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Journal of Integrative Agriculture  2017, Vol. 16 Issue (01): 65-75    DOI: 10.1016/S2095-3119(16)61389-8
Crop Genetics · Breeding · Germplasm Resources Advanced Online Publication | Current Issue | Archive | Adv Search |
SlMYB1 and SlMYB2, two new MYB genes from tomato, transcriptionally regulate cellulose biosynthesis in tobacco
SHI Yan-na1, 2, 3*, LIU Xiao-fen1, 2, 3*, LI Xue1, 2, DONG Wen-cheng1, 2, Donald Grierson1, 4, YIN Xue-ren1, 2, 3, CHEN Kun-song1, 2, 3

1 College of Agriculture & Biotechnology, Zhejiang University, Hangzhou 310058, P.R.China

2 Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Zhejiang University, Hangzhou 310058, P.R.China

Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Ministry of Agriculture, Zhejiang University, Hangzhou 310058, P.R.China

4 Plant & Crop Sciences Division, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD, UK  

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Abstract  Cellulose, a major constituent of plant biomass, is synthesized by a cellulose synthase complex.  It has been demonstrated that MYB genes transcriptionally regulate cellulose synthase in Arabidopsis.  However, little is known about this process in tomato.  Here, two MYB (SlMYB1/2) and three cellulose synthase (CESA) (SlCESA4/5/6) genes were isolated.  SlMYB1/2 and SlCESA4/5/6 accumulation was found to correspond to cellulose accumulation in different tissues of tomato.  Dual luciferase assays indicated that these two MYBs were transcriptional activators that interact with promoters of SlCESA4/5/6.  Moreover, SlMYB2 could also activate promoters of SlMYB1/2, suggesting the possible underlying auto-activation mechanisms for MYB transcription factors.  Transient over-expression of SlMYB1/2 in Nicotiana tabacum up-regulated tobacco endogenous NtCESA genes and increased cellulose accumulation.  The function of SlMYB1/2 was further investigated using stable transformation and the results indicated that N. tabacum lines heterologous expressing SlMYB1/2 displayed a pleiotropic phenotype, long and narrow leaves, with NtCESA induced and significant increase of cellulose.  In conclusion, our data suggest that tomato SlMYB1/2 have transcriptional regulatory roles in cellulose biosynthesis and SlMYB2 was more effective than SlMYB1, which may due to the transcriptional activation by SlMYB2 on SlMYB1 and itself.
Keywords:  MYB      cellulose      cellulose synthase      transcriptional regulation      tomato      tobacco  
Received: 18 December 2015   Accepted:
Fund: 

This research was supported by the International Science & Technology Cooperation Program of China (2011DFB31580), the National Basic Research Program of China (2013CB127104) and the Natural Science Foundation of Zhejiang Province, China (LR16C150001).

Corresponding Authors:  CHEN Kun-song, Tel: +86-571-88982931, Fax: +86-571-88982224, E-mail: akun@zju.edu.cn    
About author:  SHI Yan-na, E-mail: shiyanna@zju.edu.cn

Cite this article: 

SHI Yan-na, LIU Xiao-fen, LI Xue, DONG Wen-cheng, Donald Grierson, YIN Xue-ren, CHEN Kun-song . 2017. SlMYB1 and SlMYB2, two new MYB genes from tomato, transcriptionally regulate cellulose biosynthesis in tobacco. Journal of Integrative Agriculture, 16(01): 65-75.

Adato A, Mandel T, Mintz-Oron S, Venger I, Levy D, Yativ M, Dominguez E, Wang Z H, De Vos R C H, Jetter R, Schreiber L, Heredia A, Rogachev I, Aharoni A. 2009. Fruit-surface flavonoid accumulation in tomato is controlled by a SIMYB12-regulated transcriptional network. PLoS Genetics, 5, e1000777.

Ambawat S, Sharma P, Yadav N R, Yadav R C. 2013. MYB transcription factor genes as regulators for plant responses: An overview. Physiology and Molecular Biology of Plants, 19, 307–321.

Appenzeller L, Doblin M, Barreiro R, Wang H Y, Niu X M, Kollipara K, Carrigan L, Tomes D, Chapman M, Dhugga K S. 2004. Cellulose synthesis in maize: Isolation and expression analysis of the cellulose synthase (CesA) gene family. Cellulose, 11, 287–299.

Arioli T, Peng L C, Betzner A S, Burn J, Wittke W, Herth W, Camilleri C, Hofte H, Plazinski J, Birch R, Cork A, Glover J, Redmond J, Williamson R E. 1998. Molecular analysis of cellulose biosynthesis in Arabidopsis. Science, 279, 717–720.

Ballester A R, Molthoff J, de Vos R, Hekkert B, Orzaez D, Fernandez-Moreno J P, Tripodi P, Grandillo S, Martin C, Heldens J, Ykema M, Granell A, Bovy A. 2010. Biochemical and molecular analysis of pink tomatoes: Deregulated expression of the gene encoding transcription factor SlMYB12 leads to pink tomato fruit color. Plant Physiology, 152, 71–84.

Bhargava A, Mansfield S D, Hall H C, Douglas C J, Ellis B E. 2010. MYB75 functions in regulation of secondary cell wall formation in the Arabidopsis inflorescence stem. Plant Physiology, 154, 1428–1438.

Chai G, Wang Z, Tang X, Yu L, Qi G, Wang D, Yan X, Kong Y, Zhou G. 2014. R2R3-MYB gene pairs in Populus: Evolution and contribution to secondary wall formation and flowering time. Journal of Experimental Botany, 65, 4255–4269.

Correa-Aragunde N, Lombardo C, Lamattina L. 2008. Nitric oxide: An active nitrogen molecule that modulates cellulose synthesis in tomato roots. New Phytologist, 179, 386–396.

Desprez T, Juraniec M, Crowell E F, Jouy H, Pochylova Z, Parcy F, Hofte H, Gonneau M, Vernhettes S. 2007. Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 104, 15572–15577.

Desprez T, Vernhettes S, Fagard M, Refregier G, Desnos T, Aletti E, Py N, Pelletier S, Hofte H. 2002. Resistance against herbicide isoxaben and cellulose deficiency caused by distinct mutations in same cellulose synthase isoform CESA6. Plant Physiology, 128, 482–490.

Djerbi S, Aspeborg H, Nilsson P, Sundberg B, Mellerowicz E, Blomqvist K, Teeri T T. 2004. Identification and expression analysis of genes encoding putative cellulose synthases (CesA) in the hybrid aspen, Populus tremula (L.)×

P. tremuloides (Michx.). Cellulose, 11, 301–312.

Doblin M S, Kurek I, Jacob-Wilk D, Delmer D P. 2002. Cellulose biosynthesis in plants: From genes to rosettes. Plant and Cell Physiology, 43, 1407–1420.

Fadeel A A. 1962. Location and properties of chloroplasts and pigment determination in roots. Physiologia Plantarum, 15, 130–147.

Fu X M, Kong W B, Peng G, Zhou J Y, Azam M, Xu C J, Grierson D, Chen K S. 2012. Plastid structure and carotenogenic gene expression in red- and white-fleshed loquat (Eriobotrya japonica) fruits. Journal of Experimental Botany, 63, 341–354.

Hamann T, Osborne E, Youngs H L, Misson J, Nussaume L, Somerville C. 2004. Global expression analysis of CESA and CSL genes in Arabidopsis. Cellulose, 11, 279–286.

Hellens R P, Allan A C, Friel E N, Bolitho K, Grafton K, Templeton M D, Karunairetnam S, Gleave A P, Laing W A. 2005. Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods, 1, 1746–1748.

Hirano K, Kondo M, Aya K, Miyao A, Sato Y, Antonio B A, Namiki N, Nagamura Y, Matsuoka M. 2013. Identification of transcription factors involved in rice secondary cell wall formation. Plant and Cell Physiology, 54, 1791–1802.

Huang Y J, Song S, Allan A C, Liu X F, Yin X R, Xu C J, Chen K S. 2013. Differential activation of anthocyanin biosynthesis in Arabidopsis and tobacco over-expressing an R2R3 MYB from Chinese bayberry. Plant Cell Tissue and Organ Culture, 113, 491–499.

Kim W C, Ko J H, Han K H. 2012a. Identification of a cis-acting regulatory motif recognized by MYB46, a master transcriptional regulator of secondary wall biosynthesis. Plant Molecular Biology, 78, 489–501.

Kim W C, Ko J H, Kim J Y, Kim J M, Bae H J, Han K H. 2012b. MYB46 directly regulates the gene expression of secondary wall-associated cellulose synthases in Arabidopsis. The Plant Journal, 133, 1051–1071.

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. The Plant Journal, 60, 649–665.

Lacombe E, Van Doorsselaere J, Boerjan W, Boudet A M, Grima-Pettenati J. 2000. Characterization of cis-elements required for vascular expression of the Cinnamoyl CoA Reductase gene and for protein-DNA complex formation. The Plant Journal, 23, 663–676.

Legay S, Sivadon P, Blervacq AS, Pavy N, Baghdady A, Tremblay L, Levasseur C, Ladouce N, Lapierre C, Seguin 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 Phytologist, 188, 774–786.

Lin Q, Hamilton W D O, Merryweather A. 1996. Cloning and initial characterization of 14 myb-related cDNAs from tomato (Lycopersicon esculentum cv. Ailsa Craig). Plant Molecular Biology, 30, 1009–1020.

Liu X F, Yin X R, Allan A C, Lin W K, Shi Y N, Huang Y J, Ferguson I B, Xu C J, Chen K S. 2013. The role of MrbHLH1 and MrMYB1 in regulating anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) during anthocyanin biosynthesis. Plant Cell Tissue and Organ Culture, 115, 285–298.

Mathews H, Clendennen S K, Caldwell C G, Liu X L, Connors K, Matheis N, Schuster D K, Menasco D J, Wagoner W, Lightner J, Wagner D R. 2003. Activation tagging in tomato identifies a transcriptional regulator of anthocyanin biosynthesis, modification, and transport. The Plant Cell, 15, 1689–1703.

McCarthy R L, Zhong R Q, Fowler S, Lyskowski D, Piyasena H, Carleton K, Spicer C, Ye Z H. 2010. The poplar MYB transcription factors, PtrMYB3 and PtrMYB20, are involved in the regulation of secondary wall biosynthesis. Plant and Cell Physiology, 51, 1084–1090.

McCarthy R L, Zhong R Q, Ye Z H. 2009. MYB83 is a direct target of SND1 and acts redundantly with MYB46 in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant and Cell Physiology, 50, 1950–1964.

McFarlane H E, Doring A, Persson S. 2014. The cell biology of cellulose synthesis. Annual Review of Plant Biology, 65, 69–94.

Meng X, Yin B, Feng H L, Zhang S, Liang X Q, Meng Q W. 2014. Overexpression of R2R3-MYB gene leads to accumulation of anthocyanin and enhanced resistance to chilling and oxidative stress. Biologia Pantarum, 58, 121–130.

Min T, Fang F, Ge H, Shi Y N, Luo Z R, Yao Y C, Grierson D, Yin X R, Chen K S. 2014. Two novel anoxia-induced ethylene response factors that interact with promoters of deastringency-related genes from persimmon. PLOS ONE, 9, e97043.

Min T, Yin X R, Shi Y N, Luo Z R, Yao Y C, Grierson D, Ferguson I B, Chen K S. 2012. Ethylene-responsive transcription factors interact with promoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency. Journal of Experimental Botany, 63, 6393–6405.

Nguyen C V, Vrebalov J T, Gapper N E, Zheng Y, Zhong S, Fei Z, Giovannoni J J. 2014. Tomato GOLDEN2-LIKE transcription factors reveal molecular gradients that function during fruit development and ripening. The Plant Cell, 26, 585–601.

Ohman D, Demedts B, Kumar M, Gerber L, Gorzsas A, Goeminne G, Hedenstrom M, Ellis B, Boerjan W, Sundberg B. 2012. MYB103 is required for FERULATE–5-HYDROXYLASE expression and syringyl lignin biosynthesis in Arabidopsis stems. The Plant Journal, 73, 63–76.

Perrin R M. 2001. Czellulose: How many cellulose synthases to make a plant? Current Biology, 11, R213-R216.

Powell A L, Nguyen C V, Hill T, Cheng K L, Figueroa-Balderas R, Aktas H, Ashrafi H, Pons C, Fernandez-Munoz R, Vicente A, Lopez-Baltazar J, Barry C S, Liu Y, Chetelat R, Granell A, Van Deynze A, Giovannoni J J, Bennett A B. 2012. Uniform ripening encodes a Golden 2-like transcription factor regulating tomato fruit chloroplast development. Science, 336, 1711–1715.

Raes J, Rohde A, Christensen J H, Van de Peer Y, Boerjan W. 2003. Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiology, 133, 1051–1071.

Robert S, Mouille G, Hofte H. 2004. The mechanism and regulation of cellulose synthesis in primary walls: Lessons from cellulose-deficient Arabidopsis mutants. Cellulose, 11, 351–364.

Scheible W R, Eshed R, Richmond T, Delmer D, Somerville C. 2001. Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis Ixr1 mutants. Proceedings of the National Academy of Sciences of the United States of America, 98, 10079–10084.

Schreiber G, Reuveni M, Evenor D, Oren-Shamir M, Ovadia R, Sapir-Mir M, Bootbool-Man A, Nahon S, Shlomo H, Chen L, Levin I. 2012. ANTHOCYANIN1 from Solanum chilense is more efficient in accumulating anthocyanin metabolites than its Solanum lycopersicum counterpart in association with the ANTHOCYANIN FRUIT phenotype of tomato. Theoretical and Applied Genetics, 124, 295–307.

Shan L L, Li X, Wang P, Cai C, Zhang B, De Sun C, Zhang W S, Xu C J, Ferguson I, Chen K S. 2008. Characterization of cDNAs associated with lignification and their expression profiles in loquat fruit with different lignin accumulation. Planta, 227, 1243–1254.

Taylor N G, Howells R M, Huttly A K, Vickers K, Turner S R. 2003. Interactions among three distinct CesA proteins essential for cellulose synthesis. Proceedings of the National Academy of Sciences of the United States of America, 100, 1450–1455.

Taylor N G, Laurie S, Turner S R. 2000. Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. The Plant Cell, 12, 2529–2539.

Turner S R, Somerville C R. 1997. Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. The Plant Cell, 9, 689–701.

Updegraf D M. 1969. Semimicro determination of cellulose in biological materials. Analytical Biochemistry, 32, 420–424.

Wang W W, Zhu C Q, Liu X H, Chen K S, Xu C J. 2011. Techniques for rapid preparation of tomato leaf DNA and its application in real-time quantitative PCR-based transgene detection. Hereditas (Beijing), 33, 1017–1022. (in Chinese)

Xu Q, Yin X R, Zeng J K, Ge H, Song M, Xu C J, Li X, Ferguson I B, Chen K S. 2014. Activator- and repressor-type MYB transcription factors are involved in chilling injury induced flesh lignification in loquat via their interactions with the phenylpropanoid pathway. Journal of Experimental Botany, 65, 4349–4359.

Yang C, Li D, Liu X, Ji C, Hao L, Zhao X, Li X, Chen C, Cheng Z, Zhu L. 2014. OsMYB103L, an R2R3-MYB transcription factor, influences leaf rolling and mechanical strength in rice (Oryza sativa L.). BMC Plant Biology, 14, 158.

Yin X R, Allan A C, Chen K S, Ferguson I B. 2010. Kiwifruit EIL and ERF genes involved in regulating fruit ripening. Plant Physiology, 153, 1280–1292.

Yin X R, Chen K S, Allan A C, Wu R M, Zhang B, Lallu N, Ferguson I B. 2008. Ethylene-induced modulation of genes associated with the ethylene signalling pathway in ripening kiwifruit. Journal of Experimental Botany, 59, 2097–2108.

Zhao P, Li Q, Li J, Wang L, Ren Z. 2014. Genome-wide identification and characterization of R2R3MYB family in Solanum lycopersicum. Molecular Genetics and Genomics, 289, 1183–1207.

Zhong R, Lee C, McCarthy R L, Reeves C K, Jones E G, Ye Z H. 2011. Transcriptional activation of secondary wall biosynthesis by rice and maize NAC and MYB transcription factors. Plant and Cell Physiology, 52, 1856–1871.

Zhong R, McCarthy R L, Haghighat M, Ye Z H. 2013. The poplar MYB master switches bind to the SMRE site and activate the secondary wall biosynthetic program during wood formation. PLOS ONE, 8, e69219.

Zhong R, Richardson E A, Ye Z H. 2007. The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. The Plant Cell, 19, 2776–2792.

Zhong R, Ye Z H. 2012. MYB46 and MYB83 bind to the SMRE sites and directly activate a suite of transcription factors and secondary wall biosynthetic genes. Plant and Cell Physiology, 53, 368–380.

Zhong R Q, Lee C H, Ye Z H. 2010. Evolutionary conservation of the transcriptional network regulating secondary cell wall biosynthesis. Trends in Plant Science, 15, 625–632.

Zhong R Q, Lee C H, Zhou J L, McCarthy R L, Ye Z H. 2008. A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. The Plant Cell, 20, 2763–2782.

Zhou J L, Lee C H, Zhong R Q, Ye Z H. 2009. MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. The Plant Cell, 21, 248–266.
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