Growth modulation effects of CBM2a under the control of AtEXP4 and CaMV35S promoters in Arabidopsis thaliana, Nicotiana tabacum and Eucalyptus camaldulensis

Transgenic Research - Tập 26 - Trang 447-463 - 2017
Pornthep Keadtidumrongkul1, Anongpat Suttangkakul1,2,3, Phitsanu Pinmanee1, Kanokwan Pattana1, Chokchai Kittiwongwattana4, Somsak Apisitwanich1,2,3,5, Supachai Vuttipongchaikij1,2,3
1Department of Genetics, Faculty of Science, Kasetsart University, Bangkok, Thailand
2Special Research Unit in Microalgal Molecular Genetics and Functional Genomics (MMGFG), Department of Genetics, Faculty of Science, Kasetsart University, Bangkok, Thailand
3Center of Advanced Studies for Tropical Natural Resources, Kasetsart University, Bangkok, Thailand
4Department of Biology, Faculty of Science, King Mongkut’s Institute of Technology Ladkrabang, Bangkok, Thailand
5School of Science, Mae Fah Luang University, Chiang Rai, Thailand

Tóm tắt

The expression of cell-wall-targeted Carbohydrate Binding Modules (CBMs) can alter cell wall properties and modulate growth and development in plants such as tobacco and potato. CBM2a identified in xylanase 10A from Cellulomonas fimi is of particular interest for its ability to bind crystalline cellulose. However, its potential for promoting plant growth has not been explored. In this work, we tested the ability of CBM2a to promote growth when expressed using both CaMV35S and a vascular tissue-specific promoter derived from Arabidopsis expansin4 (AtEXP4) in three plant species: Arabidopsis, Nicotiana tabacum and Eucalyptus camaldulensis. In Arabidopsis, the expression of AtEXP4pro:CBM2a showed trends for growth promoting effects including the increase of root and hypocotyl lengths and the enlargements of the vascular xylem area, fiber cells and vessel cells. However, in N. tabacum, the expression of CBM2a under the control of either CaMV35S or AtEXP4 promoter resulted in subtle changes in the plant growth, and the thickness of secondary xylem and vessel and fiber cell sizes were generally reduced in the transgenic lines with AtEXP4pro:CBM2a. In Eucalyptus, while transgenics expressing CaMV35S:CBM2a showed very subtle changes compared to wild type, those transgenics with AtEXP4pro:CBM2a showed increases in plant height, enlargement of xylem areas and xylem fiber and vessel cells. These data provide comparative effects of expressing CBM2a protein in different plant species, and this finding can be applied for plant biomass improvement.

Tài liệu tham khảo

Abramson M, Shoseyov O, Shani Z (2010) Plant cell wall reconstruction toward improved lignocellulosic production and processability. Plant Sci 178(2):61–72 Baghdady A, Blervacq AS, Jouanin L, Grima-Pettenati J, Sivadon P, Hawkins S (2006) Eucalyptus gunnii CCR and CAD2 promoters are active in lignifying cells during primary and secondary xylem formation in Arabidopsis thaliana. Plant Physiol Biochem 44(11):674–683 Bolam DN, Xie H, White P, Simpson PJ, Hancock SM, Williamson MP, Gilbert HJ (2001) Evidence for synergy between family 2b carbohydrate binding modules in Cellulomonas fimi xylanase 11A. Biochemistry 40(8):2468–2477 Boraston AB, Creagh AL, Alam MM, Kormos JM, Tomme P, Haynes CA et al (2001) Binding specificity and thermodynamics of a family 9 carbohydrate-binding module from Thermotoga maritima xylanase 10A. Biochemistry 40(21):6240–6247 Boraston AB, Bolam DN, Gilbert HJ, Davies GJ (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382(3):769–781 Charnock SJ, Bolam DN, Nurizzo D, Szabó L, McKie VA, Gilbert HJ, Davies GJ (2002) Promiscuity in ligand-binding: the three-dimensional structure of a Piromyces carbohydrate-binding module, CBM29-2, in complex with cello-and mannohexaose. Proc Natl Acad Sci USA 99(22):14077–14082 Cho HT, Cosgrove DJ (2000) Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. Proc Natl Acad Sci USA 97(17):9783–9788 Choi D, Lee Y, Cho HT, Kende H (2003) Regulation of expansin gene expression affects growth and development in transgenic rice plants. Plant Cell 15(6):1386–1398 Cosgrove DJ (2016) Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes. J Exp Bot 67(2):463–476 de la Torre F, Rodríguez R, Jorge G, Villar B, Álvarez-Otero R, Grima-Pettenati J, Gallego PP (2014) Genetic transformation of Eucalyptus globulus using the vascular-specific EgCCR as an alternative to the constitutive CaMV35S promoter. Plant Cell, Tissue Organ Cult 117(1):77–84 Dietz KJ (2001) The extracellular matrix of the plant cell: location of signal perception, transduction and response. In: Esser K, Luttge U, Kadereit JW, Beyschlag W (eds) Progress in botany. Springer, Berlin, pp 215–237 Din N, Forsythe IJ, Burtnick LD, Gilkes NR, Miller RC, Warren RAJ, Kilburn DG (1994) The cellulose-binding domain of endoglucanase A (CenA) from Cellulomonas fimi: evidence for the involvement of tryptophan residues in binding. Mol Microbiol 11(4):747–755 Feuillet C, Lauvergeat V, Deswarte C, Pilate G, Boudet A, Grima-Pettenati J (1995) Tissue-and cell-specific expression of a cinnamyl alcohol dehydrogenase promoter in transgenic poplar plants. Plant Mol Biol 27(4):651–667 Freelove AC, Bolam DN, White P, Hazlewood GP, Gilbert HJ (2001) A novel carbohydrate-binding protein is a component of the plant cell wall-degrading complex of Piromyces equi. J Biol Chem 276(46):43010–43017 Gago J, Grima-Pettenati J, Gallego PP (2011) Vascular-specific expression of GUS and GFP reporter genes in transgenic grapevine (Vitis vinifera L. cv. Albariño) conferred by the EgCCR promoter of Eucalyptus gunnii. Plant Physiol Biochem 49(4):413–419 Goldstein MA, Takagi M, Hashida S, Shoseyov O, Doi RH, Segel IH (1993) Characterization of the cellulose-binding domain of the Clostridium cellulovorans cellulose-binding protein A. J Bacteriol 175(18):5762–5768 Gray-Mitsumune M, Blomquist K, McQueen-Mason S, Teeri TT, Sundberg B, Mellerowicz EJ (2008) Ectopic expression of a wood-abundant expansin PttEXPA1 promotes cell expansion in primary and secondary tissues in aspen. Plant Biotech J 6(1):62–72 Guillén D, Sánchez S, Rodríguez-Sanoja R (2010) Carbohydrate-binding domains: multiplicity of biological roles. Appl Microbiol Biotechnol 85(5):1241–1249 Hervé C, Rogowski A, Blake AW, Marcus SE, Gilbert HJ, Knox JP (2010) Carbohydrate-binding modules promote the enzymatic deconstruction of intact plant cell walls by targeting and proximity effects. Proc Natl Acad Sci USA 107(34):15293–15298 Levy I, Shani Z, Shoseyov O (2002) Modification of polysaccharides and plant cell wall by endo-1,4-β-glucanase and cellulose-binding domains. Biomol Eng 19(1):17–30 Kwan EM, Boraston AB, McLean BW, Kilburn DG, Warren RAJ (2005) N-Glycosidase–carbohydrate-binding module fusion proteins as immobilized enzymes for protein deglycosylation. Protein Eng Des Sel 18(10):497–501 Lauvergeat V, Rech P, Jauneau A, Guez C, Coutos-Thevenot P, Grima-Pettenati J (2002) The vascular expression pattern directed by the Eucalyptus gunnii cinnamyl alcohol dehydrogenase EgCAD2 promoter is conserved among woody and herbaceous plant species. Plant Mol Biol 50(3):497–509 McLean BW, Bray MR, Boraston AB, Gilkes NR, Haynes CA, Kilburn DG (2000) Analysis of binding of the family 2a carbohydrate-binding module from Cellulomonas fimi xylanase 10A to cellulose: specificity and identification of functionally important amino acid residues. Protein Eng 13(11):801–809 McQueen-Mason S, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4(11):1425–1433 Nardi C, Escudero C, Villarreal N, Martínez G, Civello PM (2013) The carbohydrate-binding module of Fragaria × ananassa expansin 2 (CBM-FaExp2) binds to cell wall polysaccharides and decreases cell wall enzyme activities “in vitro”. J Plant Res 126(1):151–159 Nardi CF, Villarreal NM, Rossi FR, Martínez S, Martínez GA, Civello PM (2015) Overexpression of the carbohydrate binding module of strawberry expansin2 in Arabidopsis thaliana modifies plant growth and cell wall metabolism. Plant Mol Biol 88(1–2):101–117 Obembe OO, Jacobsen E, Timmers J, Gilbert H, Blake AW, Knox JP et al (2007a) Promiscuous, non-catalytic, tandem carbohydrate-binding modules modulate the cell-wall structure and development of transgenic tobacco (Nicotiana tabacum) plants. J Plant Res 120(5):605–617 Obembe OO, Jacobsen E, Visser R, Vincken JP (2007b) Expression of an expansin carbohydrate-binding module affects xylem and phloem formation. Afr J Biotechnol 6(14):1608–1616 Poon DK, Withers SG, McIntosh LP (2007) Direct demonstration of the flexibility of the glycosylated proline-threonine linker in the Cellulomonas fimi xylanase Cex through NMR spectroscopic analysis. J Biol Chem 282(3):2091–2100 Safra-Dassa L, Shani Z, Danin A, Roiz L, Shoseyov O, Wolf S (2006) Growth modulation of transgenic potato plants by heterologous expression of bacterial carbohydrate-binding module. Mol Breed 17(4):355–364 Shani Z, Shpigel E, Roiz L, Goren R, Vinocur B, Tzfira T, Altman A, Shoseyov O (1999) Cellulose binding domain increases cellulose synthase activity in Acetobacter xylinum, and biomass of transgenic plants. In: Altman A, Ziv M, Izhar S (eds) Plant biotechnology and in vitro biology in the 21st century, vol l. Kluwer, Dordrecht, pp 213–218 Shpigel E, Roiz L, Goren R, Shoseyov O (1998) Bacterial cellulose-binding domain modulates in vitro elongation of different plant cells. Plant Physiol 117(4):1185–1194 Xu GY, Ong E, Gilkes NR, Kilburn DG, Muhandiram DR, Harris-Brandts M et al (1995) Solution structure of a cellulose-binding domain from Cellulomonas fimi by nuclear magnetic resonance spectroscopy. Biochemistry 34(21):6993–7009