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The expression of a rice secondary wall-specific cellulose synthase gene, OsCesA7, is directly regulated by a rice transcription factor, OsMYB58/63

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Abstract

Main conclusion

A rice MYB transcription factor, OsMYB58/63, was found to directly upregulate the expression of a rice secondary wall-specific cellulose synthase gene, cellulose synthase A7 ( OsCesA7 ); in contrast, the Arabidopsis putative orthologs AtMYB58 and AtMYB63 have been shown to specifically activate lignin biosynthesis.

Although indirect evidence has shown that grass plants are similar to but partially different from dicotyledonous ones in transcriptional regulation of lignocellulose biosynthesis, little is known about the differences. This study showed that a rice MYB transcription factor, OsMYB58/63, directly upregulated the expression of a rice secondary wall-specific cellulose synthase gene, cellulose synthase A7 (OsCesA7). Gene co-expression analysis showed that, in rice, OsMYB58/63 and several rice MYB genes were co-expressed with genes encoding lignocellulose biosynthetic enzymes. The expression levels of OsMYB55/61, OsMYB55/61-L, OsMYB58/63, and OsMYB42/85 were commonly found to be high in culm internodes and nodes. All four MYB transcription factors functioned as transcriptional activators in yeast cells. OsMYB58/63 most strongly transactivated the expression of OsCesA7 in rice protoplasts. Moreover, recombinant OsMYB58/63 protein was bound to two distinct cis-regulatory elements, AC-II and SMRE3, in the OsCesA7 promoter. This is in sharp contrast to the role of Arabidopsis orthologs, AtMYB58 and AtMYB63, which had been reported to specifically activate lignin biosynthesis. The promoter analysis revealed that AC elements, which are the binding sites for MYB58 and MYB63, were lacking in cellulose and xylan biosynthetic genes in Arabidopsis, but present in cellulose, xylan, and lignin biosynthetic genes in rice, implying that the difference of transcriptional regulation between rice and Arabidopsis is due to the distinct composition of promoters. Our results provide a new insight into transcriptional regulation in grass lignocellulose biosynthesis.

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Abbreviations

COR:

Correlation coefficient

EMSA:

Electrophoretic mobility shift assay

GAL4BD:

GAL4 DNA-binding domain

OsCesA7:

Oryza sativa cellulose synthase A7

OsCAldOMT1:

Oryza sativa 5-hydroxyconiferaldehyde O-methyltransferase 1

OsGT43A:

Oryza sativa glycosyltransferase family 43A

SCW:

Secondary cell wall

TF:

Transcription factor

References

  • Aohara T, Kotake T, Kaneko Y, Takatsuji H, Tsumuraya Y, Kawasaki S (2009) Rice BRITTLE CULM 5 (BRITTLE NODE) is involved in secondary cell wall formation in the sclerenchyma tissue of nodes. Plant Cell Physiol 50:1886–1897

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Baba A, Hasezawa S, Syono K (1986) Cultivation of rice protoplasts and their transformation mediated by Agrobacterium spheroplasts. Plant Cell Physiol 27:463–471

    CAS  Google Scholar 

  • Bromley JR, Busse-Wicher M, Tryfona T, Mortimer JC, Zhang Z, Brown DM, Dupree P (2013) GUX1 and GUX2 glucuronyltransferases decorate distinct domains of glucuronoxylan with different substitution patterns. Plant J 74:423–434

    Article  CAS  PubMed  Google Scholar 

  • Cao P, Jung KH, Choi D, Hwang D, Zhu J, Ronald PC (2012) The Rice Oligonucleotide Array Database: an atlas of rice gene expression. Rice 5:17

    Article  PubMed  Google Scholar 

  • Chiniquy D, Sharma V, Schultink A, Baidoo EE, Rautengarten C, Cheng K, Carroll A, Ulvskov P, Harholt J, Keasling JD, Pauly M, Scheller HV, Ronald PC (2012) XAX1 from glycosyltransferase family 61 mediates xylosyltransfer to rice xylan. Proc Natl Acad Sci USA 109:17117–17122

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Demura T, Ye ZH (2010) Regulation of plant biomass production. Curr Opin Plant Biol 13:299–304

    Article  PubMed  Google Scholar 

  • 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: ZmMYB31 controls phenylpropanoids. Plant J 64:633–644

    Article  PubMed  Google Scholar 

  • Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12:393–404

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Graham RL, Nelson R, Sheehan J, Perlack RD, Wright LL (2007) Current and potential U.S. corn stover supplies. Agron J 99:1–11

    Article  Google Scholar 

  • Gui J, Shen J, Li L (2011) Functional characterization of evolutionarily divergent 4-coumarate:coenzyme A ligases in rice. Plant Physiol 157:574–586

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Handakumbura PP, Hazen SP (2012) Transcriptional regulation of grass secondary cell wall biosynthesis: playing catch-up with Arabidopsis thaliana. Front Plant Sci 3:74

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hatton D, Sablowski R, Yung MH, 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

    Article  CAS  PubMed  Google Scholar 

  • Hirano K, Aya K, Morinaka Y, Nagamatsu S, Sato Y, Antonio BA, Kamiki N, Nagamura Y, Matsuoka M (2013a) Survey of genes involved in rice secondary cell wall formation through a co-expression network. Plant Cell Physiol 54:1803–1821

    Article  CAS  PubMed  Google Scholar 

  • Hirano K, Kondo M, Aya K, Miyao A, Sato Y, Antonio BA, Kamiki N, Nagamura Y, Matsuoka M (2013b) Identification of transcription factors involved in rice secondary cell wall formation. Plant Cell Physiol 54:1791–1802

    Article  CAS  PubMed  Google Scholar 

  • Hiratsu K, Ohta M, Matsui K, Ohme-Takagi M (2002) The SUPERMAN protein is an active repressor whose carboxy-terminal repression domain is required for the development of normal flowers. FEBS Lett 514:351–354

    Article  CAS  PubMed  Google Scholar 

  • Hussey SG, Mizrachi E, Creux NM, Myburg AA (2013) Navigating the transcriptional roadmap regulating plant secondary cell wall deposition. Front Plant Sci 4:325

    Article  PubMed Central  PubMed  Google Scholar 

  • Kim WC, Ko JH, Han KH (2012) Identification of a cis-acting regulatory motif recognized by MYB46, a master transcriptional regulator of secondary wall biosynthesis. Plant Mol Biol 78:489–501

    Article  CAS  PubMed  Google Scholar 

  • Ko JH, Kim WC, Han KH (2009) Ectopic expression of MYB46 identifies transcriptional regulatory genes involved in secondary wall biosynthesis in Arabidopsis. Plant J 60:649–665

    Article  CAS  PubMed  Google Scholar 

  • Ko JH, Kim WC, Kim JY, Ahn SJ, Han KH (2012) MYB46-mediated transcriptional regulation of secondary wall biosynthesis. Mol Plant 5:961–963

    Article  CAS  PubMed  Google Scholar 

  • Koshiba T, Hirose N, Mukai M, Yamamura M, Hattori T, Suzuki S, Sakamoto M, Umezawa T (2013a) Characterization of 5-hydroxyconiferaldehyde O-methyltransferase in Oryza sativa. Plant Biotechnol 30:157–167

    Article  CAS  Google Scholar 

  • Koshiba T, Murakami S, Hattori T, Mukai M, Takahashi A, Miyao A, Hirochika H, Suzuki S, Sakamoto M, Umezawa T (2013b) CAD2 deficiency causes both brown midrib and gold hull and internode phenotypes in Oryza sativa L. cv. Nipponbare. Plant Biotechnol 30:365–373

    Article  CAS  Google Scholar 

  • Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19:1855–1860

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Lee C, Teng Q, Zhong R, Yuan Y, Ye ZH (2014) Functional roles of rice glycosyltransferase family GT43 in xylan biosynthesis. Plant Signal Behav 9:e27809

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Lemmon ZH, Bukowski R, Sun Q, Doebley JF (2014) The role of cis regulatory evolution in maize domestication. PLOS Genet 10:e100474

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Mitsuda N, Iwase A, Yamamoto H, Yoshida M, Seki M, Shinozaki K, Ohme-Takagi M (2007) NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in wood tissues of Arabidopsis. Plant Cell 19:270–280

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Noda S, Takahashi Y, Tsurumaki Y, Yamamura M, Nishikubo N, Yamaguchi M, Sakurai N, Hattori T, Suzuki H, Demura T, Shibata D, Suzuki S, Umezawa T (2013a) ATL54, a RING-H2 domain protein selected by a gene co-expression network analysis, is associated with secondary cell wall formation in Arabidopsis. Plant Biotechnol 30:169–177

    Article  CAS  Google Scholar 

  • Noda S, Yamaguchi M, Tsurumaki Y, Takahashi Y, Nishikubo N, Hattori T, Demura T, Suzuki S, Umezawa T (2013b) ATL54, a ubiquitin ligase gene related to secondary cell wall formation, is transcriptionally regulated by MYB46. Plant Biotechnol 30:503–509

    Article  CAS  Google Scholar 

  • Ohashi-Ito K, Oda Y, Fukuda H (2010) Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 directly regulates the genes that govern programmed cell death and secondary wall formation during xylem differentiation. Plant Cell 22:3461–3473

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ohtani M, Nishikubo N, Xu B, Yamaguchi M, Mitsuda N, Goué N, Shi F, Ohme-Takagi M, Demura T (2011) A NAC domain protein family contributing to the regulation of wood formation in poplar. Plant J 67:499–512

    Article  CAS  PubMed  Google Scholar 

  • Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rennie EA, Scheller HV (2014) Xylan biosynthesis. Curr Opin Biotechnol 26:100–107

    Article  CAS  PubMed  Google Scholar 

  • Shen H, He X, Poovaiah CR, Wuddineh WA, Ma J, Mann DGJ, Wang H, Jackson L, Tang Y, Stewart CN Jr, 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

    Article  CAS  PubMed  Google Scholar 

  • Silveira RL, Stoyanov SR, Gusarov S, Skaf MS, Kovalenko A (2015) Supramolecular interaction in secondary plant cell walls: effect of lignin chemical composition revealed with the molecular theory of solvation. J Phys Chem Lett 6:206–211

    Article  CAS  PubMed  Google Scholar 

  • Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4:447–456

    Article  CAS  PubMed  Google Scholar 

  • Suzuki S, Li L, Sun YH, Chiang VL (2006) The cellulose synthase gene superfamily and biochemical functions of xylem-specific cellulose synthase-like genes in Populus trichocarpa. Plant Physiol 142:1233–1245

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tanaka K, Murata K, Yamazaki M, Onosato K, Miyao A, Hirochika H (2003) Three distinct rice cellulose synthase catalytic subunit genes required for cellulose synthesis in the secondary wall. Plant Physiol 133:73–83

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Taylor NG, Gardiner JC, Whiteman R, Turner SR (2004) Cellulose synthesis in the Arabidopsis secondary cell wall. Cellulose 11:329–338

    Article  CAS  Google Scholar 

  • Taylor-Teeples M, Lin L, de Lucas M, Turco G, Toal TW, Gaudinier A, Young NF, Trabucco GM, Veling MT, Lamothe R et al (2014) An Arabidopsis gene regulatory network for secondary cell wall synthesis. Nature. doi:10.1038/nature14099

    PubMed Central  PubMed  Google Scholar 

  • Umezawa T (2010) The cinnamate/monolignol pathway. Phytochem Rev 9:1–17

    Article  CAS  Google Scholar 

  • Vogel J (2008) Unique aspects of the grass cell wall. Curr Opin Plant Biol 11:301–307

    Article  CAS  PubMed  Google Scholar 

  • Wang HZ, Dixon RA (2012) On–off switches for secondary cell wall biosynthesis. Mol Plant 5:297–303

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi M, Kubo M, Fukuda H, Demura T (2008) VASCULAR-RELATED NAC-DOMAIN7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots. Plant J 55:652–664

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi M, Ohtani M, Mitsuda N, Kubo M, Ohme-Takagi M, Fukuda H, Demura T (2010) VND-INTERACTING2, a NAC domain transcription factor, negatively regulates xylem vessel formation in Arabidopsis. Plant Cell 22:1249–1263

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yamaguchi K, Imai K, Akamatsu A, Mihashi M, Hayashi N, Shimamoto K, Kawasaki T (2012) SWAP70 functions as a Rac/Rop guanine nucleotide-exchange factor in rice. Plant J 70:389–397

    Article  CAS  PubMed  Google Scholar 

  • Yamamura M, Noda S, Hattori T, Shino A, Kikuchi J, Takabe K, Tagane S, Gau M, Uwatoko N, Mii M, Suzuki S, Shibata D, Umezawa T (2013) Characterization of lignocellulose of Erianthus arundinaceus in relation to enzymatic saccharification efficiency. Plant Biotechnol 30:25–35

    Article  CAS  Google Scholar 

  • Yokoyama KD, Zhang Y, Ma J (2014) Tracing the evolution of lineage-specific transcription factor binding sites in a birth-death framework. PLoS Comput Biol 10:e1003771

    Article  PubMed Central  PubMed  Google Scholar 

  • Yoshida K, Sakamoto S, Kawai T, Kobayashi Y, Sato K, Ichinose Y, Yaoi K, Akiyoshi-Endo M, Sato H, Takamizo T, Ohme-Takagi M, Mitsuda N (2013) Engineering the Oryza sativa cell wall with rice NAC transcription factors regulating secondary wall formation. Front Plant Sci 4:383

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhang K, Qian Q, Huang Z, Wang Y, Li M, Hong L, Zeng D, Gu M, Chu C, Cheng Z (2006) GOLD HULL AND INTERNODE2 encodes a primarily multifunctional cinnamyl-alcohol dehydrogenase in rice. Plant Physiol 140:972–983

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhao K, Bartley LE (2014) Comparative genomic analysis of the R2R3 MYB secondary cell wall regulators of Arabidopsis, poplar, rice, maize, and switchgrass. BMC Plant Biol 14:135

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhao Q, Gallego-Giraldo L, Wang H, Zeng Y, Ding S-Y, Chen F, Dixon RA (2010) An NAC transcription factor orchestrates multiple features of cell wall development in Medicago truncatula. Plant J 63:100–114

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Zhong R, Demura T, Ye ZH (2006) SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18:3158–3170

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhong R, Richardson EA, Ye ZH (2007) The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell 19:2776–2792

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhong R, Lee C, Ye Z-H (2010) Functional characterization of poplar wood-associated NAC domain transcription factors. Plant Physiol 152:1044–1055

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhong R, Lee C, McCarthy RL, Reeves CK, Jones EG, Ye ZH (2011) Transcriptional activation of secondary wall biosynthesis by rice and maize NAC and MYB transcription factors. Plant Cell Physiol 52:1856–1871

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Ms. Kumiko Murata for technical assistance in cultivating rice plants. We appreciate Dr. Koji Yamaguchi and Dr. Tsutomu Kawasaki of Kinki University, Japan, and Dr. Shingo Sakamoto and Dr. Nobutaka Mitsuda of the National Institute of Advanced Industrial Science and Technology (AIST), Japan, for technical advice about protoplast preparation and PEG-mediated transfection. Seeds of O. sativa L. ssp. japonica cv. Nipponbare were a generous gift from the Shiga Prefecture Agricultural Technology Promotion Center, Shiga, Japan. The vectors pH35GS and pBD-GAL4-GWRFC were the kind gifts of Dr. Taku Demura of the Nara Institute of Science and Technology, Japan; and the vectors p35SG, p190LUC, and pPTRL were the kind gifts of Dr. N. Mitsuda and Dr. Masaru Takagi of AIST. Rice Oc suspension cells and rice full-length cDNA clones were provided by RIKEN Bioresouce Center and the National Institute of Agrobiological Sciences, Japan, respectively. This work was partly supported by Grants-in-Aid for Young Scientists (B) (No. 22780161) and for Scientific Research (C) (No. 25450241) from the Japan Society for the Promotion of Science (JSPS); and a grant from the “Advanced Low Carbon Technology Research and Development Program (ALCA)”, managed by the Japan Science and Technology Agency. A part of this study was conducted using the Development and Assessment of Sustainable Humanosphere/Forest Biomass Analytical System (DASH/FBAS) at the Research Institute for Sustainable Humanosphere, Kyoto University, Japan.

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Correspondence to Shiro Suzuki.

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Special topic: Polyphenols: biosynthesis and function in plants and ecosystems. Guest editor: Stefan Martens.

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Noda, S., Koshiba, T., Hattori, T. et al. The expression of a rice secondary wall-specific cellulose synthase gene, OsCesA7, is directly regulated by a rice transcription factor, OsMYB58/63. Planta 242, 589–600 (2015). https://doi.org/10.1007/s00425-015-2343-z

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