Allelic variation in the coumarate 3-hydroxylase gene associated with wood properties of Catalpa fargesii Bur.

Abstract

Coumarate 3-hydroxylase (C3h) genes participate in the synthesis of lignin and may affect the properties of wood that are important for its commercial value. A better understanding of the natural variation in C3h genes and their associations to wood properties is required to effectively improve wood quality. We used a candidate gene-based association mapping approach to identify CfC3h allelic variants associated with traits that affect the wood properties of Catalpa fargesii. We first isolated the full-length CfC3h cDNA (1825 bp), which was expressed at relatively high levels in xylem according to real time-polymerase chain reaction. In totally, 17 common single-nucleotide polymorphisms (minor allele frequency > 5%) were identified through cloning and sequencing the CfC3h locus from a mapping population (including 88 unrelated natural C. fargesii individuals collected from main distribution area). Nucleotide diversity and linkage disequilibrium (LD) in CfC3h indicate that CfC3h has low nucleotide diversity (π _t = 0.0031 and θ _w = 0.0103) and relatively low LD (within 1800 bp; r ² ≥ 0.1). An association analysis identified eight common single-nucleotide polymorphisms (SNPs) (false discovery rate, Q < 0.10) and ten haplotypes (Q < 0.10) associated with wood properties, explaining 4.92–12.09% of the phenotypic variance in an association population consisted of 125 unrelated natural individuals (The 88 individuals from the mapping population were comprised in the association population). Our study would provide new insight into C3h gene affecting wood quality, and the SNP markers identified would have potential applications in marker-assisted breeding in the future.

Keywords

Catalpa fargesii / Coumarate 3-hydroxylase / Haplotype-based association analyses / Linkage disequilibrium / Single-nucleotide polymorphisms / Wood properties

References

[1] Abdurakhmonov I, Abdukarimov A. Application of association mapping to understanding the genetic diversity of plan germplasm resources. Int J Plant Genomics, 2008 2008 2 574927

[2] Bate N, Sivasankar S, Moxon C, Riley J, Thompson J, Rothstein S. Molecular characterization of an Arabidopsis gene encoding hydroperoxide lyase, a cytochrome P-450 that is wound inducible. Plant Physiol, 1998, 117(4): 1393-1400.

[3] Beaulieu J, Doerksen T, Boyle B, Clément S, Deslauriers M. Association genetics of wood physical traits in the conifer white spruce and relationships with gene expression. Genetics, 2011, 188: 197-214.

[4] Carocha V, Soler M, Hefer C, Cassan-Wang H, Fevereiro P, Myburg A, Paiva J, Grima-pettenati J. Genome-wide analysis of the lignin toolbox of Eucalyptus grandis. New Phytol, 2015, 206(4): 1297-1313.

[5] Chu Y, Huang Q, Zhang B, Ding C, Su X. Expression and molecular evolution of two DREB1 genes in black poplar (Populus nigra). PLoS ONE, 2014, 9: e98334.

[6] Dillon S, Brawner J, Meder R, Lee D, Southerton S. Association genetics in Corymbia citriodora subsp variegata identifies single nucleotide polymorphisms affecting wood growth and cellulosic pulp yield. New Phytol, 2012, 195(3): 596-608.

[7] Du Q, Xu B, Pan W, Gong C, Wang Q, Tian J, Li B, Zhang D. Allelic variation in a cellulose synthase gene (PtoCesA4) associated with growth and wood properties in Populus tomentosa. G3 Genes Genomes Genet, 2013, 3(11): 2069-2084.

[8] Du Q, Gong C, Wang Q, Zhou D, Yang H, Pan W, Li B, Zhang D. Genetic architecture of growth traits in Populus revealed by integrated quantitative trait locus (QTL) analysis and association studies. New Phytol, 2016, 209(3): 1067-1082.

[9] Du Q, Yang X, Xie J, Quan M, Xiao L, Lu W, Tian J, Gong C, Chen J, Li B, Zhang D. Time-specific and pleiotropic quantitative trait loci coordinately modulate stem growth in Populus. Plant Biotechnol J, 2019, 17(3): 608-624.

[10] Duan H, Cao S, Zheng H, Hu D, Lin J, Lin H, Hu R, Sun Y, Li Y. Variation in the growth traits and wood properties of Chinese Fir from six provinces of southern China. Forests, 2016 7 9 192

[11] Eckert A, Bower A, Wegrzyn J, Pande B, Jermstad K, Krutovsky K, Clair J, Neale D. Association genetics of coastal Douglas fir (Pseudotsuga menziesii var. menziesii, Pinaceae) I Cold-hardiness related traits. Genetics, 2009, 182: 1289-1302.

[12] Fang X, Xu H, Zhang C, Zhang J, Lan X, Gu C, Chen H. Polymorphisms in BMP-2 gene and their associations with growth traits in goats. Genes Genom, 2010, 32: 29-35.

[13] Fornalé S, Rencoret J, Garcia-Calvo L, Capellades M, Encina A, Santiago R, Rigau J, Gutierrez A, del Rio J, Caparros-Ruiz D. Cell wall modifications triggered by the down-regulation of Coumarate 3-hydroxylase-1 in maize. Plant Sci, 2015, 236: 272-282.

[14] Guerra F, Wegrzyn J, Sykes R, Davis M, Stanton B, Neale D. Association genetics of chemical wood properties in black poplar (Populus nigra). New Phytol, 2013, 197: 162-176.

[15] Hill W, Robertson A. Linkage disequilibrium in finite populations. Theor Appl Genet, 1968, 38: 226-231.

[16] Jing D, Xia Y, Chen F, Wang Z, Zhang S, Wang J. Ectopic expression of a Catalpa bungei (Bignoniaceae) PISTILLATA homologue rescues the petal and stamen identities in Arabidopsis pi-1 mutant. Plant Sci, 2015, 231: 40-51.

[17] Jones L, Ennos AR, Turner S. Cloning and characterization of irregular xylem4 (irx4): a severely lignin-deficient mutant of Arabidopsis. Plant J, 2001, 26(2): 205-216.

[18] Kim G, Tsukaya H, Uchimiya H. The ROTUNDIFOLIA3 gene of Arabidopsis thalianaen codes a new member of the cytochrome P-450 family that is required for the regulated polar elongation of leaf cells. Genes Dev, 1998, 12(15): 2381-2391.

[19] Kim J, Ciesielski P, Donohoe B, Chapple C, Li X. Chemically induced conditional rescue of the reduced epidermal fluorescence8 mutant of Arabidopsis reveals rapid restoration of growth and selective turnover of secondary metabolite pools. Plant Physiol, 2014, 164(2): 584-595.

[20] Lamara M, Raherison E, Lenz P, Beaulieu J, Bousquet J, Mackay J. Genetic architecture of wood properties based on association analysis and co-expression networks in white spruce. New Phytol, 2016, 210(1): 240-255.

[21] Larkin M, Blackshields G, Brown N, Chenna R, McGettigan P, McWillam H, Valentin F, Wallace I, Wilm A, Lopez R, Thompon J, Gibson T, Higgins D. Clustal W and Clustal X version 2.0. Bioinformatics, 2007, 23: 2947-2948.

[22] Lenz P, Beaulieu J, Mansfield SD, Clément S, Desponts M, Bousquet J. Factors affecting the accuracy of genomic selection for growth and wood quality traits in an advanced-breeding population of black spruce (Picea mariana). BMC Genomics, 2017 18 1 335

[23] Li X, Jia J, Wang J, Ma W, Ma J, Zhao Q. Morphological diversity analysis and preliminary construction of core collection of Catalpa fargesii Bureau. J Plant Genet Resour, 2013, 14(2): 243-248. (in Chinese)

[24] Li Q, Wang J, Li D, Hu C, Qi S. Wood traits of Picea crassifolia clones. J Northeast For Univ, 2015, 43(12): 12-16. (in Chinese)

[25] Lisperguer J, Perez P, Urizar S. Structure and thermal properties of lignins: characterization by infrared spectroscopy and differential scanning calorimetry. J Chil Chem Soc, 2009, 54(4): 460-463.

[26] Lu N, Mei F, Wang Z, Wang N, Xiao Y, Kong L, Qu G, Ma W, Wang J. Single-nucleotide polymorphisms (SNPs) in a sucrose synthase gene are associated with wood properties in Catalpa fargesii Bur. BMC Genet, 2018 19 1 99

[27] Nei M. Molecular evolutionary genetics, 1987, New York: Columbia University Press

[28] Özparpucu M, Rüggeberg M, Gierlinger N, Cesarino I, Vanholme R, Boerjan W, Burgert I. Unravelling the impact of lignin on cell wall mechanics–a comprehensive study on young poplar trees downregulated for Cinnamyl Alcohol Dehyrogenase (CAD). Plant J, 2017, 91: 480-490.

[29] Poovaiah C, Nageswara-Rao M, Soneji J, Baxter H, Stewart C Jr. Altered lignin biosynthesis using biotechnology to improve lignocellulosic biofuel feedstocks. Plant Biotechnol J, 2014, 12(9): 1163-1173.

[30] Porth I, Klapšte J, Skyba O, Hannemann J, McKown AD, Guy RD, DiFazio SP, Muchero W, Ranjan P, Tuskan GA, Friedmann MC, Ehlting J, Cronk Q, EI-Kassaby YA, Douglas CJ, Mansfied SD. Genome wide association mapping for wood characteristics in populus identifies an array of candidate single nucleotide polymorphisms. New Phytol, 2013, 200: 710-726.

[31] Rafalskia A. Applications of single nucleotide polymorphisms in crop genetics. Curr Opin Plant Biol, 2002, 5: 94-100.

[32] Ralph J, Akiyama T, Kim H, Lu F, Schatz P, Marita J, Ralph S, Reddy M, Chen F, Dixon R. Effects of coumarate 3-hydroxylase down-regulation on lignin structure. J Biol Chem, 2006, 281(13): 8843-8853.

[33] Resende M, Resende M, Sansaloni C, Petroli C, Missiaggia A, Aguiar A, Abad J, Takahashi E, Rosado A, Faria D, Pappas G Jr, Kilian A, Grattapaglia D. Genomic selection for growth and wood quality in Eucalyptus: capturing the missing heritability and accelerating breeding for complex traits in forest trees. New Phytol, 2012, 194(1): 116-128.

[34] Resende R, Resende M, Silva F, Azevedo C, Takahashi E, Silva-Junior O, Grattapagila D. Regional heritability mapping and genome-wide association identify loci for complex growth, wood and disease resistance traits in Eucalyptus. New Phytol, 2017, 213(3): 1287-1300.

[35] Ritland K. Estimators for pairwise relatedness and individual inbreeding coefficients. Genet Res, 1996, 67: 175-185.

[36] Storey J, Tibshirani R. Statistical significance for genome wide studies. Proc Natl Acad Sci, 2003, 100: 9440-9445.

[37] Sykes R, Gjersing E, Foutz K, Rottmann W, Kuhn S, Foster C, Ziebell A, Turner G, Decker S, Hinchee M, Davis M. Down-regulation of p-coumaroyl quinate/shikimate 3′-hydroxylase (C3′H) and cinnamate 4-hydroxylase (C4H) genes in the lignin biosynthetic pathway of Eucalyptus urophylla × E. grandis leads to improved sugar release. Biotechnol Biofuels, 2015 8 1 128

[38] Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol, 2011, 28: 2731-2739.

[39] Thavamanikumar S, McManus L, Ades P, Bossinger G, Stackpole D, Kerr R, Hadjigol S, Freeman J, Vaillancourt R, Zhu P, Tibbits J. Association mapping for wood quality and growth traits in Eucalyptus globulus ssp. globulus Labill identifies nine stable marker-trait associations for seven traits. Tree Genet Genomes, 2014, 10(6): 1661-1678.

[40] Tian J, Chang M, Du Q, Xu B, Zhang D. Single-nucleotide polymorphisms in PtoCesA7 and their association with growth and wood properties in Populus tomentosa. Mol Genet Genomics, 2014, 289(3): 439-455.

[41] Vanholme B, Cesarino I, Goeminne G, Kim H, Marroni F, Acker RV, Vanholme R, Morreel K, Ivens B, Pinosio S, Morgante M, Ralph J, Bastien C, Mansfield S. Breeding with rare defective alleles (BRDA): a natural Populus nigra HCT mutant with modified lignin as a case study. New Phytol, 2013, 198: 765-776.

[42] Wang X, Liu Z, Liu Y. Principal component analysis on micrograph character parameter of wood transverse section. J Northeast For Univ, 2005, 33(5): 30-32. (in Chinese)

[43] Wang L, Wang B, Du Q, Chen J, Tian J, Yang X, Zhang D. Allelic variation in PtoPsbW associated with photosynthesis, growth, and wood properties in Populus tomentosa. Mol Genet Genomics, 2017, 292(1): 77-91.

[44] Wang JP, Matthews ML, Williams CM, Shi R, Yang C, Tunlaya-Anukit S, Chen HC, Li Q, Liu J, Lin CY, Naik P, Sun YH, Loziuk PL, Yeh TF, Kim H, Gjersing E, Shollenberger T, Shuford CM, Song J, Miller Z, Huang YY, Edmunds CW, Liu B, Sun Y, Lin YJ, Li W, Chen H, Peszlen I, Ducoste JJ, Ralph J, Chang HM, Muddiman DC, Davis MF, Smith C, Isik F, Sederoff R, Chiang VL. Improving wood properties for wood utilization through multi-omics integration in lignin biosynthesis. Nat Commun, 2018 9 1 1579

[45] Watterson G. On the number of segregating sites in genetical models without recombination. Theor Popul Biol, 1975, 7: 256-276.

[46] Wegrzyn J, Eckert A, Choi M, Lee J, Stanton B, Sykes R, Davis M, Tsai C, Neale D. Association genetics of traits controlling lignin and cellulose biosynthesis in black cottonwood (Populus trichocarpa, Salicaceae) secondary xylem. New Phytol, 2010, 188(2): 515-532.

[47] Zaykin D, Westfall P, Young S, Karnoub M, Wagner M, Ehm M. Testing association of statistically inferred haplotypes with discrete and continuous traits in samples of unrelated individuals. Hum Hered, 2002, 53: 79-91.

[48] Zhang D, Yang X, Zhang Z, Li B. Expression and nucleotide diversity of the poplar COBL gene. Tree Genet Genomes, 2010, 6: 331-344.

[49] Zhao Q, Ma J, Wang J, Feng X, Ma L, Chen J. Blastation and diversities of Catalpa Fargesii genetic resources among basions. J Plant Genet Resour, 2012, 13(5): 803-809. (in Chinese)

[50] Zheng H, Hu D, Wang R, Wei R, Yan S. Assessing 62 Chinese Fir (Cunninghamia lanceolata) breeding parents in a 12-year grafted clone test. Forests, 2015, 6(10): 3799-3808.