Abstract
Key message
A sugarcane MYB present in the culm induces suberin biosynthesis and is involved both with fatty acid and phenolics metabolism.
Abstract
Few transcription factors have been described as regulators of cell wall polymers deposition in C4 grasses. Particularly, regulation of suberin biosynthesis in this group of plants remains poorly understood. Here, we showed that the sugarcane MYB transcription factor ShMYB78 is an activator of suberin biosynthesis and deposition. ShMYB78 was identified upon screening genes whose expression was upregulated in sugarcane internodes undergoing suberization during culm development or triggered by wounding. Agrobacterium-mediated transient expression of ShMYB78 in Nicotiana benthamiana leaves induced the ectopic deposition of suberin and its aliphatic and aromatic monomers. Further, the expression of suberin-related genes was induced by ShMYB78 heterologous expression in Nicotiana benthamiana leaves. ShMYB78 was shown to be a nuclear protein based on its presence in sugarcane internode nuclear protein extracts, and protoplast transactivation assays demonstrated that ShMYB78 activates the promoters of the sugarcane suberin biosynthetic genes β-ketoacyl-CoA synthase (ShKCS20) and caffeic acid-O-methyltransferase (ShCOMT). Our results suggest that ShMYB78 may be involved in the transcriptional regulation of suberin deposition, from fatty acid metabolism to phenylpropanoid biosynthesis, in sugarcane internodes.
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All data generated or analyzed during this study are included in this published article [and its supplementary information files].
References
Abdelkareem A, Thagun C, Imanishi S, Hashimoto T, Shoji T (2019) Identification of genes regulated by a jasmonate- and salt-inducible transcription factor JRE3 in tomato. Plant Biotechnol 36:29–37
Alonso-Serra J, Safronov O, Lim K-J, Fraser-Miller SJ, Blokhina OB, Campilho A, Chong S-L, Fagerstedt K, Haavikko R, Helariutta Y, Immanen J, Kangasjärvi J, Kauppila TJ, Lehtonen M, Ragni L, Rajaraman S, Räsänen R-M, Safdari P, Tenkanen M, Yli-Kauhaluoma JT, Teeri TH, Strachan CJ, Nieminen K, Salojärvi J (2019) Tissue-specific study across the stem reveals the chemistry and transcriptome dynamics of birch bark. New Phytol 222:1816–1831. https://doi.org/10.1111/nph.15725
Asikin Y, Takahashi M, Hirose N, Hou D-X, Takara K, Wada K (2012) Wax, policosanol, and long-chain aldehydes of different sugarcane (Saccharum officinarum L.) cultivars. Eur J Lipid Sci Technol 114:583–591. https://doi.org/10.1002/ejlt.201100300
Barros J, Serrani-Yarce JC, Chen F, Baxter D, Venables BJ, Dixon RA (2016) Role of bifunctional ammonia-lyase in grass cell wall biosynthesis. Nat Plants 2:16050. https://doi.org/10.1038/nplants.2016.50
Batoko H, Zheng H-Q, Hawes C, Moore I (2000) A Rab1 GTPase is required for transport between the endoplasmic reticulum and golgi apparatus and for normal golgi movement in plants. Plant Cell 12:2201–2217. https://doi.org/10.1105/tpc.12.11.2201
Bihmidine S, Hunter C, Johns C, Koch K, Braun D (2013) Regulation of assimilate import into sink organs: update on molecular drivers of sink strength. Front Plant Sci 4:177. https://doi.org/10.3389/fpls.2013.00177
Boher P, Serra O, Soler M, Molinas M, Figueras M (2013) The potato suberin feruloyl transferase FHT which accumulates in the phellogen is induced by wounding and regulated by abscisic and salicylic acids. J Exp Bot 64:3225–3236. https://doi.org/10.1093/jxb/ert163
Bottcher A, Cesarino I, Brombini dos Santos A, Vicentini R, Mayer JLS, Vanholme R, Morreel K, Goeminne G, Moura JCMS, Nobile PM, Carmello-Guerreiro SM, Antonio dos Anjos I, Creste S, Boerjan W, de Landell MG (2013) Lignification in sugarcane: biochemical characterization, gene discovery, and expression analysis in two genotypes contrasting for lignin content. Plant Physiol 163:1539–1557. https://doi.org/10.1104/pp.113.225250
Bowman JL, Kohchi T, Yamato KT, Jenkins J, Shu S, Ishizaki K, Yamaoka S, Nishihama R, Nakamura Y, Berger F, Adam C, Aki SS, Althoff F, Araki T, Arteaga-Vazquez MA, Balasubrmanian S, Barry K, Bauer D, Boehm CR, Briginshaw L, Caballero-Perez J, Catarino B, Chen F, Chiyoda S, Chovatia M, Davies KM, Delmans M, Demura T, Dierschke T, Dolan L, Dorantes-Acosta AE, Eklund DM, Florent SN, Flores-Sandoval E, Fujiyama A, Fukuzawa H, Galik B, Grimanelli D, Grimwood J, Grossniklaus U, Hamada T, Haseloff J, Hetherington AJ, Higo A, Hirakawa Y, Hundley HN, Ikeda Y, Inoue K, Inoue S, Ishida S, Jia Q, Kakita M, Kanazawa T, Kawai Y, Kawashima T, Kennedy M, Kinose K, Kinoshita T, Kohara Y, Koide E, Komatsu K, Kopischke S, Kubo M, Kyozuka J, Lagercrantz U, Lin S-S, Lindquist E, Lipzen AM, Lu C-W, De LE, Martienssen RA, Minamino N, Mizutani M, Mizutani M, Mochizuki N, Monte I, Mosher R, Nagasaki H, Nakagami H, Naramoto S, Nishitani K, Ohtani M, Okamoto T, Okumura M, Phillips J, Pollak B, Reinders A, Rövekamp M, Sano R, Sawa S, Schmid MW, Shirakawa M, Solano R, Spunde A, Suetsugu N, Sugano S, Sugiyama A, Sun R, Suzuki Y, Takenaka M, Takezawa D, Tomogane H, Tsuzuki M, Ueda T, Umeda M, Ward JM, Watanabe Y, Yazaki K, Yokoyama R, Yoshitake Y, Yotsui I, Zachgo S, Schmutz J (2017) Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171:287–304. https://doi.org/10.1016/j.cell.2017.09.030
Capote T, Barbosa P, Usié A, Ramos AM, Inácio V, Ordás R, Gonçalves S, Morais-Cecílio L (2018) ChIP-Seq reveals that QsMYB1 directly targets genes involved in lignin and suberin biosynthesis pathways in cork oak (Quercus suber). BMC Plant Biol 18:198. https://doi.org/10.1186/s12870-018-1403-5
Carvalho-Netto OV, Bressiani JA, Soriano HL, Fiori CS, Santos JM, Barbosa GVS, Xavier MA, Landell MGA, Pereira GAG (2014) The potential of the energy cane as the main biomass crop for the cellulosic industry. Chem Biol Technol Agric 1:20. https://doi.org/10.1186/s40538-014-0020-2
Casu RE, Grof CPL, Rae AL, McIntyre CL, Dimmock CM, Manners JM (2003) Identification of a novel sugar transporter homologue strongly expressed in maturing stem vascular tissues of sugarcane by expressed sequence tag and microarray analysis. Plant Mol Biol 52:371–386. https://doi.org/10.1023/A:1023957214644
Dantas GA, Legey LFL, Mazzone A (2013) Energy from sugarcane bagasse in Brazil: an assessment of the productivity and cost of different technological routes. Renew Sustain Energy Rev 21:356–364. https://doi.org/10.1016/j.rser.2012.11.080
Davin LB, Wang H-B, Crowell AL, Bedgar DL, Martin DM, Sarkanen S, Lewis NG (1997) Stereoselective bimolecular phenoxy radical coupling by an auxiliary (Dirigent) protein without an active center. Science 80(275):362–367. https://doi.org/10.1126/science.275.5298.362
de Setta N, Monteiro-Vitorello CB, Metcalfe CJ, Cruz GMQ, Del Bem LE, Vicentini R, Nogueira FTS, Campos RA, Nunes SL, Turrini PCG, Vieira AP, Ochoa Cruz EA, Corrêa TCS, Hotta CT, de Mello VA, Vautrin S, da Trindade AS, de Mendonça VM, Lembke CG, Sato PM, de Andrade RF, Nishiyama MY, Cardoso-Silva CB, Scortecci KC, Garcia AAF, Carneiro MS, Kim C, Paterson AH, Bergès H, D’Hont A, de Souza AP, Souza GM, Vincentz M, Kitajima JP, Van Sluys M-A (2014) Building the sugarcane genome for biotechnology and identifying evolutionary trends. BMC Genom 15:540. https://doi.org/10.1186/1471-2164-15-540
Du H, Yang S-S, Liang Z, Feng B-R, Liu L, Huang Y-B, Tang Y-X (2012) Genome-wide analysis of the MYB transcription factor superfamily in soybean. BMC Plant Biol 12:106. https://doi.org/10.1186/1471-2229-12-106
Espelie KE, Sadek NZ, Kolattukudy PE (1980) Composition of suberin-associated waxes from the subterranean storage organs of seven plants. Planta 148:468–476. https://doi.org/10.1007/BF02395317
Ferreira SS, Hotta CT, de Poelking VG et al (2016) Co-expression network analysis reveals transcription factors associated to cell wall biosynthesis in sugarcane. Plant Mol Biol 91:15–35. https://doi.org/10.1007/s11103-016-0434-2
Figueiredo R, Araújo P, Llerena JPP, Mazzafera P (2019) Suberin and hemicellulose in sugarcane cell wall architecture and crop digestibility: a biotechnological perspective. Food Energy Secur. https://doi.org/10.1002/fes3.163
Figueiredo R, Cesarino I, Mazzafera P (2016) Suberin as an extra barrier to grass digestibility: a closer look to sugarcane forage. Trop Plant Biol 9:96–108. https://doi.org/10.1007/s12042-016-9166-3
Gou M, Hou G, Yang H, Zhang X, Cai Y, Kai G, Liu C-J (2017) The MYB107 transcription factor positively regulates suberin biosynthesis. Plant Physiol 173:1045–1058. https://doi.org/10.1104/pp.16.01614
Graça J, Cabral V, Santos S, Lamosa P, Serra O, Molinas M, Schreiber L, Kauder F, Franke R (2015) Partial depolymerization of genetically modified potato tuber periderm reveals intermolecular linkages in suberin polyester. Phytochemistry 117:209–219. https://doi.org/10.1016/j.phytochem.2015.06.010
Graça J, Santos S (2006a) Glycerol-derived ester oligomers from cork suberin. Chem Phys Lipids 144:96–107. https://doi.org/10.1016/j.chemphyslip.2006.08.001
Graça J, Santos S (2006b) Linear aliphatic dimeric esters from cork suberin. Biomacromol 7:2003–2010. https://doi.org/10.1021/bm060174u
Grivet L, Glaszmann J-C, D’Hont A (2006) Molecular evidence of sugarcane evolution and domestication. In: Motley TJ, Zerega N, Cross H (eds) Darwin’s harvest. Columbia University Press, New York, pp 49–66
Hosmani PS, Kamiya T, Danku J, Naseer S, Geldner N, Lou GM, Salt DE (2013) Dirigent domain-containing protein is part of the machinery required for formation of the lignin-based Casparian strip in the root. Proc Natl Acad Sci USA 110:14498–14503. https://doi.org/10.1073/pnas.1308412110
Huis R, Morreel K, Fliniaux O, Lucau-Danila A, Fénart S, Grec S, Neutelings G, Chabbert B, Mesnard F, Boerjan W, Hawkins S (2012) Natural hypolignification is associated with extensive oligolignol accumulation in flax stems. Plant Physiol 158:1893–1915. https://doi.org/10.1104/pp.111.192328
Jenkin S, Molina I (2015) Isolation and compositional analysis of plant cuticle lipid polyester monomers. JoVE. https://doi.org/10.3791/53386
Jin J, Tian F, Yang D-C, Meng Y-Q, Kong L, Luo J, Gao G (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res 45:D1040–D1045. https://doi.org/10.1093/nar/gkw982
Karimi M, Inzé D, Depicker A (2002) GATEWAYTM vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193–195. https://doi.org/10.1016/S1360-1385(02)02251-3
Kiyota E, Mazzafera P, Sawaya ACHF (2012) Analysis of soluble lignin in sugarcane by ultrahigh performance liquid chromatography-tandem mass spectrometry with a do-it-yourself oligomer database. Anal Chem 84:7015–7020. https://doi.org/10.1021/ac301112y
Kosma DK, Murmu J, Razeq FM, Santos P, Bourgault R, Molina I, Rowland O (2014) AtMYB41 activates ectopic suberin synthesis and assembly in multiple plant species and cell types. Plant J 80:216–229. https://doi.org/10.1111/tpj.12624
Le Roy J, Huss B, Creach A, Hawkins S, Neutelings G (2016) Glycosylation is a major regulator of phenylpropanoid availability and biological activity in plants. Front Plant Sci 7:735. https://doi.org/10.3389/fpls.2016.00735
Lee SB, Kim HU, Suh MC (2016) MYB94 and MYB96 additively activate cuticular wax biosynthesis in Arabidopsis. Plant Cell Physiol 57:2300–2311. https://doi.org/10.1093/pcp/pcw147
Legay S, Cocco E, André CM, Guignard C, Hausman J-F, Guerriero G (2017) Differential lipid composition and gene expression in the semi-russeted “Cox Orange Pippin” apple variety. Front Plant Sci 8:1656. https://doi.org/10.3389/fpls.2017.01656
Legay S, Guerriero G, André C, Guignard C, Cocco E, Charton S, Boutry M, Rowland O, Hausman J-F (2016) MdMyb93 is a regulator of suberin deposition in russeted apple fruit skins. New Phytol 212:977–991. https://doi.org/10.1111/nph.14170
Legay S, Guerriero G, Deleruelle A, Lateur M, Evers D, André CM, Hausman J-F (2015) Apple russeting as seen through the RNA-seq lens: strong alterations in the exocarp cell wall. Plant Mol Biol 88:21–40. https://doi.org/10.1007/s11103-015-0303-4
Li-Beisson Y, Nakamura Y, Harwood J (2016) Lipids: From chemical structures, biosynthesis, and analyses to industrial applications. In: Nakamura Y, Li-Beisson Y (eds) Lipids in plant and algae development. Springer, Cham, pp 1–18
Lin C-S, Hsu C-T, Yang L-H, Lee L-Y, Fu J-Y, Cheng Q-W, Wu F-H, Hsiao HC-W, Zhang Y, Zhang R, Chang W-J, Yu C-T, Wang W, Liao L-J, Gelvin SB, Shih M-C (2018) Application of protoplast technology to CRISPR/Cas9 mutagenesis: from single-cell mutation detection to mutant plant regeneration. Plant Biotechnol J 16:1295–1310. https://doi.org/10.1111/pbi.12870
Liu D, Shi L, Han C, Yu J, Li D, Zhang Y (2012) Validation of reference genes for gene expression studies in virus-infected Nicotiana benthamiana using quantitative real-time PCR. PLoS ONE 7:1–14. https://doi.org/10.1371/journal.pone.0046451
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Llerena JPP, Figueiredo R, dos Brito M et al (2019) Deposition of lignin in four species of Saccharum. Sci Rep 9:5877. https://doi.org/10.1038/s41598-019-42350-3
Martins I, Hartmann DO, Alves PC, Martins C, Garcia H, Leclercq CC, Ferreira R, He J, Renaut J, Becker JD, Silva Pereira C (2014) Elucidating how the saprophytic fungus Aspergillus nidulans uses the plant polyester suberin as carbon source. BMC Genom 15:613. https://doi.org/10.1186/1471-2164-15-613
Mattiello L, Riaño-Pachón DM, Martins MCM, da Cruz LP, Bassi D, Marchiori PER, Ribeiro RV, Labate MTV, Labate CA, Menossi M (2015) Physiological and transcriptional analyses of developmental stages along sugarcane leaf. BMC Plant Biol 15:300. https://doi.org/10.1186/s12870-015-0694-z
Mertz RA, Brutnell TP (2014) Bundle sheath suberization in grass leaves: multiple barriers to characterization. J Exp Bot 65:3371–3380. https://doi.org/10.1093/jxb/eru108
Ming R, Moore PH, Wu K-K, D’hont A, Glaszmann JC, Tew TL, Mirkov TE, da Silva J, Jifon J, Rai M, Schnell RJ, Brumbley SM, Lakshmanan P, Comstock JC, Paterson AH (2010) Sugarcane improvement through breeding and biotechnology. Plant breeding reviews. Wiley, New York, pp 15–118
Moore P (1995) Temporal and spatial regulation of sucrose accumulation in the sugarcane stem. Aust J Plant Physiol 22:661–680. https://doi.org/10.1071/PP9950661
Moreira A, Nunes FM, Simões C, Maciel E, Domingues P, Domingues MR, Coimbra M (2017) Data on coffee composition and mass spectrometry analysis of mixtures of coffee related carbohydrates, phenolic compounds and peptides. Data Br. https://doi.org/10.1016/j.dib.2017.05.027
Nobile PM, Bottcher A, Mayer JLS, Brito MS, dos Anjos IA, de Landell MG et al (2017) Identification, classification and transcriptional profiles of dirigent domain-containing proteins in sugarcane. Mol Genet Genomics 292:1323–1340. https://doi.org/10.1007/s00438-017-1349-6
Pollard M, Beisson F, Li Y, Ohlrogge JB (2008) Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci 13:236–246. https://doi.org/10.1016/j.tplants.2008.03.003
Rains MK, de Silva ND, Molina I (2018) Reconstructing the suberin pathway in poplar by chemical and transcriptomic analysis of bark tissues. Tree Physiol 38:340–361. https://doi.org/10.1093/treephys/tpx060
Riaño-Pachón DM, Mattiello L (2017) Draft genome sequencing of the sugarcane hybrid SP80-3280. F1000Research 6:861. https://doi.org/10.12688/f1000research.11859.2
Salvato F, Loziuk P, Kiyota E, Daneluzzi GS, Araújo P, Muddiman DC, Mazzafera P (2019) Label-free quantitative proteomics of enriched nuclei from sugarcane (Saccharum ssp) stems in response to drought stress. Proteomics. https://doi.org/10.1002/pmic.201900004
Scalabrin E, Radaelli M, Rizzato G, Bogani P, Buiatti M, Gambaro A, Capodaglio G (2015) Metabolomic analysis of wild and transgenic Nicotiana langsdorffii plants exposed to abiotic stresses: unraveling metabolic responses. Anal Bioanal Chem 407:6357–6368. https://doi.org/10.1007/s00216-015-8770-7
Scully ED, Gries T, Palmer NA, Sarath G, Funnell-Harris DL, Baird L, Twigg P, Seravalli J, Clemente TE, Sattler SE (2018) Overexpression of SbMyb60 in Sorghum bicolor impacts both primary and secondary metabolism. New Phytol 217:82–104. https://doi.org/10.1111/nph.14815
Sidibé A, Simao-Beaunoir A-M, Lerat S, Giroux L, Toussaint V, Beaulieu C (2016) Proteome analyses of soil bacteria grown in the presence of potato suberin, a recalcitrant biopolymer. Microbes Environ 31:418–426. https://doi.org/10.1264/jsme2.ME15195
Silva NV, Mazzafera P, Cesarino I (2019) Should I stay or should I go: are chlorogenic acids mobilized towards lignin biosynthesis? Phytochemistry 166:112063. https://doi.org/10.1016/j.phytochem.2019.112063
Siqueira G, Arantes V, Saddler JN, Ferraz A, Milagres AMF (2017) Limitation of cellulose accessibility and unproductive binding of cellulases by pretreated sugarcane bagasse lignin. Biotechnol Biofuels 10:176. https://doi.org/10.1186/s13068-017-0860-7
Soler M, Serra O, Molinas M, Huguet G, Fluch S, Figueras M (2007) A genomic approach to suberin biosynthesis and cork differentiation. Plant Physiol 144:419–431. https://doi.org/10.1104/pp.106.094227
Sullivan ML (2017) Identification of bean hydroxycinnamoyl-CoA:tetrahydroxyhexanedioate hydroxycinnamoyl transferase (HHHT): use of transgenic alfalfa to determine acceptor substrate specificity. Planta 245:397–408. https://doi.org/10.1007/s00425-016-2613-4
Teixeira RT, Fortes AM, Bai H, Pinheiro C, Pereira H (2018) Transcriptional profiling of cork oak phellogenic cells isolated by laser microdissection. Planta 247:317–338. https://doi.org/10.1007/s00425-017-2786-5
To A, Joubès J, Thueux J, Kazaz S, Lepiniec L, Baud S (2020) AtMYB92 enhances fatty acid synthesis and suberin deposition in leaves of Nicotiana benthamiana. Plant J. https://doi.org/10.1111/tpj.14759
Torras-Claveria L, Jáuregui O, Codina C, Tiburcio AF, Bastida J, Viladomat F (2012) Analysis of phenolic compounds by high-performance liquid chromatography coupled to electrospray ionization tandem mass spectrometry in senescent and water-stressed tobacco. Plant Sci 182:71–78. https://doi.org/10.1016/j.plantsci.2011.02.009
Valiñas MA, Lanteri MA, Have A, Andreu AB (2015) Chlorogenic acid biosynthesis appears linked with suberin production in potato tuber (Solanum tuberosum). J Agric Food Chem 63(19):4902–4913. https://doi.org/10.1021/jf505777p
Vanhercke T, Divi UK, El TA, Liu Q, Mitchell M, Taylor MC, Eastmond PJ, Bryant F, Mechanicos A, Blundell C, Zhi Y, Belide S, Shrestha P, Zhou X-R, Ral J-P, White RG, Green A, Singh SP, Petrie JR (2017) Step changes in leaf oil accumulation via iterative metabolic engineering. Metab Eng 39:237–246. https://doi.org/10.1016/j.ymben.2016.12.007
Vicentini R, Bottcher A, dos Brito M et al (2015) Large-scale transcriptome analysis of two sugarcane genotypes contrasting for lignin content. PLoS ONE 10:1–19. https://doi.org/10.1371/journal.pone.0134909
Vishwanath SJ, Delude C, Domergue F, Rowland O (2015) Suberin: biosynthesis, regulation, and polymer assembly of a protective extracellular barrier. Plant Cell Rep 34:573–586. https://doi.org/10.1007/s00299-014-1727-z
Zale J, Jung JH, Kim JY, Pathak B, Karan R, Liu H, Chen X, Wu H, Candreva J, Zhai Z, Shanklin J, Altpeter F (2016) Metabolic engineering of sugarcane to accumulate energy-dense triacylglycerols in vegetative biomass. Plant Biotechnol J 14:661–669. https://doi.org/10.1111/pbi.12411
Zhao Q, Wang H, Yin Y, Xu Y, Chen F, Dixon RA (2010) Syringyl lignin biosynthesis is directly regulated by a secondary cell wall master switch. Proc Natl Acad Sci USA 107(32):14496–14501. https://doi.org/10.1073/pnas.1009170107
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(1):248–266. https://doi.org/10.1105/tpc.108.063321
Zhu YJ, Albert HH, Moore PH (2000) Differential expression of soluble acid invertase genes in the shoots of high-sucrose and low-sucrose species of Saccharum and their hybrids. Funct Plant Biol 27:193–199
Acknowledgements
We thank Dr Marie-Anne van Sluys, coordinator of the GaTElab at the Institute of Biosciences, University of São Paulo, Brazil, for the access to R570 BAC library, and specially to Tatiana Silveira Corrêa and Geovani Ragagnin for support in the library screening. We thank the access to Confocal Zeiss LSM780-NLO and assistance provided by the National Institute of Science and Technology on Photonics Applied to Cell Biology (INFABIC) at the State University of Campinas, Brazil; INFABIC is co-funded by São Paulo Research Foundation (FAPESP_08/57906-3) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq_573913/2008-0). We thank the access to microscope Olympus BX51 to Dr Juliana Meyer at the State University of Campinas, Brazil. RF thanks FAPESP and CNPq for postdoctoral fellowships (FAPESP Grant 2015/05437-3; CNPq grant 104051/2018-3) and PM thanks CNPq for a research fellowship. IC thanks FAPESP for the BIOEN Young Investigators Awards research grant (Processo FAPESP n° 2015/02527-1) and CNPq for the research fellowship 302927/2018-2.
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RF was granted FAPESP and CNPq postdoctoral fellowships (FAPESP Grant 2015/05437-3; CNPq Grant 104051/2018-3) and PM received a CNPq research fellowship. IC thanks FAPESP for the BIOEN Young Investigators Awards research Grant (Processo FAPESP n° 2015/02527-1) and CNPq for the research fellowship 302927/2018-2.
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RF and PM designed the research; RF, JPL, SSF and BC performed the research; EK, SS, MSB and LS provided technical support; RF, EK, SSF, IC and PM analyzed and interpreted the data; RF, SSF, IC and PM wrote the manuscript.
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Figueiredo, R., Portilla Llerena, J.P., Kiyota, E. et al. The sugarcane ShMYB78 transcription factor activates suberin biosynthesis in Nicotiana benthamiana. Plant Mol Biol 104, 411–427 (2020). https://doi.org/10.1007/s11103-020-01048-1
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DOI: https://doi.org/10.1007/s11103-020-01048-1