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Genome-wide identification and analysis of genes associated with lysigenous aerenchyma formation in rice roots

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Abstract

Plants develop lysigenous aerenchyma to improve their survival in soils that are low in oxygen, such as in paddy fields. To investigate the genes involved in this formation in rice, we sampled the lysigenous aerenchyma formed part (LAFP) and lysigenous aerenchyma unformed part (LAUP) from seminal roots and conducted transcriptome analysis with a whole-genome microarray platform, i.e., Agilent 4X44K arrays. In all, 268 genes were highly upregulated in LAFP and 259 genes in LAUP, showing fold-changes of at least 1.5 (log2) and p-values <0.01. The MapMan toolkit was used for functional characterization of differentially expressed genes. As expected, genes associated with ethylene signaling and the redox response, heat shock proteins, and secondary metabolite metabolism (e.g., flavonoids and phenylpropanoids) were prominent in LAFP. By contrast, genes related to auxins, peroxidase, glucosidase, and proteins active in pathogen responses were expressed more highly in LAUP. Previous research has shown that genes detected in LAFP, such as our candidates, are important for conferring tolerance to multiple abiotic stresses while genes expressed in LAUP are necessary for root development and soil stress (i.e., drought and nutrient deficiencies) tolerance. This genome-wide examination of the formation of lysigenous aerenchyma in rice roots presents potential candidate genes involved in the molecular mechanism that supports this production.

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References

  • Campbell R, Drew MC (1983) Electron microscopy of gas space (aerenchyma) formation in adventitious roots of Zea mays L. subjected to oxygen shortage. Planta 157:350–357

    CAS  Google Scholar 

  • Cao P, Jung KH, Choi D, Hwang D, Ronald PC (2012) The rice oligonucleotide array database: an atlas of rice gene expression. Rice 5:17

    Article  PubMed  Google Scholar 

  • Chen JQ, Meng XP, Zhang Y, Xia M, Wang XP (2008) Over-expression of OsDREB genes lead to enhanced drought tolerance in rice. Biotechnol Lett 30:2191–2198

    Article  PubMed  Google Scholar 

  • Colmer TD (2003) Aerenchyma and an inducible barrier to radial oxygen loss facilitate root aeration in upland, paddy and deepwater rice (Oryza sativa L.). Ann Bot 91:301–309

    Article  CAS  PubMed  Google Scholar 

  • Colmer TD, Cox MC, Voesenek LA (2006) Root aeration in rice (Oryza sativa): evaluation of oxygen, carbon dioxide, and ethylene as possible regulators of root acclimatizations. New Phytol 170:767–777

    Article  CAS  PubMed  Google Scholar 

  • Drew MC, He CJ, Morgan PW (2000a) Ethylene-triggered cell death during aerenchyma formation in roots. Symp Soc Exper Biol 52:183–192

    CAS  Google Scholar 

  • Drew MC, He CJ, Morgan PW (2000b) Programmed cell death and aerenchyma formation in roots. Trends Plant Sci 5:123–127

    Article  CAS  PubMed  Google Scholar 

  • Feng L, Wang K, Li Y, Tan Y, Kong J, Li H, Zhu Y (2007) Overexpression of SBPase enhances photosynthesis against high temperature stress in transgenic rice plants. Plant Cell Rep 26:1635–1646

    Article  CAS  PubMed  Google Scholar 

  • Fujino K, Sekiguchi H, Matsuda Y, Sugimoto K, Ono K, Yano M (2008) Molecular identification of a major quantitative trait locus, qLTG3-1, controlling low-temperature germinability in rice. Proc Natl Acad Sci USA 105:12623–12628

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fukuda A, Nakamura A, Tagiri A, Tanaka H, Miyao A, Hirochica H (2004) Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice. Plant Cell Physiol 45:146–159

    Article  CAS  PubMed  Google Scholar 

  • Gechev TS, Gadjev IZ, Hille J (2004) An extensive microarray analysis of AAL-toxin-induced cell death in Arabidopsis thaliana brings new insights into the complexity of programmed cell death in plants. Cell Mol Life Sci 61:1185–1197

    Article  CAS  PubMed  Google Scholar 

  • Gunawardena AH, Pearce DM, Jackson MB, Hawes CR, Evans DE (2001) Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta 212:205–214

    Article  CAS  PubMed  Google Scholar 

  • He C, Finlayson SA, Drew MC, Jordan WR, Morgan PW (1996) Ethylene biosynthesis during aerenchyma formation in roots of maize subjected to mechanical impedance and hypoxia. Plant Physiol 112:1679–1685

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in coldresponsive gene expression in transgenic rice. Plant Cell Physiol 47:141–153

    Article  CAS  PubMed  Google Scholar 

  • Jackson MB, Fenning TM, Drew MC, Saker LR (1985) Stimulation of ethylene production and gas-space (aerenchyma) formation in adventitious roots of Zea mays L. by small partial pressures of oxygen. Planta 165:486–492

    Article  CAS  PubMed  Google Scholar 

  • Jain M, Nijhawan A, Tyagi AK, Khurana JP (2006) Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem Biophys Res Commun 345:646–651

    Article  CAS  PubMed  Google Scholar 

  • Joshi R, Kumar P (2012) Lysigenous aerenchyma formation involves non-apoptotic programmed cell death in rice (Oryza sativa L.) roots. Physiol Mol Biol Plants 18:1–9

    Article  PubMed Central  PubMed  Google Scholar 

  • Joshi R, Shukla A, Mani SC, Kumar P (2010) Hypoxia induced nonapoptotic cellular changes during aerenchyma formation in rice (Oryza sativa L.) roots. Physiol Mol Biol Plants 16:99–106

    Article  PubMed Central  PubMed  Google Scholar 

  • Jung KH, An G (2012) Application of MapMan and RiceNet drives systematic analyses of the early heat stress transcriptome in rice seedlings. J Plant Biol 55:436–449

    Article  CAS  Google Scholar 

  • Jung KH, Dardick C, Bartley LE, Cao P, Phetsom J, Canlas P, Seo YS, Shultz M, Ouyang S, Yuan Q, Frank BC, Ly E, Zheng L, Jia Y, Hsia AP, An K, Chou HH, Rocke D, Lee GC, Schnable PS, An G, Buell CR, Ronald PC (2008) Refinement of light-responsive transcript lists using rice oligonucleotide arrays: evaluation of gene-redundancy. PLoS ONE 3:e3337

    Article  PubMed Central  PubMed  Google Scholar 

  • Jung KH, Seo YS, Walia H, Cao P, Fukao T, Canlas PE, Amonpant F, Bailey-Serres J, Ronald PC (2010) The submergence tolerance regulator Sub1A mediates stress-responsive expression of AP2/ERF transcription factors. Plant Physiol 152:1674–1692

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kamiya N, Nagasaki H, Morikami A, Sato Y, Matsuoka M (2003) Isolation and characterization of a rice WUSCHEL-type homeobox gene that is specifically expressed in the central cells of a quiescent center in the root apical meristem. Plant J 35:429–441

    Article  CAS  PubMed  Google Scholar 

  • Kim H, Park PJ, Hwang HJ, Lee SY, Oh MH, Kim SG (2006) Brassinosteroid signals control expression of the AXR3/IAA17 gene in the cross-talk point with auxin in root development. Biosci Biotechnol Biochem 70:768–773

    Article  CAS  PubMed  Google Scholar 

  • Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne D, Kumar D, Zhou JM, Shah J, Zhang S, Kachroo P, Trifa Y, Pontier D, Lam E, Silva H (2000) Nitric oxide and salicylic acid signaling in plant defense. Proc Natl Acad Sci USA 97:8849–8855

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kotake T, Aohara T, Hirano K, Sato A, Kaneko Y, Tsumuraya Y, Takatsuji H, Kawasaki S (2011) Rice Brittle culm 6 encodes a dominant-negative form of CesA protein that perturbs cellulose synthesis in secondary cell walls. J Exp Bot 62:2053–2062

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lee S, Jeong HJ, Kim SA, Lee J, Guerinot ML, An G (2010) OsZIP5 is a plasma membrane zinc transporter in rice. Plant Mol Biol 73:507–517

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Wang X, Zhang H, Yang Y, Ge X, Song F (2008) A rice serine carboxypeptidase-like gene OsBISCPL1 is involved in regulation of defense responses against biotic and oxidative stress. Gene 420:57–65

    Article  CAS  PubMed  Google Scholar 

  • Muhlenbock P, Plaszczyca M, Mellerowicz E, Karpinski S (2007) Lysigenous aerenchyma formation in Arabidopsis is controlled by LESION SIMULATING DISEASE1. Plant Cell 19:3819–3830

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nishiuchi S, Yamauchi T, Takahashi H, Kotula L, Nakazono M (2012) Mechanisms for coping with submergence and waterlogging in rice. Rice 5:2

    Article  PubMed Central  PubMed  Google Scholar 

  • Pieterse CM, van Wees SC, Hoffland E, van Pelt JA, van Loon LC (1996) Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8:1225–1237

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Qi Y, Wang S, Shen C, Zhang S, Chen Y, Xu Y, Liu Y, Wu Y, Jiang D (2012) OsARF12, a transcription activator on auxin response gene, regulates root elongation and affects iron accumulation in rice (Oryza sativa). New Phytol 193:109–120

    Article  CAS  PubMed  Google Scholar 

  • Rajhi I, Yamauchi T, Takahashi H, Nishiuchi S, Shiono K, Watanabe R, Mliki A, Nagamura Y, Tsutsumi N, Nishizawa NK, Nakazono M (2011) Identification of genes expressed in maize root cortical cells during lysigenous aerenchyma formation using laser microdissection and microarray analyses. New Phytol 190:351–368

    Article  CAS  PubMed  Google Scholar 

  • Reinbothe C, Springer A, Samol I, Reinbothe S (2009) Plant oxylipins: role of jasmonic acid during programmed cell death, defence and leaf senescence. FEBS J 276:4666–4681

    Article  CAS  PubMed  Google Scholar 

  • Sasaki A, Ashikari M, Ueguchi-Tanaka M, Itoh H, Nishimura A, Swapan D, Ishiyama K, Saito T, Kobayashi M, Khush GS, Kitano H, Matsuoka M (2002) Green revolution: a mutant gibberellin-synthesis gene in rice. Nature 416:701–702

    Article  CAS  PubMed  Google Scholar 

  • Sato K, Suzuki R, Nishikubo N, Takenouchi S, Ito S, Nakano Y, Nakaba S, Sano Y, Funada R, Kajita S, Kitano H, Katayama Y (2010) Isolation of a novel cell wall architecture mutant of rice with defective Arabidopsis COBL4 ortholog BC1 required for regulated deposition of secondary cell wall components. Planta 232:257–270

    Article  CAS  PubMed  Google Scholar 

  • Takehisa H, Sato Y, Igarashi M, Abiko T, Antonio BA, Kamatsuki K, Minami H, Namiki N, Inukai Y, Nakazono M, Nagamura Y (2012) Genome-wide transcriptome dissection of the rice root system: implications for developmental and physiological functions. Plant J 69:126–140

    Article  CAS  PubMed  Google Scholar 

  • Tanaka K, Murata K, Yamazaki M, Onosato K, Miyao A, Hirochika H (2003) Three distinct rice cellulose synthase catalytic subunit genes required for cellulose synthesis in the secondary wall. Plant Physiol 133:73–83

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tian Q, Reed JW (1999) Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development 126:711–721

    CAS  PubMed  Google Scholar 

  • Tsang DL, Edmond C, Harrington JL, Nuhse TS (2011) Cell wall integrity controls root elongation via a general 1-aminocyclopropane-1-carboxylic acid-dependent, ethylene-independent pathway. Plant Physiol 156:596–604

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Urbanczyk-Wochniak E, Usadel B, Thimm O, Nunes-Nesi A, Carrari F, Davy M, Blasing O, Kowalczyk M, Weicht D, Polinceusz A, Meyer S, Stitt M, Fernie AR (2006) Conversion of MapMan to allow the analysis of transcript data from Solanaceous species: effects of genetic and environmental alterations in energy metabolism in the leaf. Plant Mol Biol 60:773–792

    Article  CAS  PubMed  Google Scholar 

  • Usadel B, Nagel A, Thimm O, Redestig H, Blaesing OE, Palacios-Rojas N, Selbig J, Hannemann J, Piques MC, Steinhauser D, Scheible WR, Gibon Y, Morcuende R, Weicht D, Meyer S, Stitt M (2005) Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of corresponding genes, and comparison with known responses. Plant Physiol 138:1195–1204

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xiong H, Yang J, Li Y (2012) Identification of submergenceresponsive genes in two indica rice genotypes carrying SUB1A-1 but exhibiting differential tolerance. J Plant Biol 55:233–241

    Article  CAS  Google Scholar 

  • Xuan YH, Priatama RA, Huang J, Je BI, Liu JM, Park SJ, Piao HL, Son DY, Lee JJ, Park SH, Jung KH, Kim TH, Han CD (2013) Indeterminate domain 10 regulates ammonium-mediated gene expression in rice roots. New Phytol 197:791–804

    Article  CAS  PubMed  Google Scholar 

  • Yamaji N, Mitatni N, Ma JF (2008) A transporter regulating silicon distribution in rice shoots. Plant Cell 20:1381–1389

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yamamoto E, Yonemaru J-I, Yamamoto T, Yano M (2012) OGRO: The overview of functionally characterized genes in rice online database. Rice 5:26

    Article  Google Scholar 

  • Yamauchi T, Rajhi I, Nakazono M (2011) Lysigenous aerenchyma formation in maize root is confined to cortical cells by regulation of genes related to generation and scavenging of reactive oxygen species. Plant Signal Behav 6:759–761

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yan C, Yan S, Zeng X, Zhang Z, Gu M (2007) Fine mapping and isolation of Bc7(t), allelic to OsCesA4. J Genet Genom 34:1019–1027

    Article  CAS  Google Scholar 

  • Ye H, Du H, Tang N, Li X, Xiong L (2009) Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice. Plant Mol Biol 71:291–305

    Article  CAS  PubMed  Google Scholar 

  • Yukiyoshi K, Karahara I (2014) Role of ethylene signalling in the formation of constitutive aerenchyma in primary roots of rice. AoB Plants 6:plu043

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Correspondence to Ki-Hong Jung.

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Yoo, YH., Choi, HK. & Jung, KH. Genome-wide identification and analysis of genes associated with lysigenous aerenchyma formation in rice roots. J. Plant Biol. 58, 117–127 (2015). https://doi.org/10.1007/s12374-014-0486-2

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  • DOI: https://doi.org/10.1007/s12374-014-0486-2

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