Large-scale transcriptional profiling of lignified tissues in Tectona grandis

Springer Science and Business Media LLC - Tập 15 - Trang 1-21 - 2015
Esteban Galeano1, Tarcísio Sales Vasconcelos1, Mabel Vidal2, Maria Katherine Mejia-Guerra2, Helaine Carrer1
1Laboratório de Biotecnologia Agrícola (CEBTEC), Departamento de Ciências Biológicas, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, Piracicaba, Brazil
2CAPS Computational Biology Laboratory (CCBL), Center for Applied Plant Sciences, Ohio State University, Columbus, United States

Tóm tắt

Currently, Tectona grandis is one of the most valuable trees in the world and no transcript dataset related to secondary xylem is available. Considering how important the secondary xylem and sapwood transition from young to mature trees is, little is known about the expression differences between those successional processes and which transcription factors could regulate lignin biosynthesis in this tropical tree. Although MYB transcription factors are one of the largest superfamilies in plants related to secondary metabolism, it has not yet been characterized in teak. These results will open new perspectives for studies of diversity, ecology, breeding and genomic programs aiming to understand deeply the biology of this species. We present a widely expressed gene catalog for T. grandis using Illumina technology and the de novo assembly. A total of 462,260 transcripts were obtained, with 1,502 and 931 genes differentially expressed for stem and branch secondary xylem, respectively, during age transition. Analysis of stem and branch secondary xylem indicates substantial similarity in gene ontologies including carbohydrate enzymes, response to stress, protein binding, and allowed us to find transcription factors and heat-shock proteins differentially expressed. TgMYB1 displays a MYB domain and a predicted coiled-coil (CC) domain, while TgMYB2, TgMYB3 and TgMYB4 showed R2R3-MYB domain and grouped with MYBs from several gymnosperms and flowering plants. TgMYB1, TgMYB4 and TgCES presented higher expression in mature secondary xylem, in contrast with TgMYB2, TgHsp1, TgHsp2, TgHsp3, and TgBi whose expression is higher in young lignified tissues. TgMYB3 is expressed at lower level in secondary xylem. Expression patterns of MYB transcription factors and heat-shock proteins in lignified tissues are dissimilar when tree development was evaluated, obtaining more expression of TgMYB1 and TgMYB4 in lignified tissues of 60-year-old trees, and more expression in TgHsp1, TgHsp2, TgHsp3 and TgBi in stem secondary xylem of 12-year-old trees. We are opening a door for further functional characterization by reverse genetics and marker-assisted selection with those genes. Investigation of some of the key regulators of lignin biosynthesis in teak, however, could be a valuable step towards understanding how rigidity of teak wood and extractives content are different from most other woods. The obtained transcriptome data represents new sequences of T. grandis deposited in public databases, representing an unprecedented opportunity to discover several related-genes associated with secondary xylem such as transcription factors and stress-related genes in a tropical tree.

Tài liệu tham khảo

Bhat KM, Priya PB, Rugmini P. Characterisation of juvenile wood in teak. Wood Sci Technol. 2001;34:517–32. Jain A, Ansari S a. Quantification by allometric equations of carbon sequestered by Tectona grandis in different agroforestry systems. J For Res. 2013;24:699–702. Shukla SR, Viswanath S. Comparative study on growth, wood quality and financial returns of teak (Tectona grandis L.f.) managed under three different agroforestry practices. Agrofor Syst. 2014;88:331–41. Bhat KM, Nair KKN, Bhat KV, Muralidharan EM, Sharma JK. Quality timber products of Teak from sustainable forest management. In Proc Int Conf Qual Timber Prod Teak from Sustain For Manag Peechi, India, 2–5 December 2003. Peechi: Kerala Forest Research Institute; 2005. p. 669. Goh DKS, Monteuuis O. Rationale for developing intensive teak clonal plantations, with special reference to Sabah. Bois Forêts des Trop. 2005;285:5–15. Keogh RM: The Future of Teak and the High-Grade Tropical Hardwood Sector. Rome: FAO; 2009(September). Kollert W, Cherubini L: Teak Resources and Market Assessment 2010 (Tectona Grandis Linn. F.). Volume 2010. Rome: FAO; 2012(March). Shrestha MK, Volkaert H, Van Der Straeten D. Assessment of genetic diversity in Tectona grandis using amplified fragment length polymorphism markers. Can J For Res. 2005;35:1017–22. Verhaegen D, Ofori D, Fofana I, Poitel M, Vaillant A. Development and characterization of microsatellite markers in Tectona grandis (Linn. f). Mol Ecol Notes. 2005;5:945–7. Fofana IJ, Ofori D, Poitel M, Verhaegen D. Diversity and genetic structure of teak (Tectona grandis L.f) in its natural range using DNA microsatellite markers. New For. 2009;37:175–95. Sreekanth PM, Balasundaran M, Nazeem P a, Suma TB. Genetic diversity of nine natural Tectona grandis L.f. populations of the Western Ghats in Southern India. Conserv Genet. 2012;13:1409–19. Lyngdoh N, Joshi G, Ravikanth G, Vasudeva R, Shaanker RU. Changes in genetic diversity parameters in unimproved and improved populations of teak (Tectona grandis L.f.) in Karnataka state, India. J Genet. 2013;92:141–5. Minn Y, Prinz K, Finkeldey R. Genetic variation of teak (Tectona grandis Linn. f.) in Myanmar revealed by microsatellites. Tree Genet Genomes. 2014;10:1435–49. Chaffey N. Why is there so little research into the cell biology of the secondary vascular system of trees? New Phytol. 2002;153:213–23. Dharmawardhana P, Brunner AM, Strauss SH. Genome-wide transcriptome analysis of the transition from primary to secondary stem development in Populus trichocarpa. BMC Genomics. 2010;11:150. Liu L, Filkov V, Groover A. Modeling transcriptional networks regulating secondary growth and wood formation in forest trees. Physiol Plant. 2014;151:156–63. Bhat KM, Indira EP: Effect of Faster Growth on Timber Quality of Teak. Thrissur: Kerala Forest Research Institute; 1997(December). Goh DKS, Chaix G, Baillères H, Monteuuis O. Mass production and quality control of teak clones for tropical plantations : The Yayasan Sabah Group and CIRAD Joint Project as a case study. Bois Forêts des Trop. 2007;293:65–77. Yang S-H, van Zyl L, No E-G, Loopstra C a. Microarray analysis of genes preferentially expressed in differentiating xylem of loblolly pine (Pinus taeda). Plant Sci. 2004;166:1185–95. Gordo SMC, Pinheiro DG, Moreira ECO, Rodrigues SM, Poltronieri MC, de Lemos OF, et al. High-throughput sequencing of black pepper root transcriptome. BMC Plant Biol. 2012;12:168. Schliesky S, Gowik U, Weber APM, Bräutigam A. RNA-Seq Assembly - Are We There Yet? Front Plant Sci. 2012;3(September):220. Ueno S, Klopp C, Leplé JC, Derory J, Noirot C, Léger V, et al. Transcriptional profiling of bud dormancy induction and release in oak by next-generation sequencing. BMC Genomics. 2013;14:236. Wilkins AP. Sapwood, heartwood and bark thickness of silviculturally treated Eucalyptus grandis. Wood Sci Technol. 1991;25:415–23. Schrader J, Nilsson J, Mellerowicz E, Berglund A, Nilsson P, Hertzberg M. A High-Resolution Transcript Profile across the Wood-Forming Meristem of Poplar Identifies Potential Regulators of Cambial Stem Cell Identity. Plant Cell. 2004;16(September):2278–92. Qiu Q, Ma T, Hu Q, Liu B, Wu Y, Zhou H, et al. Genome-scale transcriptome analysis of the desert poplar, Populus euphratica. Tree Physiol. 2011;31:452–61. Bao H, Li E, Mansfield SD, Cronk QCB, El-Kassaby Y a, Douglas CJ. The developing xylem transcriptome and genome-wide analysis of alternative splicing in Populus trichocarpa (black cottonwood) populations. BMC Genomics. 2013;14:359. Mizrachi E, Hefer C a, Ranik M, Joubert F, Myburg A a. De novo assembled expressed gene catalog of a fast-growing Eucalyptus tree produced by Illumina mRNA-Seq. BMC Genomics. 2010;11:681. Bedon F, Grima-Pettenati J, Mackay J. Conifer R2R3-MYB transcription factors: sequence analyses and gene expression in wood-forming tissues of white spruce (Picea glauca). BMC Plant Biol. 2007;7:17. Pavy N, Boyle B, Nelson C, Paule C, Giguère I, Caron S, et al. Identification of conserved core xylem gene sets: conifer cDNA microarray development, transcript profiling and computational analyses. New Phytol. 2008;180:766–86. Bai X, Rivera-Vega L, Mamidala P, Bonello P, Herms D a, Mittapalli O. Transcriptomic signatures of ash (Fraxinus spp.) phloem. PLoS One. 2011;6, e16368. Zhong R, Lee C, Zhou J, McCarthy RL, Ye Z-H. A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell. 2008;20:2763–82. Zhao Q, Dixon R a. Transcriptional networks for lignin biosynthesis: more complex than we thought? Trends Plant Sci. 2011;16:227–33. Rogers L a, Campbell MM. The genetic control of lignin deposition during plant growth and development. New Phytol. 2004;164:17–30. Blankenberg D, Gordon A, Von Kuster G, Coraor N, Taylor J, Nekrutenko A. Manipulation of FASTQ data with Galaxy. Bioinformatics. 2010;26:1783–5. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013;8:1494–512. Rubio V, Linhares F, Solano R, Martín a C, Iglesias J, Leyva A. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev. 2001;15:2122–33. Matus JT, Aquea F, Arce-Johnson P. Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biol. 2008;8:83. Millar A a, Gubler F. The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell. 2005;17:705–21. Zenoni S, Ferrarini A, Giacomelli E, Xumerle L, Fasoli M, Malerba G, et al. Characterization of Transcriptional Complexity during Berry Development in Vitis vinifera Using RNA-Seq 1 [W]. Plant Physiol. 2010;152(April):1787–95. Roberts A, Pimentel H, Trapnell C, Pachter L. Identification of novel transcripts in annotated genomes using RNA-Seq. Bioinformatics. 2011;27:2325–9. Mutz K-O, Heilkenbrinker A, Lönne M, Walter J-G, Stahl F. Transcriptome analysis using next-generation sequencing. Curr Opin Biotechnol. 2013;24:22–30. Gangopadhyay G, Gangopadhyay SB, Poddar R, Gupta S, Mukherjee KK. Micropropagation TEAK genetic fidelity.pdf. Biol Plant. 2003;46:459–61. Fofana IJ, Lidah YJ, Diarrassouba N, N’guetta SPA, Sangare A, Verhaegen D. Genetic structure and conservation of Teak (Tectona grandis) plantations in Côte d’ Ivoire, revealed by site specific recombinase (SSR). Trop Conserv Sci. 2008;1:279–92. Alcântara BK, Veasey EA. Genetic diversity of teak (Tectona grandis L. f.) from different provenances using microsatellite markers. Rev Árvore. 2013;37:747–58. Tiwari A, Kumar P, Chawhaan PH, Singh S, Ansari SA. Carbonic anhydrase in Tectona grandis : kinetics, stability, isozyme analysis and relationship with photosynthesis. Tree Physiol. 2006;26:1067–73. Lacret R, Varela RM, Molinillo JMG, Nogueiras C, Macías F a. Anthratectone and naphthotectone, two quinones from bioactive extracts of Tectona grandis. J Chem Ecol. 2011;37:1341–8. Quiala E, Cañal MJ, Rodríguez R, Yagüe N, Chávez M, Barbón R, et al. Proteomic profiling of Tectona grandis L. leaf. Proteomics. 2012;12:1039–44. Balogun a O, Lasode O a, McDonald a G. Devolatilisation kinetics and pyrolytic analyses of Tectona grandis (teak). Bioresour Technol. 2014;156:57–62. Gill B, Yedi Y, BIR S. Cytopalynological studies in woody members of family Verbenaceae from north-west and central India. J Indian Bot Soc. 1983;62:235–44. Ohri D, Kumar a. Nuclear DNA Amounts in Some Tropical Hardwoods. Caryologia. 1986;39:303–7. Gong W, Shen Y, Ma L, Pan Y, Du Y, Wang D, et al. Genome-Wide ORFeome Cloning and Analysis of Arabidopsis Transcription Factor Genes. Plant Physiol. 2004;135(June):773–82. Wu J, Wang L, Li L, Wang S. De novo assembly of the common bean transcriptome using short reads for the discovery of drought-responsive genes. PLoS One. 2014;9, e109262. Wei K, Wang L-Y, Wu L-Y, Zhang C-C, Li H-L, Tan L-Q, et al. Transcriptome Analysis of Indole-3-Butyric Acid-Induced Adventitious Root Formation in Nodal Cuttings of Camellia sinensis (L.). PLoS One. 2014;9, e107201. Li M-Y, Tan H-W, Wang F, Jiang Q, Xu Z-S, Tian C, et al. De Novo Transcriptome Sequence Assembly and Identification of AP2/ERF Transcription Factor Related to Abiotic Stress in Parsley (Petroselinum crispum). PLoS One. 2014;9, e108977. Tang X, Xiao Y, Lv T, Wang F, Zhu Q, Zheng T, et al. High-Throughput Sequencing and De Novo Assembly of the Isatis indigotica Transcriptome. PLoS One. 2014;9, e102963. Villar E, Klopp C, Noirot C, Novaes E, Kirst M, Plomion C, et al. RNA-Seq reveals genotype-specific molecular responses to water deficit in eucalyptus. BMC Genomics. 2011;12:538. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson D a, Amit I. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011;29:644–52. Compeau PEC, Pevzner P a, Tesler G. How to apply de Bruijn graphs to genome assembly. Nat Biotechnol. 2011;29:987–91. Martin J a, Wang Z. Next-generation transcriptome assembly. Nat Rev Genet. 2011;12:671–82. Rao G, Sui J, Zeng Y, He C, Duan A, Zhang J. De Novo Transcriptome and Small RNA Analysis of Two Chinese Willow Cultivars Reveals Stress Response Genes in Salix matsudana. PLoS One. 2014;9, e109122. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11:R106. 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;26:136–8. Garber M, Grabherr MG, Guttman M, Trapnell C. Computational methods for transcriptome annotation and quantification using RNA-seq. Nat Methods. 2011;8:469–77. Kvam VM, Liu P, Si Y. A comparison of statistical methods for detecting differentially expressed genes from RNA-seq data. Am J Bot. 2012;99:248–56. Yang SS, Tu ZJ, Cheung F, Xu WW, Lamb JFS, Jung H-JG, et al. Using RNA-Seq for gene identification, polymorphism detection and transcript profiling in two alfalfa genotypes with divergent cell wall composition in stems. BMC Genomics. 2011;12:199. Sun Q, Zhou G, Cai Y, Fan Y, Zhu X, Liu Y, et al. Transcriptome analysis of stem development in the tumourous stem mustard Brassica juncea var. tumida Tsen et Lee by RNA sequencing. BMC Plant Biol. 2012;12:53. Prassinos C, Ko J-H, Yang J, Han K-H. Transcriptome profiling of vertical stem segments provides insights into the genetic regulation of secondary growth in hybrid aspen trees. Plant Cell Physiol. 2005;46:1213–25. Kakumanu A, Ambavaram MMR, Klumas C, Krishnan A, Batlang U, Myers E, et al. Effects of drought on gene expression in maize reproductive and leaf meristem tissue revealed by RNA-Seq. Plant Physiol. 2012;160:846–67. Smith AM. Prospects for increasing starch and sucrose yields for bioethanol production. Plant J. 2008;54:546–58. Eda M, Ishimaru M, Tada T, Sakamoto T, Kotake T, Tsumuraya Y, et al. Enzymatic activity and substrate specificity of recombinant tomato beta-galactosidase 1. J Plant Physiol. 2014;171:1454–60. Bobeničová M, Valko M, Brezová V, Dvoranová D. UVA generated free radicals in irinotecan (CPT-11) in the presence of copper ions. J Photochem Photobiol A Chem. 2014;290:125–38. Matsuo K, Sasaki E, Higuchi S, Takai S, Tsuneyama K, Fukami T, et al. Involvement of oxidative stress and immune- and inflammation-related factors in azathioprine-induced liver injury. Toxicol Lett. 2014;224:215–24. Chast F: A Brief History of Drugs: From Plant Extracts to DNA Technology. In Pract Med Chem. Third Edit. Edited by Wermuth CG. San Diego, CA: Academic Press; 2008;1:3–28. Souleyre EJF, Marshall SDG, Oakeshott JG, Russell RJ, Plummer KM, Newcomb RD. Biochemical characterisation of MdCXE1, a carboxylesterase from apple that is expressed during fruit ripening. Phytochemistry. 2011;72:564–71. Chae HJ, Ke N, Kim HR, Chen S, Godzik A, Dickman M, et al. Evolutionarily conserved cytoprotection provided by Bax Inhibitor-1 homologs from animals, plants, and yeast. Gene. 2003;323:101–13. Ishikawa T, Uchimiya H, Kawai-Yamada M: The Role of Plant Bax Inhibitor-1 in Suppressing H2O 2-Induced Cell Death. 1st edition. Volume 527. Elsevier Inc.; 2013. Isbat M, Zeba N, Kim SR, Hong CB. A BAX inhibitor-1 gene in Capsicum annuum is induced under various abiotic stresses and endows multi-tolerance in transgenic tobacco. J Plant Physiol. 2009;166:1685–93. Huang G, Li T, Li X, Tan D, Jiang Z, Wei Y, et al. Comparative Transcriptome Analysis of Climacteric Fruit of Chinese Pear (Pyrus ussuriensis) Reveals New Insights into Fruit Ripening. PLoS One. 2014;9, e107562. Zhong R, Richardson E a, Ye Z-H. The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell. 2007;19:2776–92. Ko J-H, Kim W-C, Han K-H. Ectopic expression of MYB46 identifies transcriptional regulatory genes involved in secondary wall biosynthesis in Arabidopsis. Plant J. 2009;60:649–65. Bhargava A, Mansfield SD, Hall HC, Douglas CJ, Ellis BE. MYB75 functions in regulation of secondary cell wall formation in the Arabidopsis inflorescence stem. Plant Physiol. 2010;154:1428–38. Kim W-C, Ko J-H, Kim J-Y, Kim J-M, Bae H-J, Han K-H. MYB46 directly regulates the gene expression of secondary wall-associated cellulose synthases in Arabidopsis. Plant J. 2012;73:26–36. Fornalé S, Shi X, Chai C, Encina A, Irar S, Capellades M, et al. ZmMYB31 directly represses maize lignin genes and redirects the phenylpropanoid metabolic flux. Plant J. 2010;64:633–44. Ma Q-H, Wang C, Zhu H-H. TaMYB4 cloned from wheat regulates lignin biosynthesis through negatively controlling the transcripts of both cinnamyl alcohol dehydrogenase and cinnamoyl-CoA reductase genes. Biochimie. 2011;93:1179–86. Patzlaff A, McInnis S, Courtenay A, Surman C, Newman LJ, Smith C, et al. Characterisation of a pine MYB that regulates lignification. Plant J. 2003;36:743–54. Bomal C, Bedon F, Caron S, Mansfield SD, Levasseur C, Cooke JEK, et al. Involvement of Pinus taeda MYB1 and MYB8 in phenylpropanoid metabolism and secondary cell wall biogenesis: a comparative in planta analysis. J Exp Bot. 2008;59:3925–39. Goicoechea M, Lacombe E, Legay S, Mihaljevic S, Rech P, Jauneau A, et al. EgMYB2, a new transcriptional activator from Eucalyptus xylem, regulates secondary cell wall formation and lignin biosynthesis. Plant J. 2005;43:553–67. Legay S, Lacombe E, Goicoechea M, Brière C, Séguin A, Mackay J, et al. Molecular characterization of EgMYB1, a putative transcriptional repressor of the lignin biosynthetic pathway. Plant Sci. 2007;173:542–9. Karpinska B, Karlsson M, Srivastava M, Stenberg A, Schrader J, Sterky F, et al. MYB transcription factors are differentially expressed and regulated during secondary vascular tissue development in hybrid aspen. Plant Mol Biol. 2004;56:255–70. McCarthy RL, Zhong R, Fowler S, Lyskowski D, Piyasena H, Carleton K, et al. The poplar MYB transcription factors, PtrMYB3 and PtrMYB20, are involved in the regulation of secondary wall biosynthesis. Plant Cell Physiol. 2010;51:1084–90. Deepak MS, Sinha SK, Rao RV. Tree-ring analysis of teak (Tectona grandis L. f.) from Western Ghats of India as a tool to determine drought years. Emirates J Food Agric. 2010;22:388–97. Salzman RA, Fujita T, Hasegawa PM. An Improved RNA Isolation Method for Plant Tissues Containing High Levels of Phenolic Compounds or Carbohydrates. Plant Mol Biol Report. 1999;17:11–7. 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;21:3674–6. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30:2725–9. Galeano E, Vasconcelos TS, Ramiro DA, De Martin VDF, Carrer H. Identification and validation of quantitative real-time reverse transcription PCR reference genes for gene expression analysis in teak (Tectona grandis L.f.). BMC Res Notes. 2014;7:464.