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3 Biotech

, 8:315 | Cite as

Co-expression network of transcription factors reveal ethylene-responsive element-binding factor as key regulator of wood phenotype in Eucalyptus tereticornis

  • Veeramuthu Dharanishanthi
  • Modhumita Ghosh Dasgupta
Original Article
  • 42 Downloads

Abstract

Suitability of wood biomass for pulp production is dependent on the cellular architecture and composition of secondary cell wall. Presently, systems genetics approach is being employed to understand the molecular basis of trait variation and co-expression network analysis has enabled holistic understanding of complex trait such as secondary development. Transcription factors (TFs) are reported as key regulators of meristematic growth and wood formation. The hierarchical TF network is a multi-layered system which interacts with downstream structural genes involved in biosynthesis of cellulose, hemicelluloses and lignin. Several TFs have been associated with wood formation in tree species such as Populus, Eucalyptus, Picea and Pinus. However, TF-specific co-expression networks to understand the interaction between these regulators are not reported. In the present study, co-expression network was developed for TFs expressed during wood formation in Eucalyptus tereticornis and ethylene-responsive element-binding factor, EtERF2, was identified as the major hub transcript which co-expressed with other secondary cell wall biogenesis-specific TFs such as EtSND2, EtVND1, EtVND4, EtVND6, EtMYB70, EtGRAS and EtSCL8. This study reveals a probable role of ethylene in determining natural variation in wood properties in Eucalyptus species. Understanding this transcriptional regulation underpinning the complex bio-processing trait of wood biomass will complement the Eucalyptus breeding program through selection of industrially suitable phenotypes by marker-assisted selection.

Keywords

Co-expression network Ethylene Regulation Transcription factor Wood formation 

Notes

Acknowledgements

We acknowledge the guidance given by Dr. Jennifer Dewoody, National Forest Genetics Laboratory, USDA Forest Service, Placerville, CA; Dr. Sucheta Tripathy, Structural Biology and Bio-informatics Division, Indian Institute of Chemical Biology, Kolkata, India; Dr. Saravanakumar Selvaraj, Centre for Pharmacology and Toxicology, Hannover Medical School, Hannover, Germany, and Dr. Gayatri Ramakrishnan, Molecular Biophysics Unit, Indian Institute of Science, Bangalore, India, for developing gene regulatory networks. The funding for the research work was provided to Dr. Modhumita Ghosh Dasgupta by Department of Biotechnology, Government of India, under the research project with grant number BT/PR10055/PBD/16/772/2007. The funding support as research fellowship was provided to Dr. Veeramuthu Dharanishanthi by Department of Biotechnology, Government of India.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Supplementary material

13205_2018_1344_MOESM1_ESM.docx (38 kb)
Supplementary material 1 (DOCX 38 KB)
13205_2018_1344_MOESM2_ESM.xls (210 kb)
Supplementary material 2 (XLS 210 KB)

References

  1. Ambavaram MM, Krishnan A, Trijatmiko KR, Pereira A (2011) Coordinated activation of cellulose and repression of lignin biosynthesis pathways in rice. Plant Physiol 155:916–931CrossRefGoogle Scholar
  2. Andersson-Gunnerås S, Hellgren JM, Björklund S, Regan S, Moritz T, Sundberg B (2003) Asymmetric expression of a poplar ACC oxidase controls ethylene production during gravitational induction of tension wood. Plant J 34:339–349CrossRefGoogle Scholar
  3. Andersson-Gunnerås S, Mellerowicz EJ, Love J, Segerman B, Ohmiya Y, Coutinho PM, Nilsson P, Henrissat B, Moritz T, Sundberg B (2006) Biosynthesis of cellulose-enriched tension wood in Populus: global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis. Plant J 45:144–165CrossRefGoogle Scholar
  4. Barros E, Staden CA, Lezar S (2009) A microarray-based method for the parallel analysis of genotypes and expression profiles of wood-forming tissues in Eucalyptus grandis. BMC Biotechnol 9(51):1472–6750Google Scholar
  5. Basnet RK, Carpio DPD, Xiao D, Bucher J, Jin M, Boyle K, Fobert P, Visser RGF, Maliepaard C, Bonnema G (2016) A systems genetics approach identifies gene regulatory networks associated with fatty acid composition in Brassica rapa seed. Plant Physiol 170:568–585CrossRefGoogle Scholar
  6. Baute J, Herman D, Coppens F, De Block J, Slabbinck B, Dell’Acqua M, Pè ME, Maere S, Nelissen H, Inzé D (2016) Combined large-scale phenotyping and transcriptomics in maize reveals a robust growth regulatory network. Plant Physiol 170:1848–1867Google Scholar
  7. Cassan-Wang H, Goue N, Saidi MN, Legay S, Sivadon P, Goffner D, Grima-Pettenati J (2013) Identification of novel transcription factors regulating secondary cell wall formation in Arabidopsis. Front Plant Sci 4:189CrossRefGoogle Scholar
  8. De Maeyer D, Weytjens B, De Raedt L, Marchal K (2016) Network-based analysis of eQTL data to prioritize driver mutations. Genome Biol Evol 8:481–494CrossRefGoogle Scholar
  9. Dharanishanthi V, Ghosh Dasgupta M (2016) Construction of co-expression network based on natural expression variation of xylogenesis-related transcripts in Eucalyptus tereticornis. Mol Biol Rep 43:1129–1146CrossRefGoogle Scholar
  10. Du J, Groover A (2010) Transcriptional regulation of secondary growth and wood formation. J Integr Plant Biol 52:17–27CrossRefGoogle Scholar
  11. Du S, Yamamoto F (2003) Ethylene evolution changes in the stems of Metasequoia glyptostroboides and Aesculus turbinata seedlings in relation to gravity-induced reaction wood formation. Trees Struct Funct 17:.522–528CrossRefGoogle Scholar
  12. Du S, Yamamoto F (2007) An overview of the biology of reaction wood formation. J Integr Plant Biol 49:131–143CrossRefGoogle Scholar
  13. Du Q, Gong C, Wang Q, Zhou D, Yang H, Pan W, Li B, Zhang D (2016) Genetic architecture of growth traits in Populus revealed by integrated quantitative trait locus (QTL) analysis and association studies. New Phytol 209:1067–1082CrossRefGoogle Scholar
  14. Etchells JP, Provost CM, Turner SR (2012) Plant vascular cell division is maintained by an interaction between PXY and ethylene signalling. PLoS Genet 8:e1002997CrossRefGoogle Scholar
  15. Felten J, Sundberg B (2013) Biology, chemistry and ultrastructure of tension wood. In: Fromm J (ed) Cellular aspects of wood formation. Springer, Berlin, pp 203–224CrossRefGoogle Scholar
  16. Felten J, Vahala J, Love J, Gorzsás A, Gerber L, Kumar M, Kangasjärvi J, Sundberg B (2011) Ethylene signaling via ethylene response factors (ERFs) modifies wood development in hybrid aspen. BMC Proc 5:115CrossRefGoogle Scholar
  17. Felten J, Vahala J, Love J, Gorzsas A, Ruggeberg M, Delhomme N et al (2018) Ethylene signaling induces gelatinous layers with typical features of tension wood in hybrid aspen. New Phytol.  https://doi.org/10.1111/nph.15078 Google Scholar
  18. Feltus FA (2014) Systems genetics: a paradigm to improve discovery of candidate genes and mechanisms underlying complex traits. Plant Sci 223:45–48CrossRefGoogle Scholar
  19. Goicoechea M, Lacombe E, Legay S, Mihaljevic S, Rech P, Jauneau A, Lapierre C, Pollet B, Verhaegen D, Chaubet-Gigot N, Grima-Pettenati J (2005) EgMYB2, a new transcriptional activator from Eucalyptus xylem, regulates secondary cell wall formation and lignin biosynthesis. Plant J 43:553–567CrossRefGoogle Scholar
  20. Groover AT, Nieminen K, Helariutta Y, Mansfield SD (2010) Wood formation in Populus. In: Jansson S, Bhalerao RP, Groover AT (eds) Genetics and genomics of Populus. Springer, New York, pp 201–224CrossRefGoogle Scholar
  21. Hefer CA, Mizrachi E, Myburg AA, Douglas CJ, Mansfield SD (2015) Comparative interrogation of the developing xylem transcriptomes of two wood-forming species: Populus trichocarpa and Eucalyptus grandis. New Phytol 206(4):1391–1405CrossRefGoogle Scholar
  22. Hussey SG, Mizrachi E, Spokevicius AV, Bossinger G, Berger DK, Myburg AA (2011) SND2, a NAC transcription factor gene, regulates genes involved in secondary cell wall development in Arabidopsis fibres and increases fibre cell area in Eucalyptus. BMC Plant Biol 11:173CrossRefGoogle Scholar
  23. Hussey SG, Mizrachi E, Creux NM, Myburg AA (2013) Navigating the transcriptional roadmap regulating plant secondary cell wall deposition. Front Plant Sci 4:1–21CrossRefGoogle Scholar
  24. Ingemarsson BSM (1995) Ethylene effects on peroxidases and cell growth patterns in Picea abies hypocotyl cuttings. Physiol Plant 94:211–218CrossRefGoogle Scholar
  25. Ingvarsson PK, Street NR (2011) Association genetics of complex traits in plants. New Phytol 189:909–922CrossRefGoogle Scholar
  26. Jia P, Zhao Z (2014) Network assisted analysis to prioritize GWAS results: principles, methods and perspectives. Hum Genet 133:125–138CrossRefGoogle Scholar
  27. Jokipii-Lukkari S, Delhomme N, Schiffthaler B, Mannapperuma C, Prestele J, Nilsson O, Street NR, Tuominen H (2018) Transcriptional roadmap to seasonal variation in wood formation of Norway Spruce. Plant Physiol 176:2851–2870CrossRefGoogle Scholar
  28. Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30CrossRefGoogle Scholar
  29. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M (2012) KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 40(D1):D109–D114CrossRefGoogle Scholar
  30. Kirst M, Basten CJ, Myburg AA, Zeng ZB, Sederoff RR (2005) Genetic architecture of transcript-level variation in differentiating xylem of a Eucalyptus hybrid. Genetics 169:2295–2303CrossRefGoogle Scholar
  31. Lamara M, Raherison E, Lenz P, Beaulieu J, Bousquet J, MacKay J (2016) Genetic architecture of wood properties based on association analysis and co-expression networks in white spruce. New Phytol 210:240–255CrossRefGoogle Scholar
  32. Legay S, Sivadon P, Blervacq AS, Pavy N, Baghdady A, Tremblay L et al (2010) EgMYB1, an R2R3 MYB transcription factor from eucalyptus negatively regulates secondary cell wall formation in Arabidopsis and poplar. New Phytol 188:774–786CrossRefGoogle Scholar
  33. Li E, Bhargava A, Qiang W, Friedmann MC, Forneris N, Savidge RA, Johnson LA, Mansfield SD, Ellis BE, Douglas CJ (2012) The Class II KNOX gene KNAT7 negatively regulates secondary wall formation in Arabidopsis and is functionally conserved in Populus. New Phytol 194:102–115CrossRefGoogle Scholar
  34. Liu Y, Wei M, Hou C, Lu T, Liu L, Wei H et al (2017) Functional characterization of populus PsnSHN2 in coordinated regulation of secondary wall components in tobacco. Sci Rep 7:42CrossRefGoogle Scholar
  35. Long TA, Benfey PN (2006) Transcription factors and hormones: new insights into plant cell differentiation. Curr Opin Cell Biol 18:710–714CrossRefGoogle Scholar
  36. Love J, Björklund S, Vahala J, Hertzberg M, Kangasjärvi J, Sundberg B (2009) Ethylene is an endogenous stimulator of cell division in the cambial meristem of Populus. Proc Natl Acad Sci USA 106:5984–5989CrossRefGoogle Scholar
  37. Ma R, Xiao Y, Lv Z, Tan H, Chen R, Li Q et al (2017) AP2/ERF Transcription Factor, Ii049, positively regulates lignan biosynthesis in Isatis indigotica through activating salicylic acid signaling and Lignan/Lignin pathway genes. Front Plant Sci 8:1361CrossRefGoogle Scholar
  38. McCarthy RL, Zhong R, Ye ZH (2009) MYB83 is a direct target of SND1 and acts redundantly with MYB46 in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell Physiol 50:1950–1964CrossRefGoogle Scholar
  39. Mizrachi E, Myburg AA (2016) Systems genetics of wood formation. Curr Opin Plant Biol 30:94–100CrossRefGoogle Scholar
  40. Mizrachi E, Verbeke L, Christie N, Fierro AC, Mansfield SD, Davis MF, Gjersing E, Tuskan GA, Montagu MV, de Peer YV, Marchal K, Myburg AA (2017) Network-based integration of systems genetics data reveals pathways associated with lignocellulosic biomass accumulation and processing. Proc Natl Acad Sci 114:1195–1200CrossRefGoogle Scholar
  41. Negishi N, Nanto K, Hayashi K, Onogi S, Kawaoka A (2011) Transcript abundances of LIM transcription factor, 4CL, CAld5H and CesAs affect wood properties in Eucalyptus globulus. Silvae Genet 60:288–296CrossRefGoogle Scholar
  42. Ohashi-Ito K, Fukuda H (2010) Transcriptional regulation of vascular cell fates. Curr Opin Plant Biol 13:670–676CrossRefGoogle Scholar
  43. Phukan UJ, Jeena GS, Tripathi V, Shukla RK (2017) Regulation of apetala2/ethylene response factors in plants. Front Plant Sci.  https://doi.org/10.3389/fpls.2017.00150 Google Scholar
  44. Porth I, Klápště J, Skyba O, Friedmann MC, Hannemann J, Ehlting J, El-Kassaby YA, Mansfield SD, Douglas CJ (2013) Network analysis reveals the relationship among wood properties, gene expression levels and genotypes of natural Populus trichocarpa accessions. New Phytol 200:727–742CrossRefGoogle Scholar
  45. Sakamoto S, Takata N, Oshima Y, Yoshida K, Taniguchi T, Mitsuda N (2016) Wood reinforcement of poplar by rice NAC transcription factor. Sci Rep 6:19925CrossRefGoogle Scholar
  46. Salazar MM, Nascimento LC, Camargo EL, Gonçalves DC, Lepikson Neto J, Marques WL, Teixeira PJ, Mieczkowski P, Mondego JM, Carazzolle MF, Deckmann AC, Pereira GA (2013) Xylem transcription profiles indicate potential metabolic responses for economically relevant characteristics of Eucalyptus species. BMC Genom 14:201CrossRefGoogle Scholar
  47. Schuetz M, Smith R, Ellis B (2013) Xylem tissue speciation, patterning and differentiation mechanisms. J Exp Bot 64:11–31CrossRefGoogle Scholar
  48. Seyfferth C, Wessels B, Jokipii-Lukkari S, Sundberg B, Delhomme N, Felten J, Tuominen H (2018) Ethylene-related gene expression networks in wood formation. Front Plant Sci 9:272CrossRefGoogle Scholar
  49. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504CrossRefGoogle Scholar
  50. Shi R, Wang JP, Lin YC, Li Q, Sun YH, Chen H, Sederoff RR, Chiang VL (2017) Tissue and cell-type co-expression networks of transcription factors and wood component genes in Populus trichocarpa. Planta 245:927–938CrossRefGoogle Scholar
  51. Shinya T, Iwata E, Nakahama K, Fukuda Y, Hayashi K, Nanto K, Rosa AC, Kawaoka A (2016) Transcriptional profiles of hybrid Eucalyptus genotypes with contrasting lignin content reveal that monolignol biosynthesis-related genes regulate wood composition. Front Plant Sci 7:443CrossRefGoogle Scholar
  52. Soler M, Plasencia A, Larbat R, Pouzet C, Jauneau A, Rivas S, Pesquet E, Lapierre C, Truchet I, Grima-Pettenati J (2017) The Eucalyptus linker histone variant EgH1.3 cooperates with the transcription factor EgMYB1 to control lignin biosynthesis during wood formation. New Phytol 213:287–299CrossRefGoogle Scholar
  53. Sundell D, Street NR, Kumar M, Mellerowicz EJ, Kucukoglu M, Johnsson C et al (2017) AspWood: high-spatial-resolution transcriptome profiles reveal uncharacterized modularity of wood formation in Populus tremula. Plant Cell 29:1585–1604CrossRefGoogle Scholar
  54. Thavamanikumar S, Southerton S, Thumma B (2014) RNA-Seq using two populations reveals genes and alleles controlling wood traits and growth in Eucalyptus nitens. PLoS One 9:e101104CrossRefGoogle Scholar
  55. Vahala J, Felten J, Love J, Gorzsas A, Gerber L, Lamminmaki A, Kangasjarvi J, Sundberg B (2013) A genome-wide screen for ethylene-induced ethylene response factors (ERFs) in hybrid aspen stem identifies ERF genes that modify stem growth and wood properties. New Phytol 200:511–522CrossRefGoogle Scholar
  56. Vanholme R, Storme V, Vanholme B, Sundin L, Christensen JH, Goeminne G, Halpin C, Rohde A, Morreel K, Boerjan W (2012) A systems biology view of responses to lignin biosynthesis perturbations in Arabidopsis. Plant Cell 24:3506–3529CrossRefGoogle Scholar
  57. Verbeke LP, Cloots L, Demeester P, Fostier J, Marchal K (2013) EPSILON: An eQTL prioritization framework using similarity measures derived from local networks. Bioinformatics 29:1308–1316CrossRefGoogle Scholar
  58. Wang HZ, Dixon RA (2012) On–off switches for secondary cell wall biosynthesis. Mol Plant 5:297–303CrossRefGoogle Scholar
  59. Xu T, Ma T, Hu Q, Liu J (2015) An integrated database of wood-formation related genes in plants. Sci Rep.  https://doi.org/10.1038/srep11422 Google Scholar
  60. Ye ZH, Zhong R (2015) Molecular control of wood formation in trees. J Exp Bot 66:4119–4131CrossRefGoogle Scholar
  61. Yu H, Soler M, San Clemente H, Mila I, Paiva JA, Myburg AA, Bouzayen M, Grima-Pettenati J, Cassan-Wang H (2015) Comprehensive genome-wide analysis of the Aux/IAA gene family in Eucalyptus: evidence for the role of EgrIAA4 in wood formation. Plant Cell Physiol 56:700–714CrossRefGoogle Scholar
  62. Zhang X, Cal AJ, Borevitz JO (2011) Genetic architecture of regulatory variation in Arabidopsis thaliana. Genome Res 21:725–733CrossRefGoogle Scholar
  63. Zhang J, Nieminen K, Serra JAA, Helariutta Y (2014) The formation of wood and its control. Curr Opin Plant Biol 17:56–63CrossRefGoogle Scholar
  64. Zhong R, Ye ZH (2014) Transcriptional regulation of biosynthesis of cell wall components during Xylem differentiation. In: Fukuda H (ed) Plant cell wall patterning and cell shape. Wiley, Hoboken, pp 351–377Google Scholar
  65. Zhong R, Lee C, Ye ZH (2010) Evolutionary conservation of the transcriptional network regulating secondary cell wall biosynthesis. Trends Plant Sci 15:625–632CrossRefGoogle Scholar
  66. Zinkgraf M, Gerttula S, Groover A (2017) Transcript profiling of a novel plant meristem, the monocot cambium. J Integr Plant Biol 59:436–449CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Division of Plant Biotechnology and CytogeneticsInstitute of Forest Genetics and Tree BreedingCoimbatoreIndia

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