Abstract
A multi-tiered transcriptional network regulates xylem differentiation and secondary cell wall (SCW) formation in plants, with evidence of both conserved and lineage-specific SCW network architecture. We aimed to elucidate the roles of selected R2R3-MYB transcription factors (TFs) linked to Eucalyptus wood formation by identifying genome-wide TF binding sites and direct target genes through an improved DAP-seq protocol combined with machine learning for target gene assignment (DAP-seq-ML). We applied this to five TFs including a well-studied SCW master regulator (EgrMYB2; homolog of AtMYB83), a repressor of lignification (EgrMYB1; homolog of AtMYB4), a TF affecting SCW thickness and vessel density (EgrMYB137; homolog of PtrMYB074) and two TFs with unclear roles in SCW regulation (EgrMYB135 and EgrMYB122). Each DAP-seq TF peak set (average 12,613 peaks) was enriched for canonical R2R3-MYB binding motifs. To improve the reliability of target gene assignment to peaks, a random forest classifier was developed from Arabidopsis DAP-seq, RNA-seq, chromatin, and conserved noncoding sequence data which demonstrated significantly higher precision and recall to the baseline method of assigning genes to proximal peaks. EgrMYB1, EgrMYB2 and EgrMYB137 predicted targets showed clear enrichment for SCW-related biological processes. As validation, EgrMYB137 overexpression in transgenic Eucalyptus hairy roots increased xylem lignification, while its dominant repression in transgenic Arabidopsis and Populus reduced xylem lignification, stunted growth, and caused downregulation of SCW genes. EgrMYB137 targets overlapped significantly with those of EgrMYB2, suggesting partial functional redundancy. Our results show that DAP-seq-ML identified biologically relevant R2R3-MYB targets supported by the finding that EgrMYB137 promotes SCW lignification in planta.
Key message
We combined DAP-seq with machine learning to identify biologically relevant gene targets for five Eucalyptus R2R3-MYB transcription factors linked to wood formation, additionally demonstrating that EgrMYB137 promotes lignification in planta.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Sequencing data were registered at the NCBI SRA database (PRJNA899014 and PRJNA899708).
References
Ambawat S, Sharma P, Yadav NR, Yadav RC (2013) MYB transcription factor genes as regulators for plant responses: an overview. Physiol Mol Biol Plants 19:307–321. https://doi.org/10.1007/s12298-013-0179-1
Andrews S (2010) A quality control tool for high throughput sequence data. Available online at: https://www.bioinformatics.babraham.ac.uk/projects/fastqc/
Arabidopsis Interactome Mapping Consortium (2011) Evidence for network evolution in an Arabidopsis interactome map. Science 1979(333):601–607
Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2:28–36
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME suite: tools for motif discovery and searching. Nucleic Acids Res. https://doi.org/10.1093/nar/gkp335
Ballouz S, Verleyen W, Gillis J (2015) Guidance for RNA-seq co-expression network construction and analysis: safety in numbers. Bioinformatics 31:2123–2130. https://doi.org/10.1093/bioinformatics/btv118
Bargmann BOR, Marshall-Colon A, Efroni I, Ruffel S, Birnbaum KD, Coruzzi GM, Krouk G (2013) Target: a transient transformation system for genome-wide transcription factor target discovery. Mol Plant 6:978–980. https://doi.org/10.1093/mp/sst010
Bar-On YM, Phillips R, Milo R (2018) The biomass distribution on earth. Proc Natl Acad Sci 115:6506–6511. https://doi.org/10.1073/pnas.1711842115
Bartlett A, Huang SC, Galli M, Nery JR, Gallavotti A, Ecker JR (2017) Mapping genome-wide transcription factor binding sites using DAP-seq. Nat Protoc 12:1659–1672. https://doi.org/10.1038/nprot.2017.055
Brooks MD, Cirrone J, Pasquino AV, Alvarez JM, Swift J, Mittal S, Juang C-L, Varala K, Gutiérrez RA, Krouk G, Shasha D, Coruzzi GM (2019) Network walking charts transcriptional dynamics of nitrogen signaling by integrating validated and predicted genome-wide interactions. Nat Commun 10:1569. https://doi.org/10.1038/s41467-019-09522-1
Brown K, Takawira LT, O’Neill MM, Mizrachi E, Myburg AA, Hussey SG (2019) Identification and functional evaluation of accessible chromatin associated with wood formation in Eucalyptus grandis. New Phytol 223:1937–1951. https://doi.org/10.1111/nph.15897
Carocha V, Soler M, Hefer C, Cassan-Wang H, Fevereiro P, Myburg AA, Paiva JAP, Grima-Pettenati J (2015) Genome-wide analysis of the lignin toolbox of Eucalyptus grandis. New Phytol 206:1297–1313. https://doi.org/10.1111/nph.13313
Cassan-Wang H, Soler M, Yu H, Camargo ELO, Carocha V, Ladouce N, Savelli B, Paiva JAP, Leplé J-C, Grima-Pettenati J (2012) Reference genes for high-throughput quantitative reverse transcription–PCR analysis of gene expression in organs and tissues of eucalyptus grown in various environmental conditions. Plant Cell Physiol 53:2101–2116. https://doi.org/10.1093/pcp/pcs152
Cassan-Wang H, Goué 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. https://doi.org/10.3389/fpls.2013.00189
Chen H, Wang JP, Liu H, Li H, Lin Y-CJ, Shi R, Yang C, Gao J, Zhou C, Li Q, Sederoff RR, Li W, Chiang VL (2019) Hierarchical transcription factor and chromatin binding network for wood formation in Populus trichocarpa. Plant Cell 31:602–626. https://doi.org/10.1105/tpc.18.00620
Chun HJ, Baek D, Cho HM, Lee SH, Jin BJ, Yun D-J, Hong Y-S, Kim MC (2019) Lignin biosynthesis genes play critical roles in the adaptation of Arabidopsis plants to high-salt stress. Plant Signal Behav 14:1625697. https://doi.org/10.1080/15592324.2019.1625697
Cochrane FC, Davin LB, Lewis NG (2004) The Arabidopsis phenylalanine ammonia lyase gene family: kinetic characterization of the four PAL isoforms. Phytochemistry 65:1557–1564. https://doi.org/10.1016/j.phytochem.2004.05.006
da Silveira FV, Severing E, Lai X, Estevan J, Farrera I, Hugouvieux V, Revers LF, Zubieta C, Coupland G, Costes E, Andrés F (2021) Unraveling the role of MADS transcription factor complexes in apple tree dormancy. New Phytol 232:2071–2088. https://doi.org/10.1111/nph.17710
Ding A, Tang X, Yang D, Wang M, Ren A, Xu Z, Hu R, Zhou G, O’Neill M, Kong Y (2021) ERF4 and MYB52 transcription factors play antagonistic roles in regulating homogalacturonan de-methylesterification in Arabidopsis seed coat mucilage. Plant Cell 33:381–403. https://doi.org/10.1093/plcell/koaa031
Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581. https://doi.org/10.1016/j.tplants.2010.06.005
el Houari I, Boerjan W, Vanholme B (2021) Behind the scenes: the impact of bioactive phenylpropanoids on the growth phenotypes of Arabidopsis lignin mutants. Front Plant Sci. https://doi.org/10.3389/fpls.2021.734070
Farahani A, Voghoei S, Rasheed K, Arabnia HR (2020) A brief review of domain adaptation. Adv Data Sci Inf Eng 2020:877–894
Fornalé S, Shi X, Chai C, Encina A, Irar S, Capellades M, Fuguet E, Torres JL, Rovira P, Puigdomènech P, Rigau J, Grotewold E, Gray J, Caparrós-Ruiz D (2010) ZmMYB31 directly represses maize lignin genes and redirects the phenylpropanoid metabolic flux. Plant J 64:633–644. https://doi.org/10.1111/j.1365-313X.2010.04363.x
Galli M, Khakhar A, Lu Z, Chen Z, Sen S, Joshi T, Nemhauser JL, Schmitz RJ, Gallavotti A (2018) The DNA binding landscape of the maize auxin response factor family. Nat Commun. https://doi.org/10.1038/s41467-018-06977-6
Geng P, Zhang S, Liu J, Zhao C, Wu J, Cao Y, Fu C, Han X, He H, Zhao Q (2020) MYB20, MYB42, MYB43, and MYB85 regulate phenylalanine and lignin biosynthesis during secondary cell wall formation1[OPEN]. Plant Physiol 182:1272–1283. https://doi.org/10.1104/PP.19.01070
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 43:553–567. https://doi.org/10.1111/j.1365-313X.2005.02480.x
Gomez-Cano F, Chu Y, Cruz-Gomez M, Abdullah HM, Lee YS, Schnell DJ, Grotewold E (2022) Exploring Camelina sativa lipid metabolism regulation by combining gene co-expression and DNA affinity purification analyses. Plant J 110:589–606. https://doi.org/10.1111/tpj.15682
Guo Y, Mahony S, Gifford DK (2012) High resolution genome wide binding event finding and motif discovery reveals transcription factor spatial binding constraints. PLoS Comput Biol 8:e1002638. https://doi.org/10.1371/journal.pcbi.1002638
Hadj Bachir I, Ployet R, Teulières C, Cassan-Wang H, Mounet F, Grima-Pettenati J (2022) Regulation of secondary cell wall lignification by abiotic and biotic constraints. Elsevier
Han Z, Yang T, Guo Y, Cui WH, Yao LJ, Li G, Wu AM, Li JH, Liu LJ (2021) The transcription factor PagLBD3 contributes to the regulation of secondary growth in Populus. J Exp Bot 72:7092–7106. https://doi.org/10.1093/jxb/erab351
Hatton D, Sablowski R, Yung M-H, Smith C, Schuch W, Bevan M (1995) Two classes of cis sequences contribute to tissue-specific expression of a PAL2 promoter in transgenic tobacco. Plant J 7:859–876. https://doi.org/10.1046/j.1365-313X.1995.07060859.x
Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J 34:733–739. https://doi.org/10.1046/j.1365-313X.2003.01759.x
Houston K, Tucker MR, Chowdhury J, Shirley N, Little A (2016) The plant cell wall: a complex and dynamic structure as revealed by the responses of genes under stress conditions. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00984
Hussey SG (2022) Transcriptional regulation of secondary cell wall formation and lignification. In: Advances in botanical research. Academic Press, New York
Hussey SG, Saïdi MN, Hefer CA, Myburg AA, Grima-Pettenati J (2015) Structural, evolutionary and functional analysis of the NAC domain protein family in Eucalyptus. New Phytol 206:1337–1350. https://doi.org/10.1111/nph.13139
Jin H, Martin C (1999) Multifunctionality and diversity within the plant MYB-gene family. Plant Mol Biol 41:577–585. https://doi.org/10.1023/a:1006319732410
Jin H, Cominelli E, Bailey P, Parr A, Mehrtens F, Jones J, Tonelli C, Weisshaar B, Martin C (2000) Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. EMBO J 19:6150–6161. https://doi.org/10.1093/emboj/19.22.6150
Kaufmann K, Muiño JM, Jauregui R, Airoldi CA, Smaczniak C, Krajewski P, Angenent GC (2009) Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower. PLoS Biol 7:e1000090. https://doi.org/10.1371/journal.pbio.1000090
Ko J-H, Kim W-C, Han K-H (2009) Ectopic expression of MYB46 identifies transcriptional regulatory genes involved in secondary wall biosynthesis in Arabidopsis. Plant J 60:649–665. https://doi.org/10.1111/j.1365-313X.2009.03989.x
Ko JH, Jeon HW, Kim WC, Kim JY, Han KH (2014) The MYB46/MYB83-mediated transcriptional regulatory programme is a gatekeeper of secondary wall biosynthesis. Ann Bot 114:1099–1107
Koncz C, Schell J (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet 204:383–396. https://doi.org/10.1007/BF00331014
Kumar M, Campbell L, Turner S (2016) Secondary cell walls: biosynthesis and manipulation. J Exp Bot 67:515–531. https://doi.org/10.1093/jxb/erv533
Lai X, Stigliani A, Lucas J, Hugouvieux V, Parcy F, Zubieta C (2020) Genome-wide binding of SEPALLATA3 and AGAMOUS complexes determined by sequential DNA-affinity purification sequencing. Nucleic Acids Res 48:9637–9648. https://doi.org/10.1093/nar/gkaa729
Landt SG, Marinov GK, Kundaje A, Kheradpour P, Pauli F, Batzoglou S, Bernstein BE, Bickel P, Brown JB, Cayting P, Chen Y, DeSalvo G, Epstein C, Fisher-Aylor KI, Euskirchen G, Gerstein M, Gertz J, Hartemink AJ, Hoffman MM, Iyer VR, Jung YL, Karmakar S, Kellis M, Kharchenko PV, Li Q, Liu T, Liu XS, Ma L, Milosavljevic A, Myers RM, Park PJ, Pazin MJ, Perry MD, Raha D, Reddy TE, Rozowsky J, Shoresh N, Sidow A, Slattery M, Stamatoyannopoulos JA, Tolstorukov MY, White KP, Xi S, Farnham PJ, Lieb JD, Wold BJ, Snyder M (2012) ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res 22:1813–1831. https://doi.org/10.1101/gr.136184.111
Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. https://doi.org/10.1186/gb-2009-10-3-r25
Laubscher M, Brown K, Tonfack LB, Myburg AA, Mizrachi E, Hussey SG (2018) Temporal analysis of Arabidopsis genes activated by Eucalyptus grandis NAC transcription factors associated with xylem fibre and vessel development. Sci Rep 8:10983. https://doi.org/10.1038/s41598-018-29278-w
Legay S, Lacombe E, Goicoechea M, Brière C, Séguin A, Mackay J, Grima-Pettenati J (2007) Molecular characterization of EgMYB1, a putative transcriptional repressor of the lignin biosynthetic pathway. Plant Sci 173:542–549. https://doi.org/10.1016/j.plantsci.2007.08.007
Legay S, Sivadon P, Blervacq A, Pavy N, Baghdady A, Tremblay L, Levasseur C, Ladouce N, Lapierre C, Séguin A, Hawkins S, Mackay J, Grima-Pettenati J (2010) EgMYB1, an R2R3 MYB transcription factor from eucalyptus negatively regulates secondary cell wall formation in Arabidopsis and poplar. New Phytol 188:774–786. https://doi.org/10.1111/j.1469-8137.2010.03432.x
Li Q, Brown JB, Huang H, Bickel PJ (2011) Measuring reproducibility of high-throughput experiments. Ann Appl Stat. https://doi.org/10.1214/11-AOAS466
Li C, Ma X, Yu H, Fu Y, Luo K (2018) Ectopic expression of PtoMYB74 in poplar and arabidopsis promotes secondary cell wall formation. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01262
Lin Y-C, Li W, Sun Y-H, Kumari S, Wei H, Li Q, Tunlaya-Anukit S, Sederoff RR, Chiang VL (2013) SND1 transcription factor-directed quantitative functional hierarchical genetic regulatory network in wood formation in Populus trichocarpa. Plant Cell 25:4324–4341. https://doi.org/10.1105/tpc.113.117697
Liu B, Liu J, Yu J, Wang Z, Sun Y, Li S, Lin Y-CJ, Chiang VL, Li W, Wang JP (2021) Transcriptional reprogramming of xylem cell wall biosynthesis in tension wood. Plant Physiol 186:250–269. https://doi.org/10.1093/plphys/kiab038
Liu H, Gao J, Sun J, Li S, Zhang B, Wang Z, Zhou C, Sulis DB, Wang JP, Chiang VL, Li W (2022) Dimerization of PtrMYB074 and PtrWRKY19 mediates transcriptional activation of PtrbHLH186 for secondary xylem development in Populus trichocarpa. New Phytol 234:918–933. https://doi.org/10.1111/nph.18028
Luo L, Li L (2022) Molecular understanding of wood formation in trees. For Res 2:1–11
Maere S, Heymans K, Kuiper M (2005) BiNGO: a cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21:3448–3449. https://doi.org/10.1093/bioinformatics/bti551
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 50:1950–1964. https://doi.org/10.1093/pcp/pcp139
Myburg AA, Grattapaglia D, Tuskan GA, Hellsten U, Hayes RD, Grimwood J, Jenkins J, Lindquist E, Tice H, Bauer D, Goodstein DM, Dubchak I, Poliakov A, Mizrachi E, Kullan ARK, Hussey SG, Pinard D, Van Der Merwe K, Singh P, Van Jaarsveld I, Silva-Junior OB, Togawa RC, Pappas MR, Faria DA, Sansaloni CP, Petroli CD, Yang X, Ranjan P, Tschaplinski TJ, Ye CY, Li T, Sterck L, Vanneste K, Murat F, Soler M, Clemente HS, Saidi N, Cassan-Wang H, Dunand C, Hefer CA, Bornberg-Bauer E, Kersting AR, Vining K, Amarasinghe V, Ranik M, Naithani S, Elser J, Boyd AE, Liston A, Spatafora JW, Dharmwardhana P, Raja R, Sullivan C, Romanel E, Alves-Ferreira M, Külheim C, Foley W, Carocha V, Paiva J, Kudrna D, Brommonschenkel SH, Pasquali G, Byrne M, Rigault P, Tibbits J, Spokevicius A, Jones RC, Steane DA, Vaillancourt RE, Potts BM, Joubert F, Barry K, Pappas GJ, Strauss SH, Jaiswal P, Grima-Pettenati J, Salse J, Van De Peer Y, Rokhsar DS, Schmutz J (2014) The genome of Eucalyptus grandis. Nature 510:356–362. https://doi.org/10.1038/nature13308
Nakano Y, Yamaguchi M, Endo H, Rejab NA, Ohtani M (2015) NAC-MYB-based transcriptional regulation of secondary cell wall biosynthesis in land plants. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00288
O’Malley RC, Huang SSC, Song L, Lewsey MG, Bartlett A, Nery JR, Galli M, Gallavotti A, Ecker JR (2016) Cistrome and epicistrome features shape the regulatory DNA landscape. Cell 165:1280–1292. https://doi.org/10.1016/j.cell.2016.04.038
Park MY, Kang J, Kim SY (2011) Overexpression of AtMYB52 confers ABA hypersensitivity and drought tolerance. Mol Cells 31:447–454. https://doi.org/10.1007/s10059-011-0300-7
Patzlaff A, McInnis S, Courtenay A, Surman C, Newman LJ, Smith C, Bevan MW, Mansfield S, Whetten RW, Sederoff RR, Campbell MM (2003) Characterisation of a pine MYB that regulates lignification. Plant J 36:743–754. https://doi.org/10.1046/j.1365-313X.2003.01916.x
Pitre FE, Pollet B, Lafarguette F, Cooke JEK, MacKay JJ, Lapierre C (2007) Effects of increased nitrogen supply on the lignification of poplar wood. J Agric Food Chem 55:10306–10314. https://doi.org/10.1021/jf071611e
Plasencia A, Soler M, Dupas A, Ladouce N, Silva-Martins G, Martinez Y, Lapierre C, Franche C, Truchet I, Grima-Pettenati J (2016) Eucalyptus hairy roots, a fast, efficient and versatile tool to explore function and expression of genes involved in wood formation. Plant Biotechnol J 14:1381–1393. https://doi.org/10.1111/pbi.12502
Ployet R, Veneziano Labate MT, Regiani Cataldi T, Christina M, Morel M, San Clemente H, Denis M, Favreau B, Tomazello Filho M, Laclau J, Labate CA, Chaix G, Grima-Pettenati J, Mounet F (2019) A systems biology view of wood formation in Eucalyptus grandis trees submitted to different potassium and water regimes. New Phytol 223:766–782. https://doi.org/10.1111/nph.15802
Qu G, Peng D, Yu Z, Chen X, Cheng X, Yang Y, Ye T, Lv Q, Ji W, Deng X, Zhou B (2021) Advances in the role of auxin for transcriptional regulation of lignin biosynthesis. Funct Plant Biol 48:743. https://doi.org/10.1071/FP20381
Raes J, Rohde A, Christensen JH, van de Peer Y, Boerjan W (2003) Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiol 133:1051–1071. https://doi.org/10.1104/pp.103.026484
Rodriguez-Zaccaro FD, Groover A (2019) Wood and water: how trees modify wood development to cope with drought. Plants People Planet 1:346–355. https://doi.org/10.1002/ppp3.29
Rohde A, Morreel K, Ralph J, Goeminne G, Hostyn V, de Rycke R, Kushnir S, van Doorsselaere J, Joseleau J-P, Vuylsteke M, van Driessche G, van Beeumen J, Messens E, Boerjan W (2004) Molecular phenotyping of the pal1 and pal2 mutants of Arabidopsis thaliana reveals far-reaching consequences on phenylpropanoid, amino acid, and carbohydrate metabolism. Plant Cell 16:2749–2771. https://doi.org/10.1105/tpc.104.023705
Romano JM, Dubos C, Prouse MB, Wilkins O, Hong H, Poole M, Kang K, Li E, Douglas CJ, Western TL, Mansfield SD, Campbell MM (2012) AtMYB61, an R2R3-MYB transcription factor, functions as a pleiotropic regulator via a small gene network. New Phytol 195:774–786. https://doi.org/10.1111/j.1469-8137.2012.04201.x
Roy S (2016) Function of MYB domain transcription factors in abiotic stress and epigenetic control of stress response in plant genome. Plant Signal Behav 11:e1117723. https://doi.org/10.1080/15592324.2015.1117723
Shen H, He X, Poovaiah CR, Wuddineh WA, Ma J, Mann DGJ, Wang H, Jackson L, Tang Y, Neal Stewart J, Chen F, Dixon RA (2012) Functional characterization of the switchgrass (Panicum virgatum) R2R3-MYB transcription factor PvMYB4 for improvement of lignocellulosic feedstocks. New Phytol 193:121–136. https://doi.org/10.1111/j.1469-8137.2011.03922.x
Shi D, Ren A, Tang X, Qi G, Xu Z, Chai G, Hu R, Zhou G, Kong Y (2018) MYB52 negatively regulates pectin demethylesterification in seed coat mucilage. Plant Physiol 176:2737–2749. https://doi.org/10.1104/pp.17.01771
Shimada TL, Shimada T, Hara-Nishimura I (2010) A rapid and non-destructive screenable marker, FAST, for identifying transformed seeds of Arabidopsis thaliana. Plant J 61:519–528. https://doi.org/10.1111/j.1365-313X.2009.04060.x
Sixto H, González-González BD, Molina-Rueda JJ, Garrido-Aranda A, Sanchez MM, López G, Gallardo F, Cañellas I, Mounet F, Grima-Pettenati J, Cantón F (2016) Eucalyptus spp. and Populus spp. coping with salinity stress: an approach on growth, physiological and molecular features in the context of short rotation coppice (SRC). Trees 30:1873–1891. https://doi.org/10.1007/s00468-016-1420-7
Soler M, Camargo ELO, Carocha V, Cassan-Wang H, San Clemente H, Savelli B, Hefer CA, Paiva JAP, Myburg AA, Grima-Pettenati J (2015) The Eucalyptus grandis R2R3-MYB transcription factor family: evidence for woody growth-related evolution and function. New Phytol 206:1364–1377. https://doi.org/10.1111/nph.13039
Soler M, Plasencia A, Lepikson-Neto J, Camargo ELO, Dupas A, Ladouce N, Pesquet E, Mounet F, Larbat R, Grima-Pettenati J (2016) The woody-preferential gene EgMYB88 regulates the biosynthesis of phenylpropanoid-derived compounds in wood. Front Plant Sci. https://doi.org/10.3389/fpls.2016.01422
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 213:287–299. https://doi.org/10.1111/nph.14129
Song Q, Lee J, Akter S, Rogers M, Grene R, Li S (2020) Prediction of condition-specific regulatory genes using machine learning. Nucleic Acids Res 48:e62–e62. https://doi.org/10.1093/nar/gkaa264
Sullivan AM, Bubb KL, Sandstrom R, Stamatoyannopoulos JA, Queitsch C (2015) DNase I hypersensitivity mapping, genomic footprinting, and transcription factor networks in plants. Curr Plant Biol 3–4:40–47. https://doi.org/10.1016/j.cpb.2015.10.001
Sundell D, Street NR, Kumar M, Mellerowicz EJ, Kucukoglu M, Johnsson C, Kumar V, Mannapperuma C, Delhomme N, Nilsson O, Tuominen H, Pesquet E, Fischer U, Niittylä T, Sundberg B, Hvidsten TR (2017) AspWood: high-spatial-resolution transcriptome profiles reveal uncharacterized modularity of wood formation in Populus tremula. Plant Cell 29:1585–1604. https://doi.org/10.1105/tpc.17.00153
Taylor-Teeples M, Lin L, De Lucas M, Turco G, Toal TW, Gaudinier A, Young NF, Trabucco GM, Veling MT, Lamothe R, Handakumbura PP, Xiong G, Wang C, Corwin J, Tsoukalas A, Zhang L, Ware D, Pauly M, Kliebenstein DJ, Dehesh K, Tagkopoulos I, Breton G, Pruneda-Paz JL, Ahnert SE, Kay SA, Hazen SP, Brady SM (2015) An Arabidopsis gene regulatory network for secondary cell wall synthesis. Nature 517:571–575. https://doi.org/10.1038/nature14099
van de Velde J, van Bel M, Vaneechoutte D, Vandepoele K (2016) A collection of conserved noncoding sequences to study gene regulation in flowering plants. Plant Physiol 171:2586–2598. https://doi.org/10.1104/pp.16.00821
Vimolmangkang S, Han Y, Wei G, Korban SS (2013) An apple MYB transcription factor, MdMYB3, is involved in regulation of anthocyanin biosynthesis and flower development. BMC Plant Biol. https://doi.org/10.1186/1471-2229-13-176
Wang X, Niu Q-W, Teng C, Li C, Mu J, Chua N-H, Zuo J (2009) Overexpression of PGA37/MYB118 and MYB115 promotes vegetative-to-embryonic transition in Arabidopsis. Cell Res 19:224–235. https://doi.org/10.1038/cr.2008.276
Wang XC, Wu J, Guan ML, Zhao CH, Geng P, Zhao Q (2020a) Arabidopsis MYB4 plays dual roles in flavonoid biosynthesis. Plant J 101:637–652. https://doi.org/10.1111/tpj.14570
Wang Z, Mao Y, Guo Y, Gao J, Liu X, Li S, Lin Y-CJ, Chen H, Wang JP, Chiang VL, Li W (2020b) MYB transcription Factor161 mediates feedback regulation of secondary wall-associated NAC-Domain1 family genes for wood formation. Plant Physiol 184:1389–1406. https://doi.org/10.1104/pp.20.01033
Wong JH, Namasivayam P, Abdullah MP (2012) The PAL2 promoter activities in relation to structural development and adaptation in Arabidopsis thaliana. Planta 235:267–277. https://doi.org/10.1007/s00425-011-1506-9
Xiao R, Zhang C, Guo X, Li H, Lu H (2021) MYB transcription factors and its regulation in secondary cell wall formation and lignin biosynthesis during xylem development. Int J Mol Sci 22:3560. https://doi.org/10.3390/ijms22073560
Xu Y, Wang Y, Wang X, Pei S, Kong Y, Hu R, Zhou G (2020) Transcription factors BLH2 and BLH4 regulate demethylesterification of homogalacturonan in seed mucilage. Plant Physiol 183:96–111. https://doi.org/10.1104/pp.20.00011
Yoon J, Choi H, An G (2015) Roles of lignin biosynthesis and regulatory genes in plant development. J Integr Plant Biol 57:902–912. https://doi.org/10.1111/jipb.12422
Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol 9:R137. https://doi.org/10.1186/gb-2008-9-9-r137
Zhang J, Xie M, Tuskan GA, Muchero W, Chen JG (2018) Recent advances in the transcriptional regulation of secondary cell wall biosynthesis in the woody plants. Front Plant Sci 9:871
Zhong R, Ye Z-H (2007) Regulation of cell wall biosynthesis. Curr Opin Plant Biol 10:564–572. https://doi.org/10.1016/j.pbi.2007.09.001
Zhong R, Ye ZH (2012) MYB46 and MYB83 bind to the SMRE sites and directly activate a suite of transcription factors and secondary wall biosynthetic genes. Plant Cell Physiol 53:368–380. https://doi.org/10.1093/pcp/pcr185
Zhong R, Ye ZH (2015) Secondary cell walls: biosynthesis, patterned deposition and transcriptional regulation. Plant Cell Physiol 56:195–214
Zhong R, Lee C, Zhou J, McCarthy RL, Ye ZH (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20:2763–2782. https://doi.org/10.1105/tpc.108.061325
Zhong R, Lee C, Ye Z-H (2010) Evolutionary conservation of the transcriptional network regulating secondary cell wall biosynthesis. Trends Plant Sci 15:625–632. https://doi.org/10.1016/j.tplants.2010.08.007
Zhong R, McCarthy RL, Haghighat M, Ye ZH (2013) The poplar MYB master switches bind to the SMRE site and activate the secondary wall biosynthetic program during wood formation. PLoS ONE. https://doi.org/10.1371/journal.pone.0069219
Zhou J, Lee C, Zhong R, Ye ZH (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21:248–266. https://doi.org/10.1105/tpc.108.063321
Zhu LJ, Gazin C, Lawson ND, Pagès H, Lin SM, Lapointe DS, Green MR (2010) ChIPpeakAnno: a bioconductor package to annotate ChIP-seq and ChIP-chip data. BMC Bioinform 11:1–10
Zhu C-C, Wang C-X, Lu C-Y, Wang J-D, Zhou Y, Xiong M, Zhang C-Q, Liu Q-Q, Li Q-F, Wang C-Y, Zhou J-D, Xiong Y, Zhang M, Liu C-Q, Li Q-Q (2021) Genome-wide identification and expression analysis of OsbZIP09 target genes in rice reveal its mechanism of controlling seed germination. Int J Mol Sci. https://doi.org/10.3390/ijms
Acknowledgements
We thank Jonathan Featherston and Dirk Swanevelder from the Agricultural Research Council, Pretoria, and Dr Tuan Dong (University of Pretoria) for their assistance with Covaris sonication. The authors acknowledge the Genotoul GeT Platform for genomic analyses and the TRI-Genotoul platform for microscopic analyses. RP and IHB were supported by a PhD grant from the Ministère de l’Education Nationale, de l’Enseignement Supérieur et de la Recherche. The authors acknowledge Marcal Soler and Anna Plasencia Casadeval for their involvement in this work.
Funding
Funding was provided by the National Research Foundation (NRF) (UID 129155), the Department of Science and Innovation, Mondi Ltd and Sappi Ltd. The work conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported under Contract No. DE-AC02-05CH11231. This work was supported by the University of Toulouse, the Centre National pour la Recherche Scientifique (CNRS) and the French Laboratory of Excellence project ‘TULIP’ (ANR-10-LABX-41; ANR-11- IDEX-0002–02).
Author information
Authors and Affiliations
Contributions
LTT and IHB drafted the manuscript together with SGH and FM, who conceived of the study. LTT conducted DAP-seq experiments for Laboratory 1, while IHB and NL generated EgrMYB2 and EgrMYB137 DAP-seq data (Laboratory 2). LTT, IHB and HSC performed bioinformatic analytical pipelines. JT developed the machine learning algorithm under supervision of SH, NC and RP. IHB, AD, NL and RP conducted the reverse genetics work under the supervision of FM and JG-P. AR assessed the native transcriptional activation activity of EgrMYB137 in yeast under the supervision of SH and FM. EM, AAM and JG-P co-supervised the study.
Corresponding authors
Ethics declarations
Competing Interests
The authors have not disclosed any competing interests.
Ethical approval
Ethical approval for study was obtained at the University of Pretoria (protocol number NAS105/2021).
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Takawira, L.T., Hadj Bachir, I., Ployet, R. et al. Functional investigation of five R2R3-MYB transcription factors associated with wood development in Eucalyptus using DAP-seq-ML. Plant Mol Biol 113, 33–57 (2023). https://doi.org/10.1007/s11103-023-01376-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-023-01376-y