Comparative transcriptional profiling of two rice genotypes carrying SUB1A-1 but exhibiting differential tolerance to submergence
Huaiyang Xiong A , Yang Li A , Jing Yang A and Yangsheng Li A BA State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, China.
B Corresponding author. Email: lysh2001@whu.edu.cn
Functional Plant Biology 39(6) 449-461 https://doi.org/10.1071/FP11251
Submitted: 8 November 2011 Accepted: 4 April 2012 Published: 22 May 2012
Abstract
Submergence tolerance in rainfed lowland rice (Oryza sativa L.) is determined mainly by SUB1A-1, which confers the tolerance by regulating the ethylene- and gibberellin-mediated gene expression responsible for carbohydrate consumption, cell elongation and ethanolic fermentation. However, two indica rice genotypes, FR13A and Goda Heenati, both carrying this gene, exhibited differential tolerance to submergence. Comparative analysis of transcriptional profiling of the two genotypes revealed that many of antioxidant genes were more highly expressed in FR13A than in Goda Heenati under both submergence and control conditions, or only under submergence, whereas most of genes involved in biosynthesis and signalling of ethylene and GA and in anaerobic carbohydrate metabolism had comparable levels of expression between genotypes under the same conditions. H2O2 and malondialdehyde (MDA) assays demonstrated that Goda Heenati accumulated more H2O2 and had more MDA, a product of lipid peroxidation, than FR13A under submergence. These findings suggest that apart from SUB1A-mediated ‘quiescence strategy’, the detoxification of reactive oxygen species (ROS) is another important trait associated with submergence tolerance. The information obtained from this study helps in further understanding of the mechanism underlying submergence tolerance.
Additional keywords: antioxidant genes, carbohydrate metabolism, ethylene, gibberellin, Goda Heenati.
References
Almeida AM, Vriezen WH, Van der Straeten D (2003) Molecular and physiological mechanisms of flooding avoidance and tolerance in rice. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 50, 743–751.| Molecular and physiological mechanisms of flooding avoidance and tolerance in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovFWis7o%3D&md5=97f82d823c79e3888feae0f1a0f83075CAS |
Boamfa EI, Veres AH, Ram PC, Jackson MB, Reuss J, Harren FJM (2005) Kinetics of ethanol and acetaldehyde suggest a role for acetaldehyde production in tolerance of rice seedlings to micro-aerobic conditions. Annals of Botany 96, 727–736.
| Kinetics of ethanol and acetaldehyde suggest a role for acetaldehyde production in tolerance of rice seedlings to micro-aerobic conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGitLbF&md5=307c4fde088022353c234d3157f8d105CAS |
Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker JR (1997) Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89, 1133–1144.
| Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXkt1KltLw%3D&md5=461f725e9e95ec0fc20754557d27d19cCAS |
Das KK, Panda D, Sarkar RK, Reddy JN, Ismail AM (2009) Submergence tolerance in relation to variable floodwater conditions in rice. Environmental and Experimental Botany 66, 425–434.
| Submergence tolerance in relation to variable floodwater conditions in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsV2kurk%3D&md5=37ddd8c9b0e3193deb50dbffb2ba5623CAS |
Degenkolbe T, Do PT, Zuther E, Repsilber D, Walther D, Hincha DK, Köhl KI (2009) Expression profiling of rice cultivars differing in their tolerance to long-term drought stress. Plant Molecular Biology 69, 133–153.
| Expression profiling of rice cultivars differing in their tolerance to long-term drought stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVagsb%2FJ&md5=aff02fc23cbdc7e3ceda61a13d6ff512CAS |
Ella ES, Kawano N, Ito O (2003) Importance of active oxygen-scavenging system in the recovery of rice seedlings after submergence. Plant Science 165, 85–93.
| Importance of active oxygen-scavenging system in the recovery of rice seedlings after submergence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXks1WlsbY%3D&md5=448ebb07291117792ba0cc9d902ac488CAS |
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.
| Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlertbjP&md5=470c53fd52dd10d2a899e14b897a7734CAS |
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.
| A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xos1KjtLg%3D&md5=7b3513cc5b2a96698b9118d4b7c6a28eCAS |
Hirano K, Aya K, Hobo T, Sakakibara H, Kojima M, Shim RA, Hasegawa Y, Ueguchi-Tanaka M, Matsuoka M (2008) Comprehensive transcriptome analysis of phytohormone biosynthesis and signaling genes in microspore/pollen and tapetum of rice. Plant & Cell Physiology 49, 1429–1450.
| Comprehensive transcriptome analysis of phytohormone biosynthesis and signaling genes in microspore/pollen and tapetum of rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVaiurrI&md5=2c7a1e94846b4de40d85f9d6187e82d2CAS |
Huang Y, Hui L, Hutchison CE, Laskey J, Kieber JJ (2003) Biochemical and functional analysis of CTR1, a protein kinase that negatively regulates ethylene signaling in Arabidopsis. The Plant Journal 33, 221–233.
| Biochemical and functional analysis of CTR1, a protein kinase that negatively regulates ethylene signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhslWkurY%3D&md5=7cabd2ce70376bea5eee9e9f7a8ea1d1CAS |
Itoh H, Shimada A, Ueguchi-Tanaka M, Kamiya N, Hasegawa Y, Ashikari M, Matsuoka M (2005) Overexpression of a GRAS protein lacking the DELLA domain confers altered gibberellin responses in rice. The Plant Journal 44, 669–679.
| Overexpression of a GRAS protein lacking the DELLA domain confers altered gibberellin responses in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Grtr%2FO&md5=613e82ca8dffdf673a185c4cde18ecedCAS |
Jackson MB, Ram PC (2003) Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence. Annals of Botany 91, 227–241.
| Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitVCksbY%3D&md5=abebd81f0cbc348263cd9459e2f61932CAS |
Jackson MB, Waters I, Setter T, Greenway H (1987) Injury to rice plants caused by complete submergence; a contribution by ethylerie (ethene). Journal of Experimental Botany 38, 1826–1838.
| Injury to rice plants caused by complete submergence; a contribution by ethylerie (ethene).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXltlSjsw%3D%3D&md5=e970ec5f0911ce562047d4ebf9cf826dCAS |
Kaneko M, Inukai Y, Ueguchi-Tanaka M, Itoh H, Izawa T, Kobayashi Y, Hattori T, Miyao A, Hirochika H, Ashikari M, Matsuoka M (2004) Loss-of-function mutations of the rice GAMYB gene impair alpha-amylase expression in aleurone and flower development. The Plant Cell 16, 33–44.
| Loss-of-function mutations of the rice GAMYB gene impair alpha-amylase expression in aleurone and flower development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXosVemtQ%3D%3D&md5=a6171044c46e1ffd0fefa339530b3017CAS |
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.
| Transcript profiling of the anoxic rice coleoptile.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXls1KjtL8%3D&md5=7b53ded5d366d14b85d2e26b876d8cd6CAS |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=86e5fd6e2b10f00206b12a43a671f6c8CAS |
Palada MC, Vergara BS (1972) Environmental effects on the resistance of rice seedlings to complete submergence. Crop Science 12, 209–212.
| Environmental effects on the resistance of rice seedlings to complete submergence.Crossref | GoogleScholarGoogle Scholar |
Perata P, Voesenek LA (2007) Submergence tolerance in rice requires Sub1A, an ethylene-response-factor-like gene. Trends in Plant Science 12, 43–46.
| Submergence tolerance in rice requires Sub1A, an ethylene-response-factor-like gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhvVyku7c%3D&md5=d0783a93af6a8c71fd70838ea309bccdCAS |
Perata P, Geshi N, Yamaguchi J, Akazawa T (1993) Effect of anoxia on the induction of alpha-amylase in cereal seeds. Planta 191, 402–408.
| Effect of anoxia on the induction of alpha-amylase in cereal seeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXmsVGksrg%3D&md5=3b17ab5750dd8afc7901f41741d18a2aCAS |
Perata P, Guglielminetti L, Alpi A (1997) Mobilization of endosperm reserves in cereal seeds under anoxia. Annals of Botany 79, 49–56.
Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta 975, 384–394.
| Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXkvFehtL4%3D&md5=61552bb6b1288bbccc74fc2ed3898209CAS |
Ram PC, Singh BB, Singh AK, Ram P, Singh PN, Singh HP, Boamfa I, Harren F, Santosa E, Jackson MB, Setter TL, Reuss J, Wade LJ, Singh VP, Singh RK (2002) Submergence tolerance in rainfed lowland rice: physiological basis and prospects for cultivar improvement through marker-aided breeding. Field Crops Research 76, 131–152.
| Submergence tolerance in rainfed lowland rice: physiological basis and prospects for cultivar improvement through marker-aided breeding.Crossref | GoogleScholarGoogle Scholar |
Santosa IE, Ram PC, Boamfa EI, Laarhoven LJJ, Reuss J, Jackson MB, Harren FJM (2007) Patterns of peroxidative ethane emission from submerged rice seedlings indicate that damage from reactive oxygen species takes place during submergence and is not necessarily a post-anoxic phenomenon. Planta 226, 193–202.
| Patterns of peroxidative ethane emission from submerged rice seedlings indicate that damage from reactive oxygen species takes place during submergence and is not necessarily a post-anoxic phenomenon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltlSktbs%3D&md5=25b8904f931179cd56fc2feb53984fedCAS |
Sasaki A, Itoh H, Gomi K, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Jeong DH, An G, Kitano H, Ashikari M, Matsuoka M (2003) Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299, 1896–1898.
| Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitFKksrw%3D&md5=1870eadf16fd67c5af45f63b8edd0fcdCAS |
Septiningsih EM, Pamplona AM, Sanchez DL, Neeraja CN, Vergara GV, Heuer S, Ismail AM, Mackill DJ (2009) Development of submergence-tolerant rice cultivars: the Sub1 locus and beyond. Annals of Botany 103, 151–160.
| Development of submergence-tolerant rice cultivars: the Sub1 locus and beyond.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsFCktbo%3D&md5=e5fd065113f2f48f1a6c094cb9a12a6dCAS |
Setter TL, Ellis M, Laureles EV, Ella ES, Senadhira D, Mishra SB, Sarkarung S, Datta S (1997) Physiology and genetics of submergence tolerance in rice. Annals of Botany 79, 67–77.
Singh N, Dang TTM, Vergara GV, Pandey DM, Sanchez D, Neeraja CN, Septiningsih EM, Mendioro M, Tecson-Mendoza EM, Ismail AM, Mackill DJ, Heuer S (2010) Molecular marker survey and expression analyses of the rice submergence-tolerance gene SUB1A. Theoretical and Applied Genetics 121, 1441–1453.
| Molecular marker survey and expression analyses of the rice submergence-tolerance gene SUB1A.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlehtb%2FN&md5=af499b19c15ba1642cfa44fc0fb2fc5aCAS |
Ushimaru T, Kanematsu S, Shibasaka M, Tsuji H (1999) Effect of hypoxia on the antioxidative enzymes in aerobically grown rice (Oryza sativa) seedlings. Physiologia Plantarum 107, 181–187.
| Effect of hypoxia on the antioxidative enzymes in aerobically grown rice (Oryza sativa) seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXotFSrt78%3D&md5=7c30442cbc93d84d7420dbaebe35d6a1CAS |
Vergara BS, Mazaredo A (1975) Screening for resistance to submergence under greenhouse conditions. In ‘Proceedings of the International Seminar on deep-water rice’. pp. 67–70. (Bangladesh Rice Research Institute: Dhaka)
Xu K, Deb R, Mackill DJ (2004) A microsatellite marker and a codominant PCR-based marker for marker-assisted selection of submergence tolerance in rice. Crop Science 44, 248–253.
| A microsatellite marker and a codominant PCR-based marker for marker-assisted selection of submergence tolerance in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptFejug%3D%3D&md5=8a85a20d27f92f170debe72a35be1fdeCAS |
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.
| Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnvVynsrs%3D&md5=74e8ecf0c24e8d9ec32e4954b1b1d7adCAS |
Zhou B, Wang J, Guo Z, Tan H, Zhu X (2006) A simple colorimetric method for determination of hydrogen peroxide in plant tissues. Plant Growth Regulation 49, 113–118.
| A simple colorimetric method for determination of hydrogen peroxide in plant tissues.Crossref | GoogleScholarGoogle Scholar |