High-resolution genetic mapping of allelic variants associated with cell wall chemistry in Populus

BMC Genomics

Gerald A Tuskan⁹  Olaf Czarnecki⁹  Luke M Evans⁸  Wendy Schackwitz⁴  Joel Martin⁴  Shawn D Mansfield⁶  Carl J Douglas¹  Yousry A El-Kassaby⁵  Faride Unda⁶  Oleksandr Skyba⁶  Ilga Porth⁵  Jaroslav Klápště⁵  Angela Ziebell²  Robert Sykes²  Anthony C Bryan⁹  Sara Jawdy⁹  Lee E Gunter⁹  Gancho T Slavov³  Priya Ranjan⁹  Jin-Gui Chen⁹  Stephen P DiFazio⁸  Jianjun Guo⁷  Wellington Muchero⁹ 

[1] Department of Botany, University of British Columbia, Vancouver V6T 1Z4, BC, Canada;Bioscience Center, National Renewable Energy Laboratory, 15013 Denver West Parkway, Golden CO 80401, USA;Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth SY23 3EB, UK;U.S. Department of Energy Joint Genome Institute, Walnut Creek 94598, CA, USA;Department of Forest and Conservation Sciences, Faculty of Forestry, University of British Columbia, Forest Sciences Centre, 2424 Main Mall, Vancouver V6T 1Z4, BC, Canada;Department of Wood Science, Faculty of Forestry, University of British Columbia, Forest Sciences Centre, 2424 Main Mall, Vancouver V6T 1Z4, BC, Canada;Current address: Department of Plant Biology, Carnegie Institute for Science, Stanford 94305, CA, USA;Department of Biology, West Virginia University, Morgantown 26506, WV, USA;BioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge 37831, TN, USA

关键词: Hemicellulose;    Cellulose;    Lignin;    Cell wall recalcitrance;    Association genetics;    QTL cloning;   

Others  :  1109675
DOI  :  10.1186/s12864-015-1215-z

 received in 2014-04-27, accepted in 2015-01-02,  发布年份 2015

【 摘 要 】

Background

QTL cloning for the discovery of genes underlying polygenic traits has historically been cumbersome in long-lived perennial plants like Populus. Linkage disequilibrium-based association mapping has been proposed as a cloning tool, and recent advances in high-throughput genotyping and whole-genome resequencing enable marker saturation to levels sufficient for association mapping with no a priori candidate gene selection. Here, multiyear and multienvironment evaluation of cell wall phenotypes was conducted in an interspecific P. trichocarpa x P. deltoides pseudo-backcross mapping pedigree and two partially overlapping populations of unrelated P. trichocarpa genotypes using pyrolysis molecular beam mass spectrometry, saccharification, and/ or traditional wet chemistry. QTL mapping was conducted using a high-density genetic map with 3,568 SNP markers. As a fine-mapping approach, chromosome-wide association mapping targeting a QTL hot-spot on linkage group XIV was performed in the two P. trichocarpa populations. Both populations were genotyped using the 34 K Populus Infinium SNP array and whole-genome resequencing of one of the populations facilitated marker-saturation of candidate intervals for gene identification.

Results

Five QTLs ranging in size from 0.6 to 1.8 Mb were mapped on linkage group XIV for lignin content, syringyl to guaiacyl (S/G) ratio, 5- and 6-carbon sugars using the mapping pedigree. Six candidate loci exhibiting significant associations with phenotypes were identified within QTL intervals. These associations were reproducible across multiple environments, two independent genotyping platforms, and different plant growth stages. cDNA sequencing for allelic variants of three of the six loci identified polymorphisms leading to variable length poly glutamine (PolyQ) stretch in a transcription factor annotated as an ANGUSTIFOLIA C-terminus Binding Protein (CtBP) and premature stop codons in a KANADI transcription factor as well as a protein kinase. Results from protoplast transient expression assays suggested that each of the polymorphisms conferred allelic differences in the activation of cellulose, hemicelluloses, and lignin pathway marker genes.

Conclusion

This study illustrates the utility of complementary QTL and association mapping as tools for gene discovery with no a priori candidate gene selection. This proof of concept in a perennial organism opens up opportunities for discovery of novel genetic determinants of economically important but complex traits in plants.

【 授权许可】

   
2015 Muchero et al.; licensee Biomed Central.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Dinus RJ, Payne P, Sewell MM, Chiang VL, Tuskan GA: Genetic modification of short rotation poplar wood: Properties for ethanol fuel and fiber production. Crit Rev Plant Sci 2001, 20:51-69.
• [2]Studer MH, DeMartini JD, Davis MF, Sykes RW, Davison B, Keller M, et al.: Lignin content in natural Populus variants affects sugar release. Proc Natl Acad Sci U S A 2011, 108:6300-6305.
• [3]Lynd LR, Cushman JH, Nichols RJ, Wyman CE: Fuel ethanol from cellulosic biomass. Science 1991, 251:1318-1323.
• [4]Vermerris W, Saballos A, Ejeta G, Mosier NS, Ladisch MR: Molecular breeding to enhance ethanol production from corn and sorghum stover. Crop Sci 2007, 47:S142-S153.
• [5]Fu C, Mielenz J, Xiao X, Ge Y, Hamilton CY, Rodriguez M Jr, et al.: Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass. Proc Natl Acad Sci U S A 2011, 108:3803-3808.
• [6]Novaes E, Osorio L, Drost DR, Miles BL, Boaventura-Novaes CRD, Benedict C, et al.: Quantitative genetic analysis of biomass and wood chemistry of Populus under different nitrogen levels. New Phytol 2009, 182:878-890.
• [7]Yin T, Zhang X, Gunter L, Priya R, Sykes R, Davis M, et al.: Differential detection of genetic loci underlying stem and root lignin content in Populus. PLoS ONE 2010, 5:e14021.
• [8]Rafalski JA: Association genetics in crop improvement. Curr Opin Plant Biol 2010, 13:174-180.
• [9]Wegrzyn JL, Eckert AJ, Choi M, Lee JM, Stanton BJ, Sykes R, et al.: Association genetics of traits controlling lignin and cellulose biosynthesis in black cottonwood (Populus trichocarpa, Salicaceae) secondary xylem. New Phytol 2010, 188:515-532.
• [10]Guerra FP, Wegrzyn JL, Sykes R, Davis MF, Stanton BJ, Neale DB: Association genetics of chemical wood properties in black poplar (Populus nigra). New Phytol 2013, 197:162-176.
• [11]Du Q, Pan W, Tian J, Li B, Zhang D: The UDP-Glucuronate decarboxylase gene family in Populus: Structure, expression and association genetics. PLoS ONE 2013, 8:e60880.
• [12]Porth I, Klápště J, Skyba O, Hannemann J, Mckown AD, Guy R, et al.: Genome-wide association mapping for wood characteristics in Populus identifies an array of candidate single nucleotide polymorphisms. New Phytol 2013, 200:710-726.
• [13]Slavov GT, DiFazio SP, Martin J, Schackwitz W, Muchero W, et al.: Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa. New Phytol 2012, 196:713-725.
• [14]Geraldes A, DiFazio S, Slavov GT, Priya R, Muchero W, et al.: A 34 K SNP genotyping array for Populus trichocarpa: Design, application to the study of natural populations and transferability to other Populus species. Mol Ecol Resour 2013, 13:306-323.
• [15]Porth I, Klápště J, Skyba O, Lai BSK, Geraldes A, Muchero W, et al.: Populus trichocarpa cell wall chemistry and ultrastructure trait variation, genetic control and genetic correlations. New Phytol 2013, 197:777-790.
• [16]Faix O, Meier D, Fortmann : Thermal degradation products of wood: Gas chromatographic separation and mass spectrometric characterization of monomeric lignin derived products. Holz als Rohund Werkstoff 1990, 48:281-285.
• [17]Sun Y-P, Nguyen KL, Wallis AFA: Ring-opened products from reaction of lignin model compounds with UV-assisted peroxide. Holzforschung 1998, 52:61-66.
• [18]Evans RJ, Milne TA: Molecular characterization of the pyrolysis of biomass. 1. Fundamentals. Energy Fuels 1987, 1:123-137.
• [19]Tuskan G, West D, Bradshaw HD, Neale D, Sewell M, et al.: Two high-throughput techniques for determining wood properties as part of a molecular genetics analysis of hybrid poplar and loblolly pine. Appl Biochem Biotechnol 1999, 77:55-65.
• [20]Sykes R, Yung M, Novaes E, Kirst M, Peter G, Davis M: High-throughput screening of plant cell-wall composition using pyrolysis molecular beam mass spectroscopy. In Biofuels: Methods and Protocols. Edited by Mielenz JR. Humana Press, New York; 2009:169-183.
• [21]Ranjan P, Yin T, Zhang X, Kalluri UC, Yang X, Jawdy S, et al.: Bioinformatics-based identification of candidate genes from QTLs associated with cell wall traits in Populus. Bioenergy Res 2010, 3:172-182.
• [22]Plavcová L, Hacke UG, Almeida-Rodriguez AM, Li E, Douglas CJ: Gene expression patterns underlying changes in xylem structure and function in response to increased nitrogen availability in hybrid poplar. Plant Cell Environ 2013, 36:186-199.
• [23]Chen L, Ortiz-Lopez A, Jung A, Bush DR: ANT1, an aromatic and neutral amino acid transporter in Arabidopsis. Plant Physiol 2001, 125:1813-1820.
• [24]Lu S, Li Q, Wei H, Chang M-J, Tunlaya-Anukit S, Kim H, et al: Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa. Proc Natl Acad Sci USA 2013, doi:10.1073/pnas.1308936110.
• [25]Dı́az J, Bernal A, Pomar F, Merino F: Induction of shikimate dehydrogenase and peroxidase in pepper (Capsicum annuum L.) seedlings in response to copper stress and its relation to lignifications. Plant Sci 2001, 161:179-188.
• [26]Kováčik J, Klejdus B: Dynamics of phenolic acids and lignin accumulation in metal-treated Matricaria chamomilla roots. Plant Cell Rep 2008, 27:605-615.
• [27]Downes GM, Ward JV, Turvey ND: Lignin distribution across tracheid cell walls of poorly lignified wood from deformed copper deficient Pinus radiata (D. Don). Wood Sci Technol 1991, 25:7-14.
• [28]Manley HA, Lennon VA: Endoplasmic reticulum membrane-sorting protein of lymphocytes (BAP31) is highly expressed in neurons and discrete endocrine cells. J Histochem Cytochem 2001, 49:1235-1243.
• [29]Kalluri UC, Hurst GB, Lankford PK, Priya R, Pelletier DA: Shotgun proteome profile of Populus developing xylem. Proteomics 2009, 9:4871-4880.
• [30]Atanesyan L, Günther V, Dichtl B, Georgiev O, Schaffner W: Polyglutamine tracts as modulators of transcriptional activation from yeast to mammals. Biol Chem 2012, 393:63-70.
• [31]Chinnadurai G: CtBP family proteins: More than transcriptional corepressors. Bioessays 2002, 25:9-12.
• [32]Kim G-T, Shoda K, Tsuge T, Cho K-H, Uchimiya H, et al.: The ANGUSTIFOLIA gene of Arabidopsis, a plant CtBP gene, regulates leaf-cell expansion, the arrangement of cortical microtubules in leaf cells and expression of a gene involved in cell-wall formation. EMBO J 2002, 21:1267-1279.
• [33]IIegems M, Douet V, Meylan-Bettex M, Uyttewaal M, Brand L, Bowman JL, et al.: Interplay of auxin, KANADI and Class III HD-ZIP transcription factors in vascular tissue formation. Development 2010, 137:975-984.
• [34]Hepler PK: Calcium: A central regulator of plant growth and development. Plant Cell 2005, 17:2142-2155.
• [35]Lautner S, Ehlting B, Windeisen E, Rennenberg H, Matyssek R, et al.: Calcium nutrition has a significant influence on wood formation in poplar. New Phytol 2007, 173:743-752.
• [36]Vanholme B, Cesarino I, Goeminne G, Kim H, Marroni F, Van Acker R, et al.: 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.
• [37]Libby WJ, Cockerham CC: Random non-contiguous plots in interlocking field layouts. Silvae Genet 1980, 29:183-190.
• [38]Van Ooijen JW: MapQTL®6, Software for the mapping of quantitative trait loci in experimental populations of diploid species Kyazma BV. Wageningen, Netherlands; 2009.
• [39]Churchill GA, Doerge RW: Empirical threshold values for quantitative trait mapping. Genetics 1994, 138:963-971.
• [40]Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, et al.: A unified mixed-model method for association mapping accounting for multiple levels of relatedness. Nat Genet 2005, 38:203-208.
• [41]Bonferroni CE: II calcolo delle assicurazioni su gruppi di teste chapter “Studi in Onore del Professore Salvatore ortu Carboni” Rome 13–60. 1935.
• [42]Analytical software: Statistix 8 User’s manual: Analytical software Tallahassee, FL. 2003.