RNA-Seq reveals a xenobiotic stress response in the soybean aphid, Aphis glycines, when fed aphid-resistant soybean

BMC Genomics

Andy P Michel²  Omprakash Mittapalli²  MAR Mian¹  Raman Bansal² 

[1] USDA-ARS Corn and Soybean Research Unit, and the Department of Horticulture and Crop Sciences, OARDC, The Ohio State University, 1680 Madison Ave., Wooster, OH 44691, USA;Department of Entomology, The Ohio Agricultural Research and Development Center, The Ohio State University, 1680 Madison Ave., Wooster, OH 44691, USA

关键词: RNA-Seq;    Biotype;    Host-plant resistance;    Aphis glycines;   

Others  :  1127603
DOI  :  10.1186/1471-2164-15-972

 received in 2014-08-08, accepted in 2014-10-29,  发布年份 2014

【 摘 要 】

Background

While much recent research has expanded our understanding of the molecular interactions between aphids and their host plants, it is lacking for the soybean aphid, Aphis glycines. Since its North American invasion, A. glycines has become one of the most damaging insect pests on this important crop. Five soybean genes for host plant resistance to A. glycines have been identified, but populations of A. glycines have already adapted to overcome these resistance genes. Understanding the molecular interactions between resistant soybean and A. glycines can provide clues to its adaptation mechanisms. Here, we used RNA-Sequencing to compare and contrast A. glycines gene expression when fed resistant (Rag1) and susceptible soybean.

Results

Combining results from a previous A. glycines transcriptome, we generated 64,860 high quality transcripts, totaling 41,151,086 bases. Statistical analysis revealed 914 genes with significant differential expression. Most genes with higher expression in A. glycines on resistant plants (N = 352) were related to stress and detoxification such as cytochrome P450s, glutathione-S-transferases, carboxyesterases, and ABC transporters. A total of 562 genes showed lower transcript abundance in A. glycines on resistant plants. From our extensive transcriptome data, we also identified genes encoding for putative salivary effector proteins (N = 73). Among these, 6 effector genes have lower transcript abundance in A. glycines feeding on resistant soybean.

Conclusions

Overall, A. glycines exhibited a pattern typical of xenobiotic challenge, thereby validating antibiosis in Rag1, presumably mediated through toxic secondary metabolites. Additionally, this study identified many A. glycines genes and gene families at the forefront of its molecular interaction with soybean. Further investigation of these genes in other biotypes may reveal adaptation mechanisms to resistant plants.

【 授权许可】

   
2014 Bansal et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Tilmon KJ: Specialization, Speciation, and Radiation: the Evolutionary Biology of Herbivorous Insects. Berkeley, CA: University of California Press; 2008:360.
• [2]Smith CM: Plant Resistance to Arthropods: Molecular and Conventional Approaches. AA Dordrecht, The Netherlands: Springer; 2005:423.
• [3]Van Emden HF, Harrington R: Aphids as Crop Pests/edited by Helmut F. van Emden and Richard Harrington. Oxfordshire, UK: CABI Publishing; 2007.
• [4]Smith CM, Chuang W: Plant resistance to aphid feeding: behavioral, physiological, genetic and molecular cues regulate aphid host selection and feeding. Pest Manag Sci 2014, 70:528-540.
• [5]Li X, Schuler MA, Berenbaum MR: Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 2007, 52:231-253.
• [6]Xu C, Li CY, Kong AT: Induction of phase I, II and III drug metabolism/transport by xenobiotics. Arch Pharm Res 2005, 28(3):249-268.
• [7]Misra JR, Horner MA, Lam G, Thummel CS: Transcriptional regulation of xenobiotic detoxification in Drosophila. Genes Dev 2011, 25(17):1796-1806.
• [8]Jongsma M, Beekwilder J: Co-evolution of insect proteases and plant protease inhibitors. Curr Protein Pept Sci 2011, 12(5):437-447.
• [9]Prasain K, Nguyen TD, Gorman MJ, Barrigan LM, Peng Z, Kanost MR, Syed LU, Li J, Zhu KY, Hua DH: Redox potentials, laccase oxidation, and antilarval activities of substituted phenols. Bioorg Med Chem 2012, 20(5):1679-1689.
• [10]King-Jones K, Horner MA, Lam G, Thummel CS: The DHR96 nuclear receptor regulates xenobiotic responses in Drosophila. Cell Metab 2006, 4(1):37-48.
• [11]Cai Q, Han Y, Cao Y, Hu Y, Zhao X, Bi J: Detoxification of gramine by the cereal aphid Sitobion avenae. J Chem Ecol 2009, 35(3):320-325.
• [12]Hogenhout SA, Bos JI: Effector proteins that modulate plant–insect interactions. Curr Opin Plant Biol 2011, 14(4):422-428.
• [13]Carolan JC, Caragea D, Reardon KT, Mutti NS, Dittmer N, Pappan K, Cui F, Castaneto M, Poulain J, Dossat C: Predicted effector molecules in the salivary secretome of the pea aphid (Acyrthosiphon pisum): a dual transcriptomic/proteomic approach. J Proteome Res 2011, 10(4):1505-1518.
• [14]Elzinga DA, Jander G: The role of protein effectors in plant–aphid interactions. Curr Opin Plant Biol 2013, 16(4):451-456.
• [15]Tilmon K, Hodgson E, O’Neal M, Ragsdale D: Biology of the soybean aphid, Aphis glycines (Hemiptera: Aphididae) in the United States. J Int Pest Manag 2011, 2(2):A1-A7.
• [16]Ragsdale DW, Landis DA, Brodeur J, Heimpel GE, Desneux N: Ecology and management of the soybean aphid in North America. Annu Rev Entomol 2011, 56:375-399.
• [17]Hodgson E, McCornack B, Tilmon K, Knodel J: Management recommendations for soybean aphid (Hemiptera: Aphididae) in the United States. J Int Pest Manag 2012, 3(1):E1-E10.
• [18]Ragsdale DW, Voegtlin DJ, O’Neil RJ: Soybean aphid biology in North America. Ann Entomol Soc Am 2004, 97(2):204-208.
• [19]Hesler LS, Chiozza MV, O’Neal ME, MacIntosh GC, Tilmon KJ, Chandrasena DI, Tinsley NA, Cianzio SR, Costamagna AC, Cullen EM: Performance and prospects of Rag genes for management of soybean aphid. Entomol Exp Appl 2013, 147(3):201-206.
• [20]Hill CB, Li Y, Hartman GL: A single dominant gene for resistance to the soybean aphid in the soybean cultivar Dowling. Crop Sci 2006, 46(4):1601-1605.
• [21]Hill CB, Li Y, Hartman GL: Soybean aphid resistance in soybean Jackson is controlled by a single dominant gene. Crop Sci 2006, 46(4):1606-1608.
• [22]Mian MR, Kang S, Beil SE, Hammond RB: Genetic linkage mapping of the soybean aphid resistance gene in PI 243540. Theor Appl Genet 2008, 117(6):955-962.
• [23]Zhang G, Gu C, Wang D: A novel locus for soybean aphid resistance. Theor Appl Genet 2010, 120(6):1183-1191.
• [24]Diaz-Montano J, Reese JC, Schapaugh WT, Campbell LR: Characterization of antibiosis and antixenosis to the soybean aphid (Hemiptera: Aphididae) in several soybean genotypes. J Econ Entomol 2006, 99(5):1884-1889.
• [25]Kim K, Hill CB, Hartman GL, Mian M, Diers BW: Discovery of soybean aphid biotypes. Crop Sci 2008, 48(3):923-928.
• [26]Hill CB, Crull L, Herman TK, Voegtlin DJ, Hartman GL: A new soybean aphid (Hemiptera: Aphididae) biotype identified. J Econ Entomol 2010, 103(2):509-515.
• [27]Alt J, Ryan-Mahmutagic M: Soybean aphid biotype 4 identified. Crop Sci 2013, 53(4):1491-1495.
• [28]Bansal R, Jun T, Mian M, Michel AP: Developing Host-Plant Resistance for Hemipteran Soybean Pests: Lessons from Soybean Aphid and Stink Bugs. In Soybean - Pest Resistance. Edited by El-Shemy HA. Rijeka, Croatia: INTECH Publishing; 2013:19-46.
• [29]Li Y, Zou J, Li M, Bilgin DD, Vodkin LO, Hartman GL, Clough SJ: Soybean defense responses to the soybean aphid. New Phytol 2008, 179(1):185-195.
• [30]Studham ME, MacIntosh GC: Multiple phytohormone signals control the transcriptional response to soybean aphid infestation in susceptible and resistant soybean plants. Mol Plant-Microbe Interact 2013, 26(1):116-129.
• [31]Diaz-Montano J, Reese JC, Louis J, Campbell LR, Schapaugh WT: Feeding behavior by the soybean aphid (Hemiptera: Aphididae) on resistant and susceptible soybean genotypes. J Econ Entomol 2007, 100(3):984-989.
• [32]Bai X, Zhang W, Orantes L, Jun T, Mittapalli O, Mian MR, Michel AP: Combining next-generation sequencing strategies for rapid molecular resource development from an invasive aphid species. Aphis glycines PLoS One 2010, 5(6):e11370.
• [33]O’Neil ST, Dzurisin JD, Carmichael RD, Lobo NF, Emrich SJ, Hellmann JJ: Population-level transcriptome sequencing of nonmodel organisms Erynnis propertius and Papilio zelicaon. BMC Genomics 2010, 11:310-2164-11-310.
• [34]Consortium IAG: Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol 2010, 8(2):e1000313.
• [35]Mittapalli O, Bai X, Mamidala P, Rajarapu SP, Bonello P, Herms DA: Tissue-specific transcriptomics of the exotic invasive insect pest emerald ash borer (Agrilus planipennis). PLoS One 2010, 5(10):e13708.
• [36]Chen Y, Cassone BJ, Bai X, Redinbaugh MG, Michel AP: Transcriptome of the plant virus vector Graminella nigrifrons, and the molecular interactions of maize fine streak rhabdovirus transmission. PLoS One 2012, 7(7):e40613.
• [37]Bai X, Mamidala P, Rajarapu SP, Jones SC, Mittapalli O: Transcriptomics of the bed bug (Cimex lectularius). PLoS One 2011, 6(1):e16336.
• [38]Nicholson SJ, Hartson SD, Puterka GJ: Proteomic analysis of secreted saliva from Russian Wheat Aphid (Diuraphis noxia Kurd.) biotypes that differ in virulence to wheat. J Proteome 2012, 75(7):2252-2268.
• [39]Carolan JC, Fitzroy CI, Ashton PD, Douglas AE, Wilkinson TL: The secreted salivary proteome of the pea aphid Acyrthosiphon pisum characterised by mass spectrometry. Proteomics 2009, 9(9):2457-2467.
• [40]Atamian HS, Chaudhary R, Cin VD, Bao E, Girke T, Kaloshian I: In planta expression or delivery of potato aphid Macrosiphum euphorbiae effectors Me10 and Me23 enhances aphid fecundity. Mol Plant-Microbe Interact 2013, 26(1):67-74.
• [41]Rao SA, Carolan JC, Wilkinson TL: Proteomic profiling of cereal aphid saliva reveals both ubiquitous and adaptive secreted proteins. PLoS One 2013, 8(2):e57413.
• [42]Cui F, Michael Smith C, Reese J, Edwards O, Reeck G: Polymorphisms in salivary gland transcripts of Russian wheat aphid biotypes 1 and 2. Insect Science 2012, 19(4):429-440.
• [43]Pechan T, Ye L, Chang Y, Mitra A, Lin L, Davis FM, Williams WP, Luthe DS: A unique 33-kD cysteine proteinase accumulates in response to larval feeding in maize genotypes resistant to fall armyworm and other Lepidoptera. The Plant Cell Online 2000, 12(7):1031-1040.
• [44]Mohan S, Ma PW, Williams WP, Luthe DS: A naturally occurring plant cysteine protease possesses remarkable toxicity against insect pests and synergizes Bacillus thuringiensis toxin. PLoS One 2008, 3(3):e1786.
• [45]Will T, Tjallingii WF, Thönnessen A, van Bel AJ: Molecular sabotage of plant defense by aphid saliva. Proc Natl Acad Sci 2007, 104(25):10536-10541.
• [46]Will T, Kornemann SR, Furch AC, Tjallingii WF, van Bel AJ: Aphid watery saliva counteracts sieve-tube occlusion: a universal phenomenon? J Exp Biol 2009, 212(20):3305-3312.
• [47]Darby NJ, Penka E, Vincentelli R: The multi-domain structure of protein disulfide isomerase is essential for high catalytic efficiency. J Mol Biol 1998, 276(1):239-247.
• [48]Li Y, Hill CB, Hartman GL: Effect of three resistant soybean genotypes on the fecundity, mortality, and maturation of soybean aphid (Homoptera: Aphididae). J Econ Entomol 2004, 97(3):1106-1111.
• [49]Thompson GA, Goggin FL: Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. J Exp Bot 2006, 57(4):755-766.
• [50]Feyereisen R, Feyereisen R: Insect CYP Genes and P450 Enzymes. In Insect Molecular Biology And Biochemistry. Edited by Gilbert LH. London: Academic Press/Elsevier; 2012:236-315.
• [51]Dixon RA, Achnine L, Kota P, Liu C, Reddy M, Wang L: The phenylpropanoid pathway and plant defence—a genomics perspective. Mol Plant Pathol 2002, 3(5):371-390.
• [52]Zabala G, Zou J, Tuteja J, Gonzalez D, Clough S, Vodkin L: Transcriptome changes in the phenylpropanoid pathway of Glycine max in response to pseudomonas syringae infection. BMC Plant Biol 2006, 6(1):26. BioMed Central Full Text
• [53]Mao W, Berhow MA, Zangerl AR, Mcgovern J, Berenbaum MR: Cytochrome P450-mediated metabolism of xanthotoxin by Papilio multicaudatus. J Chem Ecol 2006, 32(3):523-536.
• [54]Puinean AM, Foster SP, Oliphant L, Denholm I, Field LM, Millar NS, Williamson MS, Bass C: Amplification of a cytochrome P450 gene is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. PLoS Genet 2010, 6(6):e1000999.
• [55]Despres L, David J, Gallet C: The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 2007, 22(6):298-307.
• [56]Sattar S, Song Y, Anstead JA, Sunkar R, Thompson GA: Cucumis melo microRNA expression profile during aphid herbivory in a resistant and susceptible interaction. Mol Plant-Microbe Interact 2012, 25(6):839-848.
• [57]Sattar S, Addo-Quaye C, Song Y, Anstead JA, Sunkar R, Thompson GA: Expression of small RNA in Aphis gossypii and Its potential role in the resistance interaction with melon. PLoS One 2012, 7(11):e48579.
• [58]Zhang L, Hou D, Chen X, Li D, Zhu L, Zhang Y, Li J, Bian Z, Liang X, Cai X: Exogenous plant MIR168a specifically targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA. Cell Res 2011, 22(1):107-126.
• [59]Dogimont C, Bendahmane A, Chovelon V, Boissot N: Host plant resistance to aphids in cultivated crops: genetic and molecular bases, and interactions with aphid populations. C R Biol 2010, 333(6):566-573.
• [60]Goggin FL, Jia L, Shah G, Hebert S, Williamson VM, Ullman DE: Heterologous expression of the Mi-1.2 gene from tomato confers resistance against nematodes but not aphids in eggplant. Mol Plant-Microbe Interact 2006, 19(4):383-388.
• [61]McHale L, Tan X, Koehl P, Michelmore RW: Plant NBS-LRR proteins: adaptable guards. Genome Biol 2006, 7(4):212. BioMed Central Full Text
• [62]Giordanengo P, Brunissen L, Rusterucci C, Vincent C, Van Bel A, Dinant S, Girousse C, Faucher M, Bonnemain J: Compatible plant-aphid interactions: how aphids manipulate plant responses. C R Biol 2010, 333(6):516-523.
• [63]Habib H, Fazili KM: Plant protease inhibitors: a defense strategy in plants. Biotechnol Mol Biol Rev 2007, 2(3):68-85.
• [64]Bown DP, Wilkinson HS, Gatehouse JA: Differentially regulated inhibitor-sensitive and insensitive protease genes from the phytophagous insect pest, Helicoverpa armigera, are members of complex multigene families. Insect Biochem Mol Biol 1997, 27(7):625-638.
• [65]Ge Z, Wan P, Cheng X, Zhang Y, Li G, Han Z, Bell J: Cloning and characterization of serpin-like genes from the striped rice stem borer. Chilo suppressalis Genome 2013, 56(6):359-366.
• [66]Li Y, Hill CB, Carlson SR, Diers BW, Hartman GL: Soybean aphid resistance genes in the soybean cultivars Dowling and Jackson map to linkage group M. Mol Breed 2007, 19(1):25-34.
• [67]Hill CB, Li Y, Hartman GL: Resistance to the soybean aphid in soybean germplasm. Crop Sci 2004, 44(1):98-106.
• [68]Michel AP, Mian MR, Davila-Olivas NH, Cañas LA: Detached leaf and whole plant assays for soybean aphid resistance: differential responses among resistance sources and biotypes. J Econ Entomol 2010, 103(3):949-957.
• [69]Blankenberg D, Gordon A, Von Kuster G, Coraor N, Taylor J, Nekrutenko A, Galaxy Team: Manipulation of FASTQ data with Galaxy. Bioinformatics 2010, 26(14):1783-1785.
• [70]Martin M: Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet journal 2011, 17(1):10-12.
• [71]Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M: Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21(18):3674-3676.
• [72]Zhi-Liang H, Bao J, Reecy J: CateGOrizer: a web-based program to batch analyze gene ontology classification categories. Online J Bioinformatics 2008, 9:108-112.
• [73]Du Z, Zhou X, Ling Y, Zhang Z, Su Z: agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 2010, 38(suppl 2):W64-W70.
• [74]Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M: KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 1999, 27(1):29-34.
• [75]Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B: Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Meth 2008, 5(7):621-628.
• [76]Bansal R, Mian M, Mittapalli O, Michel AP: Molecular characterization and expression analysis of soluble trehalase gene in Aphis glycines, a migratory pest of soybean. Bull Entomol Res 2013, 1-10.
• [77]Bansal R, Mamidala P, Mian MR, Mittapalli O, Michel AP: Validation of reference genes for gene expression studies in Aphis glycines (Hemiptera: Aphididae). J Econ Entomol 2012, 105(4):1432-1438.
• [78]Schmittgen TD, Livak KJ: Analyzing real-time PCR data by the comparative CT method. Nat Protoc 2008, 3(6):1101-1108.
• [79]Petersen TN, Brunak S, von Heijne G, Nielsen H: SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011, 8(10):785-786.
• [80]Krogh A, Larsson B, Von Heijne G, Sonnhammer EL: Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001, 305(3):567-580.