BMC Genomics | |
Transcriptome analysis of Gossypium hirsutum flower buds infested by cotton boll weevil (Anthonomus grandis) larvae | |
Marcio Alves-Ferreira2  Adriana Pinheiro Martinelli6  Maria Fátima Grossi-de-Sa5  Sylvia Silveira6  Leonardo Lima Pepino de Macedo1  Osmundo Brilhante Oliveira-Neto3  Marcelo Ribeiro-Alves4  Sinara Artico2  | |
[1] Embrapa Genetic Resources and Biotechnology, Parque Estação Biológica, PqEB - Av. W5 Norte (final) Caixa Postal 02372, CEP 70770-900 Brasília, DF, Brazil;Department of Genetics, Universidade Federal do Rio de Janeiro - UFRJ Av. Prof. Rodolpho Paulo Rocco, s/n - Prédio do CCS Instituto de Biologia, 2° andar - sala 93, 219410-970 Rio de Janeiro, RJ, Brazil;Department of Biochemistry and Molecular Biology, School of Medicine, FACIPLAC, SIGA AE2, Brasília, DF 72460-000, Brazil;HIV/AIDS Clinical Research Center, Evandro Chagas Clinical Research Institute, Oswaldo Cruz Foundation, Av. Brasil, 4365 - Manguinhos, 21040-360 Rio de Janeiro, RJ, Brazil;University Catholic of Brasilia, Brasília, DF, Brazil;Universidade de São Paulo, USP-CENA, Av. Centenário 303, 13416-903 Piracicaba, SP, Brazil | |
关键词: Laser microdissection (LMD); WRKY FT; Biotic stress; Transcriptome sequencing; Larvae; Cotton; | |
Others : 1136343 DOI : 10.1186/1471-2164-15-854 |
|
received in 2014-04-30, accepted in 2014-09-25, 发布年份 2014 | |
【 摘 要 】
Background
Cotton is a major fibre crop grown worldwide that suffers extensive damage from chewing insects, including the cotton boll weevil larvae (Anthonomus grandis). Transcriptome analysis was performed to understand the molecular interactions between Gossypium hirsutum L. and cotton boll weevil larvae. The Illumina HiSeq 2000 platform was used to sequence the transcriptome of cotton flower buds infested with boll weevil larvae.
Results
The analysis generated a total of 327,489,418 sequence reads that were aligned to the G. hirsutum reference transcriptome. The total number of expressed genes was over 21,697 per sample with an average length of 1,063 bp. The DEGseq analysis identified 443 differentially expressed genes (DEG) in cotton flower buds infected with boll weevil larvae. Among them, 402 (90.7%) were up-regulated, 41 (9.3%) were down-regulated and 432 (97.5%) were identified as orthologues of A. thaliana genes using Blastx. Mapman analysis of DEG indicated that many genes were involved in the biotic stress response spanning a range of functions, from a gene encoding a receptor-like kinase to genes involved in triggering defensive responses such as MAPK, transcription factors (WRKY and ERF) and signalling by ethylene (ET) and jasmonic acid (JA) hormones. Furthermore, the spatial expression pattern of 32 of the genes responsive to boll weevil larvae feeding was determined by “in situ” qPCR analysis from RNA isolated from two flower structures, the stamen and the carpel, by laser microdissection (LMD).
Conclusion
A large number of cotton transcripts were significantly altered upon infestation by larvae. Among the changes in gene expression, we highlighted the transcription of receptors/sensors that recognise chitin or insect oral secretions; the altered regulation of transcripts encoding enzymes related to kinase cascades, transcription factors, Ca2+ influxes, and reactive oxygen species; and the modulation of transcripts encoding enzymes from phytohormone signalling pathways. These data will aid in the selection of target genes to genetically engineer cotton to control the cotton boll weevil.
【 授权许可】
2014 Artico et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150312053758980.pdf | 2194KB | download | |
Figure 6. | 35KB | Image | download |
Figure 5. | 41KB | Image | download |
Figure 1. | 36KB | Image | download |
Figure 3. | 117KB | Image | download |
Figure 2. | 93KB | Image | download |
Figure 1. | 85KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 1.
Figure 5.
Figure 6.
【 参考文献 】
- [1]Wendel JF, Cronn RC: Polyploidy and the evolutionary history of cotton. Adv Agron 2003, 78:139-186.
- [2]Lee JJ, Woodward AW, Chen ZJ: Gene expression changes and early events in cotton fibre development. Ann Bot 2007, 100(7):1391-1401.
- [3]Razaq M, Aslam M, Shad SA, Naeem M: Evaluation of some new promising cotton strains against bollworm complex. Evaluation 2004, 15(3):313-318.
- [4]Dubey NK, Goel R, Ranjan A, Idris A, Singh SK, Bag SK, Chandrashekar K, Pandey KD, Singh PK, Sawant SV: Comparative transcriptome analysis of Gossypium hirsutum L. in response to sap sucking insects: aphid and whitefly. BMC Genomics 2013, 14:241-261. BioMed Central Full Text
- [5]Greenberg SM, Sappington TW, Setamou M, Coleman RJ: Influence of different cotton fruit sizes on boll weevil (Coleoptera: Curculionidae) oviposition and survival to adulthood. Environ Entomol 2003, 33:443-449.
- [6]Martins WFS, Ayres CFJ, Lucena WA: Genetic diversity of Brazilian naturalpopulations of Anthonomus grandis Boheman(Coleoptera: Curculionidae), the major cottonpest in the New World. Genet Mol Res 2007, 6:23-32.
- [7]Oliveira-Neto OB, Batista JAN, Rigden DJ, Franco OL, Fragoso RR, Monteiro ACS, Monnerat RG, Grossi-de-Sa MF: Molecular cloning of a cysteine proteinase cDNA from the cotton boll weevil Anthonomus grandis (Coleoptera: Curculionidae). 2004 Jun;68(6):1235–42. Biosci Biotechnol Biochem 2004, 68(6):1235-1242.
- [8]Dicke M, van Poecke RMP, Boer JG: Inducible indirect defence of plants: from mechanisms to ecological functions. Basic Appl Ecol 2003, 4:27-42.
- [9]Kessler A, Baldwin IT: Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 2002, 53:299-328.
- [10]Erb M, Meldau S, Howe GA: Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 2012, 17:250-259.
- [11]Jones JDG, Dangl JL: The plant immune system. Nature 2006, 444:323-329.
- [12]Wu J, Baldwin IT: New insights into plant response to the attack from insect herbivore. Annu Rev Genet 2010, 44:1-24.
- [13]Ferry N, Edwards MG, Gatehouse JA, Gatehouse AMR: Plant–insect interactions: molecular approaches to insect resistance. Curr Opin Biotechnol 2004, 15:155-161.
- [14]Wei X, Zhang X, Shen D, Wang H, Wu Q, Lu P, Qiu Y, Song J, Zhang Y, Li X: Transcriptome analysis of Barbarea vulgaris infested with diamondback moth (Plutella xylostella) larvae. PlosOne 2013, 8:1-19.
- [15]Mafra V, Martins PK, Francisco CS, Ribeiro-Alves M, Freitas-Astúa J, Machado MA: Candidatus Liberibacter americanus induces significant reprogramming of the transcriptome of the susceptible citrus genotype. BMC Genomics 2013, 14:247. BioMed Central Full Text
- [16]Xu L, Zhu L, Tu L, Liu L, Yuan D, Jin L, Long L, Zhang X: Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNA-Seq-dependent transcriptional analysis and histochemistry. J Exp Bot 2011, 62(15):5607-5621.
- [17]Little D, Gouhier-Darimont C, Bruessow F, Reymond P: Oviposition by pierid butterflies triggers defense responses in Arabidopsis. Plant Physiol 2007, 143:784-800.
- [18]De Vos M, Oosten VRV, van Poecke RMP, Van Pelt JA, Pozo MJ, Mueller MJ, Buchala AJ, Métraux JP, Van Loon LC, Dicke M, Pieterse CMJ: Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. MPMI 2005, 18:923-937.
- [19]Garg R, Patel RK, Tyagi AK, Jain M: De novo assembly of chickpea transcriptome using short reads for gene discovery and marker identification. DNA Res 2011, 18:53-63.
- [20]Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, Baren MJ, Salzberg SL, Wold BJ, Pachter L: Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010, 28:511-515.
- [21]Autran D, Baroux C, Raissig MT, Lenormand T, Wittig M, Grob S, Steimer A, Barann M, Klostermeier UC, Leblanc O, Vielle-Calzada JP, Rosenstiel P, Grimanelli D, Grossniklaus U: Maternal epigenetic pathways control parental contributions to Arabidopsis early embryogenesis. Cell 2011, 145:707-719.
- [22]Morin RD, O’Connor MD, Griffith M, Kuchenbauer F, Delaney A, Prabhu AL, Zhao Y, McDonald H, Zeng T, Hirst M, Eaves CJ, Marra MA: Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res 2008, 18:610-621.
- [23]Tarazona S, García-Alcalde F, Dopazo J, Ferrer A, Conesa A: Differential expression in RNA-seq: A matter of depth. Genome Res 2011, 21:2213-2223.
- [24]Garber M, Grabherr MG, Guttman M, Trapnell C: Computational methods for transcriptome annotation and quantification using RNA-seq. Nat Methods 2011, 8:469-477.
- [25]Pavithra SR, Kumar R, Tatu U: Systems analysis of chaperone networks in the malarial parasite Plasmodium falciparum. PLoS Comput Biol 2007, 14:1701-1715.
- [26]Panstruga R, Parker EJ, Schulze-Lefert P: SnapShot: plant immune response pathways. Cell 2009, 6:978.
- [27]He P, Shan L, Lin NC, Martin GB, Kemmerling B, Nurnberger T, Sheen J: Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in arabidopsis innate immunity. Cell 2006, 125:563-575.
- [28]Kannan P, Pandey D, Gupta AK, Punetha H, Taj G, Kumar A: Expression analysis of MAP2K9 and MAPK6 during pathogenesis of Alternaria blight in Arabidopsis thaliana ecotype Columbia. Mol Biol Rep 2012, 39:4439-4444.
- [29]Takahashi F, Mizoguchi T, Yoshida R, Ichimura K, Shinozaki K: Calmodulin-dependent activation of MAP kinase for ROS homeostasis in arabidopsis. Mol Cell 2011, 41:649-660.
- [30]Ma W, Smigel A, Tsai Y, Braam J, Berkowitz GA: Innate immunity signaling: cytosolic Ca2+ elevation is linked to downstream nitric oxide generation through the action of calmodulin or a calmodulin-like protein. Plant Physiol 2008, 148:818-828.
- [31]Libault M, Wan J, Czechowski T, Udvardi M, Stacey G: Identification of 118 Arabidopsis transcription factor and 30 ubiquitin-ligase genes responding to chitin, a plant-defense elicitor. Mol Plant Microbe Interact 2007, 20:900-911.
- [32]Rushton PJ, Somssich IE, Ringler P, Shen QJ: WRKY transcription factors. Trends Plant Sci 2010, 15:247-258.
- [33]Eulgem T, Somssich IE: Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 2007, 10:366-371.
- [34]Pandey SP, Somssich IE: The role of WRKY transcription factors in plant immunity. Plant Physiol 2009, 150:1648-1655.
- [35]Barah P, Winge P, Kusnierczyk A, Tran DH, Bones AM: Molecular signatures in arabidopsis thaliana in response to insect attack and bacterial infection. Plos One 2013, 8:1-24.
- [36]Kaur H, Heinzel N, Schottner M, Baldwin IT, Galis I: R2R3-NaMYB8 regulates the accumulation of phenylpropanoid-polyamine conjugates, which are essential for local and systemic defense against insect herbivores in Nicotiana attenuata. Plant Physiol 2010, 152:1731-1747.
- [37]Verk MC, Gatz C, Linthorst HJM: Transcriptional regulation of plant defense responses. Adv Bot Res 2009, 51:397-438.
- [38]Nakashima K, Tran LSP, Nguyen DV, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K: Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 2007, 51:617-630.
- [39]Ehlting J, Chowrira SG, Mattheus N, Aeschliman DA, Arimura GI, Bohlmann J: Comparative transcriptome analysis of Arabidopsis thaliana infested by diamondback moth (Plutella xylostella) larvae reveals signatures of stress response, secondary metabolism, and signalling. BMC Genomics 2008, 9:154. BioMed Central Full Text
- [40]Collinge M, Boller T: Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding. Plant Mol Biol 2001, 46:521-529.
- [41]Hirsch S, Oldroyd GED: GRAS-domain transcription factors that regulate plant development. Plant Signal Behav 2009, 8:698-700.
- [42]Day RB, Shibuya N, Minami E: Identification and characterization of two new members of the GRAS gene family in rice responsive to N-acetylchitooligosaccharide elicitor. Biochim Biophys Acta 2003, 1625:261-268.
- [43]Liu X, Williams CE, Nemacheck JA, Wang H, Subramanyam S, Zheng C, Chen MS: Reactive oxygen species are involved in plant defense against a gall midge. Plant Physiol 2010, 152:985-999.
- [44]Ndamukong I, Abdallat AA, Thurow C, Fode B, Zander M, Weigel R, Gatz C: SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription. Plant J 2007, 50:128-139.
- [45]Smith JL, De Moraes CM, Mescher MC: Jasmonate- and salicylate-mediated plant defense responses to insect herbivores, pathogens and parasitic plants. Pest Manag Sci 2009, 65:497-503.
- [46]Saito S, Hirai N, Matsumoto C, Ohigashi H, Ohta D, Sakata K, Mizutani M: Arabidopsis CYP707As Encode (1)-Abscisic Acid 8-Hydroxylase, a key enzyme in the oxidative catabolism of abscisic acid. Plant Physiol 2004, 134:1439-1449.
- [47]An SH, Sohn KH, Choi HW, Hwang IS, Lee SC, Hwang BK: Pepper pectin methylesterase inhibitor protein CaPMEI1 is required for antifungal activity, basal disease resistance and abiotic stress tolerance. Planta 2008, 228:61-78.
- [48]Kogovsek P, Pompe-Novaka M, Baeblera S, Rottera A, Gowb L, Grudena K, Fosterb GD, Boonhamc N, Ravnikar M: Aggressive and mild Potato virus Y isolates trigger different specific responses in susceptible potato plants. Plant Pathol 2010, 59:1121-1132.
- [49]Umate P: Genome-wide analysis of lipoxygenase gene family in Arabidopsis and rice. Plant Signal Behav 2011, 3:335-338.
- [50]Xu L, Zhu L, Tu L, Liu L, Yuan D, Jin L, Long L, Zhang X: Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNA-Seq-dependent transcriptional analysis and histochemistry. J Exp Bot 2011, 23:1-15.
- [51]Santos RC, Marcellino LH, Monnerat RG, Gander ES: Mechanical damage in cotton buds caused by the boll weevil. Pesq Agropec Bras Brasília 2003, 38:1351-1356.
- [52]Liebrand TWH, van den Berga GCM, Zhanga Z, Smita P, Cordewenerb JHG, America AHP, Sklenard J, Jonesd AME, Tamelinga WIL, Robatzekd S, Thommaa BPHJ, Joostena MHAJ: Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proc Natl Acad Sci U S A 2013, 24:10010-10015.
- [53]Liu J, Elmore LM, Lin ZD, Coaker G: A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe 2011, 2:137-146.
- [54]Son GH, Wan J, Kim HJ, Nguyen XC, Chung WS, Hong JC, Stacey G: Ethylene-Responsive Element-Binding Factor 5, ERF5, Is involved in chitin-induced innate immunity response. Mol Plant Microbe Interact 2012, 25:48-60.
- [55]McGrath KC, Dombrecht B, Manners JM, Schenk PM, Edgar CI, Maclean DJ, Scheible W, Udvardi MK, Kazan K: Repressor- and activator-type ethylene response factors functioning in jasmonate signaling and disease resistance identified via a genome-wide screen of arabidopsis transcription factor gene expression. Plant Physiol 2005, 139:949-959.
- [56]Hu Y, Donga Q, Yua D: Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Sci 2012, 185:288-297.
- [57]Rasmussen MW, Roux M, Petersen M, Mundy J: MAP kinase cascades in Arabidopsis innate immunity. Front Plant Sci 2012, 24:169.
- [58]Asai T, Tena G, Plotnikova J, Willmann MR, Chiu W, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J: MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 2001, 415:977-983.
- [59]Howe GA, Jander G: Plant immunity to insect herbivores. Annu Rev Plant Biol 2008, 59:41-66.
- [60]Torres MA, Dangl JL, Jones JDG: Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci U S A 2002, 99:517-522.
- [61]Leitner M, Boland W, Mithöfer A: Direct and indirect defences induced by piercing-sucking and chewing herbivores in Medicago truncatula. New Phytol 2005, 167:597-606.
- [62]Bostock RM: Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol 2005, 43:545-580.
- [63]O'Donnell PJ, Calvert C, Atzorn R, Wasternack C, Leyser HM, Bowles DJ: Ethylene as a signal mediating the wound response of tomato plants. Science 1996, 274:1914-1917.
- [64]Laudert D, Weiler EW: Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signalling. Plant J 1998, 5:675-684.
- [65]Schmelz EA, Alborn HT, Banchio E, Tumlinson JH: Quantitative relationships between induced jasmonic acid levels and volatile emission in Zea mays during Spodoptera exigua herbivory. Planta 2003, 216:665-673.
- [66]von Dahl CC, Winz RA, Halitschke R, Kuhnemann F, Gase K, Baldwin IT: Tuning the herbivore-induced ethylene burst: the role of transcript accumulation and ethylene perception in Nicotiana attenuata. Plant J 2007, 51:293-307.
- [67]Liu Y, Schiff M, Serino G, Deng X-W, Dinesh-Kumar SP: Role of SCF Ubiquitin-Ligase and the COP9 Signalosome in the N Gene–Mediated Resistance Response to Tobacco mosaic virus. Plant Cell 2002, 14:1483-1496.
- [68]Yang C-W, Lamothe RG, Ewan RA, Rowland O, Yoshioka H, Shenton M, Ye H, O’Donnell E, Jones JDG, Sadanandoma A: The E3 ubiquitin ligase activity of arabidopsis PLANT U-BOX17 and its functional tobacco homolog ACRE276 are required for cell death and defense. Plant Cell 2006, 18:1084-1098.
- [69]Trujillo M, Ichimura K, Casais C, Shirasu K: Negative regulation of PAMP-triggered immunity by an E3 ubiquitin ligase triplet in Arabidopsis. Curr Biol 2008, 18:1396-1401.
- [70]Hubert DA, Tornero P, Belkhadir Y, Krishna P, Takahashi A, Shirasu K, Dangl JL: Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. EMBO J 2003, 22:5679-5689.
- [71]Takahashi A, Casais C, Ichimura K, Shirasu K: HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc Natl Acad Sci U S A 2003, 100:11777-11782.
- [72]Seo Y-S, Lee S-K, Song M-Y, Suh J-P, Hahn T-R, Ronald P, Jeon J-S: The HSP90-SGT1-RAR1 molecular chaperone complex: a core modulator in plant immunity. J Plant Biol 2008, 51:1-10.
- [73]Lu R, Malcuit I, Moffett P, Ruiz MT, Peart J, Wu AJ, Rathjen JP, Bendahmane A, Day L, Baulcombe DC: High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J 2003, 22:5690-5699.
- [74]Liu Y, Burch-Smith T, Schiff M, Feng S, Dinesh-Kumar SP: Molecular chaperone Hsp90 associates with resistance protein N and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. J Biol Chem 2004, 279:2101-2108.
- [75]Monnerat RG, Dias SC, Oliveira-Neto OB, Nobre SD, Silva-Werneck JO, Grossi de Sá MF: Criação massal do bicudo do algodoeiro Anthonomus grandis em laboratório. 2000. [Comunicado Técnico. Embrapa Recursos Genéticos e Biotecnologia]
- [76]Schroeder A, Mueller O, Stocker S, Salowsky R, Leiber M, Gassmann M, Lightfoot S, Menzel W, Granzow M, Ragg T: The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol 2006, 7:3. BioMed Central Full Text
- [77]Xie F, Sun G, Stiller JW, Zhang B: Genome-wide functional analysis of the cotton transcriptome by creating an integrated EST database. Plos One 2011, 6:1-12.
- [78]Li H, Durbin R: Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 2009, 25:1754-1760.
- [79]Wang L, Feng Z, Wang X, Wang X, Zhang X: DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 2010, 26:136-138.
- [80]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 2001, 21:3674-3676.
- [81]Alexa A, Rahnenfuhrer J, Lengauer T: Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 2006, 22:1600-1607.
- [82]Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M: MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 2004, 6:914-939.
- [83]Rozen S, Skaletsky H: Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 2000, 132:365-386.
- [84]Scanlon MJ, Ohtsu K, Timmermans MC, Schnable PS: Laser microdissection-mediated isolation and in vitro transcriptional amplification of plant RNA. Curr Protoc Mol Biol 2009, Chapter 25:Unit 25A.3.
- [85]Zhao S, Fernald RD: Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 2005, 12:1047-1064.
- [86]Artico S, Nardeli SM, Brilhante O, Grossi-de-Sa MF, Alves-Ferreira M: Identification and evaluation of new reference genes in Gossypium hirsutum for accurate normalization of real-time quantitative RT-PCR data. BMC Plant Biol 2010, 10:49. BioMed Central Full Text
- [87]Pfaffl MW, Horgan GW, Dempfle L: Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30:2-10.
- [88]Bailey TL, Williams N, Misleh C, Li WW: MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 2006, 34:W369-W373.
- [89]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 10:2731-2739.
- [90]Whelan S, Goldman N: A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 2001, 5:691-699.
- [91]Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O: New algorithms and methods to estimate maximum-likelihood phylogenies: as sessing the performance of PhyML 3.0. Syst Biol 2010, 59(3):307-321.