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Journal of Integrative Agriculture  2015, Vol. 14 Issue (9): 1723-1734    DOI: 10.1016/S2095-3119(15)61138-8
Crop Genetics · Breeding · Germplasm Resources Advanced Online Publication | Current Issue | Archive | Adv Search |
Comparison of transcriptomes undergoing waterlogging at the seedling stage between tolerant and sensitive varieties of Brassica napus L.
 ZOU Xi-ling, ZENG Liu, LU Guang-yuan, CHENG Yong, XU Jin-song, ZHANG Xue-kun
Key Laboratory of Biology and Genetic Improvement of Oil Crops, Ministry of Agriculture/Oil Crops Research Institute, Chinese Academy of Agricultural Sciences, Wuhan 430062, P.R.China
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摘要  RNA sequencing of the sensitive GH01 variety of Brassica napus L. seedling roots under 12 h of waterlogging was compared with previously published data of the ZS9 tolerant variety to unravel genetic mechanisms of waterlogging tolerance beyond natural variation. A total of 2 977 genes with similar expression patterns and 17 genes with opposite expression patterns were identified in the transcription profiles of ZS9 and GH01. An additional 1 438 genes in ZS9 and 1 861 genes in GH01 showed strain specific regulation. Analysis of the overlapped genes between ZS9 and GH01 revealed that waterlogging tolerance is determined by ability to regulate genes with similar expression patterns. Moreover, differences in both gene expression profiles and abscisic acid (ABA) contents between the two varieties suggest that ABA may play some role in waterlogging tolerance. This study identifies a subset of candidate genes for further functional analysis.

Abstract  RNA sequencing of the sensitive GH01 variety of Brassica napus L. seedling roots under 12 h of waterlogging was compared with previously published data of the ZS9 tolerant variety to unravel genetic mechanisms of waterlogging tolerance beyond natural variation. A total of 2 977 genes with similar expression patterns and 17 genes with opposite expression patterns were identified in the transcription profiles of ZS9 and GH01. An additional 1 438 genes in ZS9 and 1 861 genes in GH01 showed strain specific regulation. Analysis of the overlapped genes between ZS9 and GH01 revealed that waterlogging tolerance is determined by ability to regulate genes with similar expression patterns. Moreover, differences in both gene expression profiles and abscisic acid (ABA) contents between the two varieties suggest that ABA may play some role in waterlogging tolerance. This study identifies a subset of candidate genes for further functional analysis.
Keywords:  rapeseed (Brassica napus L.)       waterlogging       digital gene expression (DGE)       roots       transcriptome       comparative analysis  
Received: 28 September 2014   Accepted:
Corresponding Authors:  ZHANG Xue-kun, E-mail: seedcq@263.net     E-mail:  seedcq@263.net

Cite this article: 

ZOU Xi-ling, ZENG Liu, LU Guang-yuan, CHENG Yong, XU Jin-song, ZHANG Xue-kun. 2015. Comparison of transcriptomes undergoing waterlogging at the seedling stage between tolerant and sensitive varieties of Brassica napus L.. Journal of Integrative Agriculture, 14(9): 1723-1734.

Barnawal D, Bharti N, Maji D, Chanotiya C S, Kalra A. 2012.1-Aminocyclopropane-1-carboxylic acid (ACC) deaminasecontainingrhizobacteria protect Ocimum sanctum plantsduring waterlogging stress via reduced ethylene generationPlant Physiology Biochemistry, 58, 227-235

Benschop J J, Jackson M B, Guhl K, Vreeburg R A, Croker S J,Peeters A J, Voesenek L A. 2005. Contrasting interactionsbetween ethylene and abscisic acid in Rumex speciesdiffering in submergence tolerance. The Plant Journal, 44,756-768

Dennis E S, Dolferus R, Ellis M, Rahman M, Wu Y, Hoeren FU, Grover A, Ismond K P, Good A G, Peacock W J. 2000.Molecular strategies for improving waterlogging tolerancein plants. Journal of Experimental Botany, 51, 89-97

Fukao T, Bailey-Serres J. 2004. Plant responses to hypoxia--is survival a balancing act? Trends in Plant Science, 9,449-456

Fukao T, Bailey-Serres J. 2008. Submergence toleranceconferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice. Proceedings ofthe National Academy of Sciences of the United States ofAmerica, 105, 16814-16819

Geigenberger P. 2003. Response of plant metabolism to toolittle oxygen. Current Opinion in Plant Biology, 6, 247-256

Geisler-Lee J, Caldwell C, Gallie D R. 2010. Expression of theethylene biosynthetic machinery in maize roots is regulatedin response to hypoxia. Journal of Experimental Botany,61, 857-71

Gibbs D J, Lee S C, Isa N M, Gramuglia S, Fukao T, BasselG W, Correia C S, Corbineau F, Theodoulou F L, Bailey-Serres J, Holdsworth M J. 2011. Homeostatic response tohypoxia is regulated by the N-end rule pathway in plants.Nature, 479, 415-417

Gunawardena A H, Pearce D M, Jackson M B, Hawes C R,Evans D E. 2001. Characterisation of programmed celldeath during aerenchyma formation induced by ethyleneor hypoxia in roots of maize (Zea mays L.). Planta, 212,205-214

Hattori Y, Nagai K, Furukawa S, Song X J, Kawano R,Sakakibara H, Wu J, Matsumoto T, Yoshimura A, KitanoH, Matsuoka M, Mori H, Ashikari M. 2009. The ethyleneresponse factors SNORKEL1 and SNORKEL2 allow riceto adapt to deep water. Nature, 460, 1026-1030

Hinz M, Wilson I W, Yang J, Buerstenbinder K, Llewellyn D,Dennis E S, Sauter M, Dolferus R. 2010. ArabidopsisRAP2.2, an ethylene response transcription factor thatis important for hypoxia survival. Plant Physiology, 153,757-772

Hong J H, Seah S W, Xu J. 2013. The root of ABA action inenvironmental stress response. Plant Cell Report, 32,971-983

Hong L Z, Li J, Schmidt-Kuntzel A, Warren W C, Barsh G S.2011. Digital gene expression for non-model organisms.Genome Research, 21, 1905-1915

Horchani F, Aschi-Smiti S. 2011. Prolonged root hypoxia effectson ethylene biosynthesis and perception in tomato fruit.Plant Signal Behavior, 6, 1-4

Hsu F C, Chou M Y, Chou S J, Li Y R, Peng H P, Shih M C.2013. Submergence confers immunity mediated by theWRKY22 transcription factor in Arabidopsis. The PlantCell, 25, 2699-2713

Hsu F C, Chou M Y, Peng H P, Chou S J, Shih M C. 2011.Insights into hypoxic systemic responses based on analysesof transcriptional regulation in Arabidopsis. PLoS ONE, 6,e28888.

Ismond K P, Dolferus R, de Pauw M, Dennis E S, Good A G.2003. Enhanced low oxygen survival in Arabidopsis throughincreased metabolic flux in the fermentative pathway. PlantPhysiology, 132, 1292-1302

Jackson M B, Colmer T D. 2005. Response and adaptation byplants to flooding stress. Annals of Botany, 96, 501-505

Kende H, van der Knaap E, Cho H T. 1998. Deepwater rice,A model plant to study stem elongation. Plant Physiology,118, 1105-1110

Kennedy R A, Rumpho M E, Fox T C. 1992. Anaerobicmetabolism in plants. Plant Physiology, 100, 1-6

Licausi F, Kosmacz M, Weits D A, Giuntoli B, Giorgi F M,Voesenek LA, Perata P, van Dongen J T. 2011. Oxygensensing in plants is mediated by an N-end rule pathway forprotein destabilization. Nature, 479, 419-422

Linsen S E, Cuppen E. 2012. Methods for small RNA preparationfor digital gene expression profiling by next-generationsequencing. Methods in Molecular Biology, 822, 205-217

Negi S, Sukumar P, Liu X, Cohen J D, Muday G K. 2010.Genetic dissection of the role of ethylene in regulatingauxin-dependent lateral and adventitious root formation intomato. The Plant Journal, 61, 3-15

Sachs M M, Freeling M, Okimoto R. 1980. The anaerobicproteins of maize. Cell, 20, 761-767

Sachs M M, Subbaiah C C, Saab I N. 1996. Anaerobic geneexpression and flooding tolerance in maize. Journal ofExperimental Botany, 47, 1-15

Saika H, Okamoto M, Miyoshi K, Kushiro T, Shinoda S,Jikumaru Y, Fujimoto M, Arikawa T, Takahashi H, AndoM, Arimura S, Miyao A, Hirochika H, Kamiya Y, TsutsumiN, Nambara E, Nakazono M. 2007. Ethylene promotessubmergence-induced expression of OsABA8ox1, agene that encodes ABA 8´-hydroxylase in rice. Plant CellPhysiology, 48, 287-298

Sasidharan R, Mustroph A. 2011. Plant oxygen sensing ismediated by the N-end rule pathway, a milestone in plantanaerobiosis. The Plant Cell, 23, 4173-4183

Umezawa T, Okamoto M, Kushiro T, Nambara E, Oono Y,Seki M, Kobayashi M, Koshiba T, Kamiya Y, Shinozaki K.2006. CYP707A3, a major ABA 8´-hydroxylase involvedin dehydration and rehydration response in Arabidopsisthaliana. The Plant Journal, 46, 171-182

Vidoz M L, Loreti E, Mensuali A, Alpi A, Perata P. 2010.Hormonal interplay during adventitious root formation inflooded tomato plants. The Plant Journal, 63, 551-562

Voesenek L A, Bailey-Serres J. 2013. Flooding tolerance, O2sensing and survival strategies. Current Opinion in PlantBiology, 16, 647-653

Voesenek L A, Benschop J J, Bou J, Cox M C, Groeneveld H W,Millenaar F F, Vreeburg R A, Peeters A J. 2003. Interactionsbetween plant hormones regulate submergence-inducedshoot elongation in the flooding-tolerant dicot Rumexpalustris. Annals of Botany, 91, 205-211

Voesenek L A C J, Colmer T D, Pierik R, Millenaar F F, PeetersA J M. 2006. How plants cope with complete submergence.New Phytologist, 170, 213-226

Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R,Heuer S, Ismail A M, Bailey-Serres J, Ronald P C, MackillD J. 2006. Sub1A is an ethylene-response-factor-like genethat confers submergence tolerance to rice. Nature, 442,705-708

Yang C Y. 2014. Ethylene and hydrogen peroxide are involvedin hypoxia signaling that modulates AtERF73/HRE1expression. Plant Signal Behavior, 9, 1-6

Ye N, Jia L, Zhang J. 2012. ABA signal in rice under stressconditions. Rice, 5, 1.

Zhang X K, Chen J, Chen L, Wang H Z, Li J N. 2008. Imbibitionbehavior and flooding tolerance of rapeseed seed (Brassicanapus L.) with different testa color. Genetic Resources andCrop Evolution, 55, 1175-1184

Zhou W, Zhao D, Lin X. 1997. Effects of waterlogging onnitrogen accumulation and alleviation of waterloggingdamage by application of nitrogen fertilizer and mixtalol inwinter rape (Brassica napus L.). Journal of Plant GrowthRegulation, 16, 47-53

Zhou W J, Lin XQ. 1995. Effects of waterlogging at differentgrowth stages on physiological characteristics and seedyield of winter rape (Brassica napus L.). Field CropsResearch, 44, 103-110

Zou X L, Hu C W, Zeng L, Cheng Y, Xu M Y, Zhang X K. 2014a.A comparison of screening methods to identify waterloggingtolerance in the field in Brassica napus L. during plantontogeny. PLOS ONE, 9, e89731.

Zou X L, Cong Y, Cheng Y, Lu G Y, Zhang X K. 2013a.Screening and identification of waterlogging tolerantrapeseed (Brassica napus L.) during germination stage.In: Proceedings of the Third International Conference onIntelligent System Design and Engineering Applications(ISDEA), Hong Kong, China. pp. 1248-1253

Zou X L, Hu C W, Zeng L, Cheng Y, Xu M Y, Zhang X K. 2014b.A comparison of screening methods to identify waterloggingtolerance in the field in Brassica napus L. during plantontogeny. PLOS ONE, 9, 1-9

Zou X L, Jiang Y Y, Liu L, Zhang Z X, Zheng Y L. 2010.Identification of transcriptome induced in roots of maizeseedlings at the late stage of waterlogging. BMC PlantBiology, 10, 1-16

Zou X L, Tan X Y, Hu C W, Zeng L, Lu G Y, Fu G P, Cheng Y,Zhang X K. 2013b. The transcriptome of Brassica napus L.roots under waterlogging at the seedling stage. InternationalJournal of Molecular Sciences, 14, 2637-2651
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