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ScAOC1, an allene oxide cyclase gene, confers defense response to biotic and abiotic stresses in sugarcane

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An allene oxide cyclase gene which is involved in defense against biotic and abiotic stresses was cloned and characterized in sugarcane.

Abstract

Allene oxide cyclase (AOC), a key enzyme in jasmonate acid (JA) biosynthesis, affects the stereoisomerism and biological activity of JA molecules, and plays an important role in plant stress resistance. In this study, four SsAOC alleles (SsAOC1–SsAOC4), which shared similar gene structure and were located on Chr1A, Chr1B, Chr1C, and Chr1D, respectively, were mined from sugarcane wild species Saccharum spontaneum, and a homologous gene ScAOC1 (GenBank Accession Number: MK674849) was cloned from sugarcane hybrid variety Yacheng05-179 inoculated with Sporisorium scitamineum for 48 h. ScAOC1 and SsAOC1–SsAOC4 were alkaline, unstable, hydrophilic, and non-secretory proteins, which possess the same set of conserved motifs and were clustered into one group in the phylogenetic analysis. ScAOC1 was expressed in all sugarcane tissues, but with different levels. After infection by S. scitamineum, the transcripts of ScAOC1 were increased significantly both in the smut-susceptible (ROC22) and resistant (Yacheng05-179) varieties, but its transcripts were more accumulated and lasted for a longer period in the smut-resistant variety than in the smut-susceptible one. ScAOC1 was down-regulated under MeJA and NaCl treatments, but up-regulated under SA, ABA, PEG, and cold stresses. Transiently overexpressing ScAOC1 gene into Nicotiana benthamiana leaves regulated the responses of N. benthamiana to two pathogens Ralstonia solanacearum and Fusarium solani var. coeruleum. Furthermore, prokaryotic expression analysis showed overexpression of ScAOC1 in Escherichia coli BL21 could enhance its tolerance to NaCl, mannitol, and cold stimuli. These results indicated that ScAOC1 may play an active role in response to biotic and abiotic stresses in sugarcane.

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References

  • Agrawal GK, Jwa NS, Agrawal SK, Tamogami S, Iwahashi H, Rakwal R (2003) Cloning of novel rice allene oxide cyclase (OsAOC): mRNA expression and comparative analysis with allene oxide synthase (OsAOS) gene provides insight into the transcriptional regulation of octadecanoid pathway biosynthetic genes in rice. Plant Sci 164:979–992

    CAS  Google Scholar 

  • Alexander KC, Ramakrishnan K (1980) Infection of the bud, establishment in the host and production of whips in sugarcane smut (Ustilago scitaminea Syd.) of sugarcane. Plant Pathol 17:1453–1455

    Google Scholar 

  • Choi DS, Hwang IS, Hwang BK (2012) Requirement of the cytosolic interaction between pathogenesis-related protein10 and leucine-rich repeat protein1 for cell death and defense signaling in pepper. Plant Cell 24:1675–1690

    CAS  Google Scholar 

  • Conconi A, Smerdon MJ, Howe GA, Ryan CA (1996) The octadecanoid signalling pathway in plants mediates a response to ultraviolet radiation. Nature 383:826–829

    CAS  Google Scholar 

  • D’Hont A, Grivet L, Feldmann P, Rao S, Berding N, Glaszmann JC (1996) Characterisation of the double genome structure of modern sugarcane cultivars (Saccharum spp.) by molecular cytogenetics. Mol Gen Genet 250:405–413

    Google Scholar 

  • Dong XJ, Li TZ, Feng YY, Wang XH, Gao BW (2018) Cloning and expression analysis of allene oxide cyclase gene from Aquilaria sinensis. Acta Pharm Sinica 53:467–475

    Google Scholar 

  • Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209

    CAS  Google Scholar 

  • Eddy SR (2011) Accelerated profile HMM searches. PLoS Computational Biol 7:e1002195

    CAS  Google Scholar 

  • Guo JL, Xu LP, Fang JP, Su YC, Fu HY, Que YX, Xu JS (2012) A novel dirigent protein gene with highly stem-specific expression from sugarcane, response to drought, salt and oxidative stresses. Plant Cell Rep 31:1801–1812

    CAS  Google Scholar 

  • Habora MEE, Eltayeb AE, Oka M, Tsujimoto H, Tanaka K (2013) Cloning of allene oxide cyclase gene from Leymus mollis and analysis of its expression in wheat-Leymus chromosome addition lines. Breeding Sci 63:68–76

    CAS  Google Scholar 

  • He YH, Fukushige H, Hildebrand DF, Gan SS (2002) Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol 128:876–884

    CAS  Google Scholar 

  • Irvine JE (1999) Saccharum species as horticultural classes. Theor Appl Genet 98:186–194

    Google Scholar 

  • Isayenkov S, Mrosk C, Stenzel I, Strack D, Hause B (2005) Suppression of allene oxide cyclase in hairy roots of Medicago truncatula reduces jasmonate levels and the degree of mycorrhization with Glomus intraradices. Plant Physiol 139:1401–1410

    CAS  Google Scholar 

  • Ishiga Y, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y (2003) Expression of allene oxide synthase and allene oxide cyclase in the interactions between pea and fungal pathogens. J Gen Plant Pathol 69:351–357

    CAS  Google Scholar 

  • Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593

    CAS  Google Scholar 

  • Ling H, Wu QB, Guo JL, Xu LP, Que YX (2014) Comprehensive selection of reference genes for gene expression normalization in sugarcane by real time quantitative RT-PCR. PLoS ONE 9:e97469

    Google Scholar 

  • Liu B, Wang WG, Gao JH, Chen F, Wang SH, Xu Y, Tang L, Jia YJ (2010) Molecular cloning and characterization of a jasmonate biosynthetic pathway gene for allene oxide cyclase from Jatropha curcas. Acta Physiol Plant 32:531–539

    CAS  Google Scholar 

  • Liu F, Huang N, Wang L, Ling H, Sun TT, Ahmad W, Muhammad K, Guo JX, Xu LP, Gao SW, Que YX, Su YC (2018) A novel L-ascorbate peroxidase 6 gene, ScAPX6, plays an important role in the regulation of response to biotic and abiotic stresses in sugarcane. Front Plant Sci 8:2262

    Google Scholar 

  • Liu F, Sun TT, Wang L, Su WH, Gao SW, Su YC, Xu LP, Que YX (2017) Plant jasmonate ZIM domain genes: shedding light on structure and expression patterns of JAZ gene family in sugarcane. BMC Genomics 18:771

    Google Scholar 

  • Liu HH, Wang YG, Wang SP, Li HJ (2015) Cloning and characterization of peanut allene oxide cyclase gene involved in salt-stressed responses. Genet Mol Res 14:2331–2340

    CAS  Google Scholar 

  • Liu QP, Xue QZ (2007) Molecular phylogeny, evolution, and functional divergence of the LSD1-like gene family: inference from the rice genome. J Mol Evol 64:354–363

    CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−△△CT method. Methods 25:402–408

    CAS  Google Scholar 

  • Lu L, Rong W, Zhou RH, Huo NX, Zhang ZY (2019) TaCML36, a wheat calmodulin-like protein, positively participates in an immune response to Rhizoctonia cerealis. Crop J 7:608–618

    Google Scholar 

  • Lu X, Lin XY, Shen Q, Zhang FY, Wang YY, Chen YF, Wang T, Wu SY, Tang KX (2011) Characterization of the jasmonate biosynthetic gene allene oxide cyclase in Artemisia annua L., source of the antimalarial drug artemisinin. Plant Mol Biol Rep 29:489–497

    CAS  Google Scholar 

  • Mao HY, Wang WJ, Su WH, Su YC, Liu F, Li CN, Wang L, Zhang X, Xu LP, Que YX (2019) Genome-wide identification, phylogeny, and expression analysis of Sec14-like PITP gene family in sugarcane. Plant Cell Rep 38:637–655

    Google Scholar 

  • Maucher H, Stenzel I, Miersch O, Stein N, Prasad M, Zierold U, Schweizer P, Dorer C, Hause B, Wasternack C (2004) The allene oxide cyclase of barley (Hordeum vulgare L.)-cloning and organ-specific expression. Phytochemistry 65:801–811

    CAS  Google Scholar 

  • Pi Y, Jiang KJ, Cao Y, Wang Q, Huang ZS, Li L, Hu LC, Li W, Sun XF, Tang KX (2009) Allene oxide cyclase from Camptotheca acuminata improves tolerance against low temperature and salt stress in tobacco and bacteria. Mol Biotechnol 41:115–122

    CAS  Google Scholar 

  • Que YX, Su YC, Guo JL, Wu QB, Xu LP (2014a) A global view of transcriptome dynamics during Sporisorium scitamineum challenge in sugarcane by RNA-seq. PLoS ONE 10:e0118445

    Google Scholar 

  • Que YX, Xu LP, Wu QB, Liu YF, Ling H, Liu YH, Zhang YY, Guo JL, Su YC, Chen JB, Wang SS, Zhang CG (2014b) Genome sequencing of Sporisorium scitamineum provides insights into the pathogenic mechanisms of sugarcane smut. BMC Genomics 15:996

    Google Scholar 

  • Riemann M, Haga K, Shimizu T, Okada K, Ando S, Mochizuki S, Nishizawa Y, Yamanouchi U, Nick P, Yano M, Minami E, Takano M, Yamane H, Iino M (2013) Identification of rice Allene Oxide Cyclase mutants and the function of jasmonate for defence against Magnaporthe oryzae. Plant J 74:226–238

    CAS  Google Scholar 

  • Stenzel I, Hause B, Miersch O, Kurz T, Maucher H, Weichert H, Ziegler J, Feussner I, Wasternack C (2003) Jasmonate biosynthesis and the allene oxide cyclase family of Arabidopsis thaliana. Plant Mol Biol 51:895–911

    CAS  Google Scholar 

  • Su WH, Ren YJ, Wang DJ, Su YC, Feng JF, Zhang C, Tang HC, Xu LP, Muhammad KS, Que YX (2020) The alcohol dehydrogenase gene family in sugarcane and its involvement in cold stress regulation. BMC Genomics 21:521

    CAS  Google Scholar 

  • Su YC, Guo JL, Ling H, Chen SS, Wang SS, Xu LP, Allan AC, Que YX (2014a) Isolation of a novel peroxisomal catalase gene from sugarcane, which is responsive to biotic and abiotic stresses. PLoS ONE 9:e84426

    Google Scholar 

  • Su YC, Wang ZQ, Liu F, Li Z, Peng Q, Guo JL, Xu LP, Que YX (2016) Isolation and characterization of ScGluD2, a new sugarcane beta-1,3-Glucanase D family gene induced by Sporisorium scitamineum, ABA, H2O2, NaCl, and CdCl2 stresses. Front Plant Sci 7:1348

    Google Scholar 

  • Su YC, Xu LP, Fu ZW, Yang YT, Guo JL, Wang SS, Que YX (2014b) ScChi, encoding an acidic class III chitinase of sugarcane, confers positive responses to biotic and abiotic stresses in sugarcane. Int J Mol Sci 15:2738–2760

    Google Scholar 

  • Su YC, Xu LP, Wang SS, Wang ZQ, Yang YT, Chen Y, Que YX (2015) Identification, phylogeny, and transcript of chitinase family genes in sugarcane. Sci Rep 5:10708

    CAS  Google Scholar 

  • Su YC, Xu LP, Xue BT, Wu QB, Guo JL, Wu LG, Que YX (2013) Molecular cloning and characterization of two pathogenesis-related β-1,3-glucanase genes ScGluA1 and ScGluD1 from sugarcane infected by Sporisorium scitamineum. Plant Cell Rep 32:1503–1519

    CAS  Google Scholar 

  • Sun TT, Liu F, Wang WJ, Wang L, Wang ZQ, Li J, Que YX, Xu LP, Su YC (2018) The role of sugarcane catalase gene ScCAT2 in the defense response to pathogen challenge and adversity stress. Int J Mol Sci 19:2686

    Google Scholar 

  • Sun TT, Wang WJ, Lou WY, Liu F, Zhang X, Wang L, Chen YF, Que YX, Xu LP, Li DM, Su YC (2019) Cloning and expression analysis of sugarcane lipoxygenase gene ScLOX1. Acta Agron Sin 45:1002–1016

    Google Scholar 

  • Sundar AR, Barnabas EL, Malathi P, Viswanathan R (2012) A mini-review on smut disease of sugarcane caused by Sporisorium scitamineum. In: Mworia J (ed) Botany, Croatia, pp 109–128

  • Wang L, Liu F, Zhang X, Wang WJ, Sun TT, Chen YF, Dai MJ, Yu SX, Xu LP, Su YC, Que YX (2018) Expression characteristics and functional analysis of the ScWRKY3 gene from sugarcane. Int J Mol Sci 19:4059

    Google Scholar 

  • Wang YG, Liu HH, Xin QG (2015) Improvement of copper tolerance of Arabidopsis by transgenic expression of an allene oxide cyclase gene, GhAOC1, in upland cotton (Gossypium hirsutum L.). Crop J 3:343–352

    Google Scholar 

  • Wani SH, Kumar V, Shriram V, Sah SK (2016) Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J 4:162–176

    Google Scholar 

  • Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697

    CAS  Google Scholar 

  • Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. Ann Bot 111:1021–1058

    CAS  Google Scholar 

  • Wu Q, Wang H, Wu JJ, Wang DG, Wang YL, Zhang L, Huang ZP, Yu DY (2015) Soybean GmAOC3 promotes plant resistance to the common cutworm by increasing the expression of genes involved in resistance and volatile substance emission in transgenic tobaccos. J Plant Biol 58:242–251

    CAS  Google Scholar 

  • Wu Q, Wu JJ, Sun HJ, Zhang D, Yu DY (2011) Sequence and expression divergence of the AOC gene family in soybean: insights into functional diversity for stress responses. Biotechnol Lett 33:1351–1359

    CAS  Google Scholar 

  • Yamada A, Saitoh T, Mimura T, Ozki Y (2002) Expression of mangrove allene oxide cyclase enhances salt tolerance in Escherichia coli, yeast, and tobacco cells. Plant Cell Physiol 43:903–910

    CAS  Google Scholar 

  • Yoeun S, Cho K, Han O (2018) Structural evidence for the substrate channeling of rice allene oxide cyclase in biologically analogous Nazarov reaction. Front Chem 6:500

    CAS  Google Scholar 

  • Zhang JS, Zhang XT, Tang HB, Zhang Q, Hua XT, Ma XK, Zhu F, Jones T, Zhu XG, Bowers J, Wai CM, Zheng CF, Shi Y, Chen S, Xu XM, Yue JJ, Nelson DR, Huang LX, Li Z, Xu HM, Zhou D, Wang YJ, Hu WC, Lin JS, Deng YJ, Pandey N, Mancini M, Zerpa D, Nguyen JK, Wang LM, Yu L, Xin YH, Ge LF, Arro J, Han JO, Chakrabarty S, Pushko M, Zhang WP, Ma YH, Ma PP, Lv MJ, Chen FM, Zheng GY, Xu JS, Yang ZH, Deng F, Chen XQ, Liao ZY, Zhang XX, Lin ZC, Lin H, Yan HS, Kuang Z, Zhong WM, Liang PP, Wang GF, Yuan Y, Shi JX, Hou JX, Lin JX, Jin JJ, Cao PJ, Shen QC, Jiang Q, Zhou P, Ma YY, Zhang XD, Xu R, Liu J, Zhou YM, Jia HF, Ma Q, Qi R, Zhang ZL, Fang JP, Fang HK, Song JJ, Wang MJ, Dong GR, Wang G, Chen Z, Ma T, Liu H, Dhungana SR, Huss SE, Yang XP, Sharma A, Trujillo JH, Martinez MC, Hudson M, Riascos JJ, Schuler M, Chen LQ, Braun DM, Li L, Yu QY, Wang JP, Wang K, Schatz MC, Heckerman D, Sluys MV, Mendes Souza G, Moore PH, Sankoff D, VanBuren R, Paterson AH, Nagai C, Ming R (2018) Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L. Nature Genet 50:1565–1573

    CAS  Google Scholar 

  • Zhao Y, Dong W, Zhang NB, Ai XH, Wang MC, Huang ZG, Xiao LT, Xia GM (2014) A wheat allene oxide cyclase gene enhances salinity tolerance via jasmonate signaling. Plant Physiol 164:1068–1076

    CAS  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    CAS  Google Scholar 

  • Ziegler J, Stenzel I, Hause B, Maucher H, Hamberg M, Grimm R, Ganal M, Wasternack C (2000) Molecular cloning of allene oxide cyclase, the enzyme establishing the stereochemistry of octadecanoids and jasmonates. J Biol Chem 275:19132–19138

    CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Key R&D Program of China (2018YFD1000503 and 2019YFD1000503), the National Natural Science Foundation of China (31871688), the Research Funds for Distinguished Young Scientists in Fujian Provincial Department of Education (SYC-2017), and the China Agriculture Research System (CARS-17).

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Authors and Affiliations

  1. Key Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture, College of Agriculture, Fujian Agriculture and Forestry University, Fuzhou, 350002, Fujian, China

    Tingting Sun, Guangli Cen, Wenyue Lou, Zhoutao Wang, Weihua Su, Wenju Wang, Damei Li, Youxiong Que & Yachun Su

  2. College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, 350002, Fujian, China

    Chuihuai You

  3. Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, College of Agriculture, Fujian Agriculture and Forestry University, Fuzhou, 350002, Fujian, China

    Youxiong Que & Yachun Su

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  1. Tingting Sun
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  2. Guangli Cen
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  3. Chuihuai You
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  4. Wenyue Lou
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  9. Youxiong Que
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  10. Yachun Su
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Correspondence to Youxiong Que or Yachun Su.

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Sun, T., Cen, G., You, C. et al. ScAOC1, an allene oxide cyclase gene, confers defense response to biotic and abiotic stresses in sugarcane. Plant Cell Rep 39, 1785–1801 (2020). https://doi.org/10.1007/s00299-020-02606-z

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