shi, J., Xiao, Y., Chen, Z., and Xu, X. (2010). Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biol. 10:281. doi: 10.1186/14712229-10-281.
10. Chen, L., Song, Y., Li, S., Zhang, L., Zou, C., and Yu, D. (2012). The role of WRKY transcription factors in plant abiotic stresses. Biochim. Biophys. Acta 1819, 120-128. doi: 10.1016/j.bbagrm.2011.09.002.
11. Christianson, J. A., Llewellyn, D. J., Dennis, E. S., and Wilson, I. W. (2010). Comparisons of early transcriptome responses to low oxygen environments in three dicotyledonous plant species. Plant Signal. Behav. 5, 1006-1009. doi: 10.4161/psb.5.8.12231.
12. Christianson, J. A., Wilson, I. W., Llewellyn, D. J., and Dennis, E. S. (2009). The low oxygen-induced NAC domain transcription factor ANAC102 affects viability of Arabidopsis seeds following low oxygen treatment. Plant Physiol. 149, 1724-1738. doi: 10.1104/pp.108.131912.
13. Foreman, J., Demidchik, V., Bothwell, J. H., Mylona, P., Miedema, H., Torres, M. A., et al. (2003). Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442-446. doi: 10.1038/nature01485.
14. Fukao, T., Yeung, E., and Bailey-Serres, J. (2011). The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice. Plant Cell 23, 412-427. doi: 10.1105/tpc.110.080325.
15. Gadjev, I., Vanderauwera, S., Gechev, T. S., Laloi, C., Minkov, I. N., Shulaev, V., et al. (2006). Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol. 141, 436-445. doi: 10.1104/pp.106.078717.
16. Gallardo, K., Job, C., Groot, S. P., Puype, M., Demol, H., Vandekerckhove, J., et al. (2002). Proteomics of Arabidopsis seed germination. A comparative study of wild-type and gibberellin-deficient seeds. Plant Physiol. 129, 823-837. doi: 10.1104/pp.002816.
17. Gibbs, D. J., Lee, S. C., Isa, N. M., Gramuglia, S., Fukao, T., Bassel, G.W., et al. (2011). Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature 479, 415-418. doi: 10.1038/nature10534.
18. Gibbs, J., Morrell, S., Valdez, A., Setter, T. L., and Greenway, H. (2000). Regulation of alcoholic fermentation in coleoptiles of two rice cultivars differing in tolerance to anoxia. J. Exp. Bot. 51, 785-796. doi: 10.1093/jexbot/51.345.785.
19. Guo, W., Ward, R. W., and Thomashow, M. F. (1992). Characterization of a cold-regulated wheat gene related to Arabidopsis cor47. Plant Physiol. 100, 915-922. doi: 10.1104/pp.100.2.915.
20. Hebelstrup, K. H., Igamberdiev, A. U., and Hill, R. D. (2007). Metabolic effects of hemoglobin gene expression in plants. Gene 398, 86-93. doi: 10.1016/j.gene. 2007.01.039.
21. Howell, K. A., Cheng, K., Murcha, M. W., Jenkin, L. E., Millar, A. H., and Whelan, J. (2007). Oxygen initiation of respiration and mitochondrial biogenesis in rice. J. Biol. Chem. 282, 15619-15631. doi: 10.1074/jbc.M609866200.
22. Howell, K. A., Millar, A. H., and Whelan, J. (2006). Ordered assembly of mitochondria during rice germination begins with pro-mitochondrialstructures rich in components of the protein import apparatus. Plant Mol. Biol. 60, 201-223. doi: 10.1007/s11103-005-3688-7.
23. Howell, K. A., Narsai, R., Carroll, A., Ivanova, A., Lohse, M., Usadel, B., et al. (2009). Mapping metabolic and transcript temporal switches during germination in rice highlights specific transcription factors and the role of RNA instability in the germination process. Plant Physiol. 149, 961-980. doi: 10.1104/pp.108.129874.
24. Hu, W., Hu, G., and Han, B. (2009). Genome-wide survey and expression profiling ofheat shock proteins and heat shock factors revealed overlapped and stress specific response under abiotic stresses in rice. Plant Sci. 176, 583-590. doi: 10.1016/j.plantsci.2009.01.016.
25. Huang, S., Colmer, T. D., and Millar, A.H. (2008). Does anoxia tolerance involve altering the energy currency towards PPi? Trends Plant Sci. 13, 221-227. doi: 10.1016/j.tplants.2008.02.007.
26. Igamberdiev, A. U., Bykova, N. V., Shah, J. K., and Hill, R. D. (2010). Anoxic nitric oxide cycling in plants: participating reactions and possible mechanisms. Physiol. Plant. 138, 393-404. doi: 10.1111/j.1399- 3054.2009.01314.x
27. Igamberdiev, A. U., and Hill, R. D.(2009). Plant mitochondrial function during anaerobiosis. Ann. Bot. 103, 259-268. doi: 10.1093/aob/mcn100.
28. Igamberdiev, A. U., and Kleczkowski, L. A. (2011). Magnesium and cell energetics in plants under anoxia. Biochem. J. 437, 373-379. doi: 10.1042/BJ20110213.
29. Jain, M., Nijhawan, A., Arora, R., Agarwal, P., Ray, S., Sharma, P., et al. (2007). F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiol. 143, 1467-1483. doi: 10.1104/pp.106.091900.
30. Jaiswal, P., Ni, J., Yap, I., Ware, D., Spooner, W., Youens-Clark, K., et al. (2006). Gramene: a bird's eye view of cereal genomes. Nucleic Acids Res. 34, D717-D723. doi: 10.1093/nar/gkj154.
31. Khrouchtchova, A., Monde, R. A., and Barkan, A. (2012). A short PPR protein required for the splicing of specific group II introns in angiosperm chloroplasts. RNA 18, 1197-1209. doi: 10.1261/rna.032623.112.
32. Kilian, J., Whitehead, D., Horak, J., Wanke, D., Weinl, S., Batistic, O., et al. (2007). The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J. 50, 347-363. doi: 10.1111/j.1365- 313X.2007.03052.x
33. Kursteiner, O., Dupuis, I., and Kuhlemeier, C. (2003). The pyruvate decarboxylase1 gene of Arabidopsis is required during anoxia but not other environmental stresses. Plant Physiol. 132, 968-978. doi: 10.1104/pp.102.016907.
34. Lasanthi-Kudahettige, R., Magneschi, L., Loreti, E., Gonzali, S., Licausi, F., Novi, G., et al. (2007). Transcript profiling of the anoxic rice coleop- tile. PlantPhysiol. 144,218-231. doi: 10.1104/pp.106.093997.
35. Licausi, F., Kosmacz, M., Weits, D. A., Giuntoli, B., Giorgi, F. M., Voesenek, L. A., et al. (2011). Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature 479, 419-422. doi: 10.1038/nature 10536.
36. Long, A. D., Mangalam, H. J., Chan, B.Y., Tolleri, L., Hatfield, G. W., and Baldi, P. (2001). Improved statistical inference from DNA microarray data using analysis of variance and a Bayesian statistical framework. Analysis of global gene expression in Escherichia coli K12. J. Biol. Chem. 276, 19937-19944. doi: 10.1074/jbc.M010192200.
37. Loreti, E., Poggi, A., Novi, G., Alpi, A., and Perata, P. (2005). A genome- wide analysis of the effects of sucrose on gene expression in Arabidopsis seedlings under anoxia. Plant Physiol. 137, 1130-1138. doi: 10.1104/pp.104.057299.
38. Loreti, E., Yamaguchi, J., Alpi, A., and Perata, P. (2003). Sugar modulation of alpha-amylase genes under anoxia. Ann. Bot. 91, 143-148. doi: 10.1093/aob/mcf117.
39. Lu, P. L., Chen, N. Z., An, R., Su, Z., Qi, B. S., Ren, F., et al. (2007). A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress- responsive genes in Arabidopsis. Plant Mol. Biol. 63, 289-305. doi: 10.1007/s11103-006-9089-8.
40. Magneschi, L., and Perata, P. (2008). Rice germination and seedling growth in the absence of oxygen. Ann. Bot. 103, 181-196. doi: 10.1093/aob/mcn121.
41. Mustroph, A., Lee, S. C., Oosumi, T., Zanetti, M. E., Yang, H., Ma, K., et al. (2010). Cross-kingdom comparison of transcriptomic adjustments to low oxygen stress highlights conserved and plant-specific responses. Plant Physiol. 152, 1484-1500. doi: 10.1104/pp.109.151845.
42. Nakabayashi, K., Okamoto, M., Koshiba, T., Kamiya, Y., and Nambara, E. (2005). Genome- wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J. 41, 697-709. doi: 10.1111/j.1365-313X.2005.02337.x
43. Narsai, R., Castleden, I., and Whelan, J. (2010). Common and distinct organ and stress responsive tran- scriptomic patterns in Oryza sativa and Arabidopsis thaliana. BMC Plant Biol. 10:262. doi: 10.1186/1471-2229-10-262.
44. Narsai, R., Howell, K. A., Carroll, A., Ivanova, A., Millar, A. H., and Whelan, J. (2009). Defining core metabolic and transcriptomic responses to oxygen availability in rice embryos and young seedlings. Plant Physiol. 151, 306-322. doi: 10.1104/pp.109.142026.
45. Narsai, R., Law, S. R., Carrie, C., Xu, L., and Whelan, J. (2011a). In-depth temporal transcriptome profiling reveals a crucial developmental switch with roles for RNA processing and organelle metabolism that are essential for germination in Arabidopsis. Plant Physiol. 157, 1342-1362. doi: 10.1104/pp.111.183129.
46. Narsai, R., Rocha, M., Geigenberger, P., Whelan, J., and Van Dongen, J. T. (2011b). Comparative analysis between plant species of transcriptional and metabolic responses to hypoxia. New Phytol. 190, 472-487. doi: 10.1111/j.1469-8137.2010. 03589.x
47. Ostlund, G., Schmitt, T., Forslund, K., Kostler, T., Messina, D. N., Roopra, S.,et al. (2010). InParanoid 7: new algorithms and tools for eukaryotic orthology analysis. Nucleic Acids Res. 38, D196-D203. doi: 10.1093/nar/gkp931.
48. Pucciariello, C., Banti, V., and Perata, P. (2012a). ROS signaling as common element in low oxygen and heat stresses. Plant Physiol. Biochem. 59, 3-10. doi: 10.1016/j.plaphy.2012.02.016.
49. Pucciariello, C., Parlanti, S., Banti, V., Novi, G., and Perata, P. (2012b). Reactive oxygen species-driven transcription in Arabidopsis under oxygen deprivation. Plant Physiol. 159, 184-196. doi: 10.1104/pp.111. 191122.
50. Rasmussen, S., Barah, P., Suarez- Rodriguez, M. C., Bressendorff, S., Friis, P., Costantino, P., et al. (2013). Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiol. 161, 1783-1794. doi: 10.1104/pp.112.210773.
51. Ricard, B., Rivoal, J., Spiteri, A., and Pradet, A. (1991). Anaerobic stress induces the transcription and translation of sucrose synthase in rice. Plant Physiol. 95, 669-674. doi: 10.1104/pp.95.3.669.
52. Rivoal, J., Ricard, B., and Pradet, A. (1991). Lactate dehydrogenase in Oryza sativa L. seedlings and roots: identification and partial characterization. Plant Physiol. 95, 682-686. doi: 10.1104/pp.95.3.682.
53. Sachs, M. M., Freeling, M., and Okimoto, R. (1980). The anaerobic proteins of maize. Cell 20, 761-767. doi: 10.1016/0092-8674(80)90322-0.
54. Saha, D., Prasad, A. M., and Srinivasan, R. (2007). Pentatricopeptide repeat proteins and their emerging roles in plants. Plant Physiol. Biochem. 45, 521-534. doi: 10.1016/j.plaphy.2007.03.026.
55. Schroder, F., Lisso, J., and Mussig, C. (2011). EXORDIUM-LIKE1 promotes growth during low carbon availability in Arabidopsis. Plant Physiol. 156, 1620-1630. doi: 10.1104/pp.111.177204.
56. Sirova, J., Sedlarova, M., Piterkova, J., Luhova, L., and Petrivalsky, M. (2011). The role of nitric oxide in the germination of plant seeds and pollen. Plant Sci. 181, 560-572. doi: 10.1016/j.plantsci.2011.03.014.
57. Sreenivasulu, N., Usadel, B., Winter, A., Radchuk, V., Scholz, U., Stein, N., et al. (2008). Barley grain maturation and germination: metabolic pathway and regulatory network commonalities and differences highlighted by new MapMan/PageMan profiling tools. Plant Physiol. 146, 1738-1758. doi: 10.1104/pp.107.111781.
58. Sturms, R., Dispirito, A. A., and Hargrove, M. S. (2011). Plant and cyanobacterial hemoglobins reduce nitrite to nitric oxide under anoxic conditions. Biochemistry 50, 3873-3878. doi: 10.1021/bi2004312.
59. Tsukagoshi, H., Busch, W., and Benfey, P. N. (2010). Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143, 606-616. doi: 10.1016/j.cell.2010.10.020.
60. Tzafrir, I., Dickerman, A., Brazhnik, O., Nguyen, Q., McElver, J., Frye, C., et al. (2003). The Arabidopsis seed- genes project. Nucleic Acids Res. 31, 90-93. doi: 10.1093/nar/gkg028.
61. Usadel, B., Nagel, A., Steinhauser, D., Gibon, Y., Blasing, O. E., Redestig, H., et al. (2006). PageMan: an interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments. BMC Bioinformatics 7:535. doi: 10.1186/1471-2105-7-535.
62. Wells, D. M., Wilson, M. H., and Bennett, M. J. (2010). Feeling UPBEAT about growth: linking ROS gradients and cell proliferation. Dev. Cell 19, 644-646. doi: 10.1016/j.devcel.2010.10.017.
63. Xu, K., Xu, X., Fukao, T., Canlas, P., Maghirang-Rodriguez, R., Heuer, S., et al. (2006). Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442, 705-708. doi: 10.1038/nature04920