Effect of the suppression of BpAP1 on the expression of lignin related genes in birch

Abstract

Lignin is an integral part of secondary cell walls in plants and plays important roles in maintaining the strength of stems, enhancing transport ability of stems, and providing resistance to multiple stresses. Lignin biosynthesis has become one of the hotspots in molecular forest biology research. The AP1 transcription factor plays important roles in plant flower development. However, in this study, suppression of BpAP1 altered the transcription profiles of white birch and RNA-seq was used to find that suppression of BpAP1 changed the expression of lignin pathway-related genes; C4H/CYP73A, POD were down-regulated and HCT, CCoAOMT, REF1 and CAD were up-regulated. Cell walls of the suppressed transgenic birch were significantly thinner than the wild type of birch, and BpAP1- repressed birch contained less lignin. In addition to regulation of floral development, BpAP1 might play a role in regulating the expression of genes in lignin biosynthesis of birch. This study could provide a new insight into the function of AP1 genes in woody species.

Keywords

BpAP1 / Lignin biosynthesis / RNA-seq / Wood fiber cell walls

References

[1] Bhuiyan NH, Selvaraj G, Wei Y, King J. Role of lignification in plant defense. Plant Signal Behav, 2009, 4: 158-159.

[2] Bjurhager I, Olsson AM, Zhang B, Gerber L, Kumar M, Berglund LA, Burgert I, Sundberg B, Salmén L. Ultrastructure and mechanical properties of Populus wood with reduced lignin content caused by transgenic down-regulation of cinnamate 4-hydroxylase. Bio Macromol, 2010, 11(9): 2359-2365.

[3] Blee K, Choi JW, O’Connell AP, Jupe SC, Schuch W, Lewis NG, Bolwell GP. Antisense and sense expression of cDNA coding for CYP73A15, a class II cinnamate 4-hydroxylase, leads to a delayed and reduced production of lignin in tobacco. Phyto Chem, 2001, 57(7): 1159-1166.

[4] Boerjan W, Ralph J, Baucher M. Lignin biosynthesis. Ann Rev Plant Biol, 2003, 54(1): 519-546.

[5] Boudet AM, Kajita S, Grima-Pettenati J, Goffner D. Lignins and lignocellulosics: a better control of synthesis for new and improved uses. Trends Plant Sci, 2003, 8: 576-581.

[6] Chabannes M, Ruel K, Yoshinaga A, Chabbert B, Jauneau A, Joseleau JP, Boudet AM. In situ analysis of lignins in transgenic tobacco reveals a differential impact of individual transformations on the spatial patterns of lignin deposition at the cellular and subcellular levels. Plant J, 2001, 28: 271-282.

[7] Chang S, Puryear J, Cairney J. A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep, 1993, 11: 113-116.

[8] Chen S, Lin X, Zhang D, Li Q, Zhao X, Chen S. Genome-wide analysis of NAC gene family in Betula pendula. Forests, 2019 10 9 741

[9] Chi Y, Huang F, Liu H, Yang S, Yu D. An APETALA1-like gene of soybean regulates flowering time and specifies floral organs. J Plant Physiol, 2011, 168: 2251-2259.

[10] Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 2005, 21: 3674-3676.

[11] Cseke LJ, Sen B, Ravinder N, Karnosky DF. MADS-box genes in dioecious aspen I: characterization of PTM1 and PTM2 floral MADS-box genes. Physiol Mol Biol Plants, 2003, 9: 187-196.

[12] Day A, Neutelings G, Nolin F, Grec S, Habrant A, Croˆnier D, Maher B, Rolando C, David H, Chabbert B, Hawkins S. Caffeoyl coenzyme A O–methyl transferase down-regulation is associated with modifications in lignin and cell-wall architecture in flax secondary xylem. Plant Physiol Biochem, 2009, 47(1): 9-19.

[13] Dence C (1992) The determination of lignin. Methods in lignin chemistry. Springer, Berlin, pp 33–61

[14] Elo A, Lemmetyinen J, Turunen ML, Tikka L, Sopanen T. Three MADS-box genes similar to APETALA1 and FRUITFULL from silver birch (Betula pendula). Physiol Plant, 2001, 112: 95-103.

[15] Fernando DD, Zhang S. Constitutive expression of the SAP1 gene from willow (Salix discolor) causes early flowering in Arabidopsis thaliana. Dev Genes Evol, 2005, 216: 19-28.

[16] Gang H, Li R, Zhao Y, Liu G, Chen S, Jiang J. Loss of GLK1 transcription factor function reveals new insights in chlorophyll biosynthesis and chloroplast development. J Exp Bot, 2019, 70: 3125-3138.

[17] Gotz S, Garcia-Gomez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talón M, Dopazo J, Conesa A. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res, 2008, 36(10): 3420-3435.

[18] Guo D, Chen F, Inoue K, Blount JW, Dixon RA. Down regulation of caffeic acid 3-O-methyl transferase and caffeoyl CoA 3-O-methyltransferase in transgenic alfalfa: impacts on lignin structure and implications for the biosynthesis of G and S lignin. Plant Cell Online, 2001, 13(1): 73-88.

[19] Huang H, Chen S, Li H, Jiang J. Next-generation transcriptome analysis in transgenic birch overexpressing and suppressing APETALA1 sheds lights in reproduction development and diterpenoid biosynthesis. Plant Cell Rep, 2015, 34: 1663-1680.

[20] Huang H, Wang S, Jiang J, Liu G, Li H, Chen S, Xu H. Overexpression of BpAP1 induces early flowering and produces dwarfism in Betula platyphylla × Betula pendula. Physiol Plant, 2014, 151(4): 495-506.

[21] Irish VF, Sussex IM. Function of the apetala-1 gene during Arabidopsis floral development. Plant Cell, 1990, 2: 741-753.

[22] Ithal N, Recknor J, Nettleton D, Maier T, Baum TJ, Mitchum MG. Developmental transcript profiling of cyst nematode feeding cells in soybean roots. Mol Plant Microbe Interact, 2007, 20: 510-525.

[23] Jaya ESKD, Clemens J, Song J, Zhang H, Jameson PE. Quantitative expression analysis of meristem identity genes in Eucalyptus occidentalis: AP1 is an expression marker for flowering. Tree Physiol, 2009, 30: 304-312.

[24] Kotoda N, Wada M, Kusaba S, Kano-Murakami Y, Masuda T, Soejima J. Overexpression of MdMADS5, an APETALA1-like gene of apple, causes early flowering in transgenic Arabidopsis. Plant Sci, 2005, 162: 679-687.

[25] Lapierre C, Rolando C, Monties B. Characterization of poplar lignins acidolysis products: capillary gas-liquid and liquid-liquid chromatography of monomeric compounds. Holzforschung, 1983, 37(4): 189-198.

[26] Li HY, Yang Y, Wang ZJ, Guo XH, Liu FF, Liu GF, Jiang J. BpMADS12 gene role in lignin biosynthesis of Betula platyphylla Suk by transcriptome analysis. J For Res, 2016, 27(5): 1111-1120.

[27] Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2^-ΔΔCT Method. Methods, 2001, 25: 402-408.

[28] Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF. Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature, 1992, 360: 273-277.

[29] Pea L, Martín-Trillo M, Juárez J, Pina JA, Martínez-Zapater JM. Constitutive expression of Arabidopsis leafy or apetala1 genes in citrus reduces their generation time. Nat Biotechnol, 2001, 19(3): 263-267.

[30] Plomion C, Leprovost G, Stokes A. Wood formation in trees. Plant Physiol, 2001, 127: 1513-1523.

[31] Reddy MSS, Chen F, Shadle G, Jackson L, Aljoe H, Dixon RA. Targeted down-regulation of cytochrome P450 enzymes for forage quality improvement in alfalfa (Medicago sativa L.). PNAS, 2005, 102(46): 16573-16578.

[32] Ritonga FN, Chen S. Physiological and molecular mechanism involved in cold stress tolerance in plants. Plants, 2020 9 5 560

[33] Robinson MD, McCarthy DJ, Smyth GK. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 2010, 26(1): 139-140.

[34] Schilmiller AL, Stout J, Weng JK, Humphreys J, Ruegger MO, Chapple C. Mutations in the cinnamate 4-hydroxylase gene impact metabolism, growth and development in Arabidopsis. Plant J, 2009, 60(5): 771-782.

[35] Sewalt VJH, Ni W, Blount JW, Jung HG, Masoud SA, Howles PA, Lamb C, Dixon RA. Reduced lignin content and altered lignin composition in transgenic tobacco down-regulated in expression of L-phenylalanine ammonia-lyase or cinnamate 4-hydroxylase. Plant Physiol, 1997, 115(1): 41-50.

[36] Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 2009, 25: 1105-1111.

[37] Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol, 2010, 28: 511-515.

[38] Wang F, Chen S, Liang D, Qu G, Chen S, Zhao X. Transcriptomic analyses of Pinus koraiensis under different cold stresses. BMC Genomics, 2020, 21: 1-14.

[39] Wang S, Huang H, Han R, Chen J, Jiang J, Li H, Liu G, Chen S. BpAP1 directly regulates BpDEF to promote male inflorescence formation in Betula platyphylla × B. pendula. Tree Physiol, 2019, 39: 1046-1060.

[40] Whiting P, Favis B, St-Germain F, Goring D. Fractional separation of middle lamella and secondary wall tissue from spruce wood. J Wood Chem Technol, 1981, 1: 29-42.

[41] Yu H, Liu Y, Cui Y, Liu Z. Measurement of wood micro structural parameters on transverse section by binary morphology. Mater Sci Technol, 2008, 16(1): 107-111.

[42] Zabala G, Zou J, Tuteja J, Gonzalez DO, Clough SJ, Vodkin LO. Transcriptome changes in the phenylpropanoid pathway of glycine max in response to Pseudomonas syringae infection. BMC Plant Biol, 2006, 6: 26.

[43] Zhao HY, Zhang JX, Liu HR, Wang T, Song YR, Wei JH. Inhibition of COMT and CCOAOMT on the biosynthesis of plant lignin. Chin Sci Bull, 2002, 47(8): 604-607.