Allelic variation in candidate genes associated with wood properties of cultivated poplars

Cseke Klára; Köbölkuti Zoltán Attila; Benke Attila; Rumi Andrea; Báder Mátyás; Borovics Attila; Németh Róbert

Bulletin of Forestry Science / Volume 10 / Issue 1 / Pages 5-16
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Klára Cseke, Attila Zoltán Köbölkuti, Attila Benke, Andrea Rumi, Mátyás Báder, Attila Borovics & Róbert Németh

Correspondence

Correspondence: Cseke Klára

Postal address: H-9600 Sárvár, Várkerület 30/A

e-mail: cseke.klara[at]erti.naik.hu

Abstract

Poplars represent high economic value. The aim of the present study was to initiate a research methodology that at first identifies candidate genes encoding enzymes with wood property phenotypic traits, towards the aim of developing a genomics-based breeding technology. As a first step, primer pairs were designed on the coding region of 24 candidate genes. 55 primer pairs were tested with 47.27% success rate. In the next phase, eight enzymes were selected for further analysis on 23 genotypes containing seven different poplar species and 11 hybrids. One group of the analyzed enzymes is involved in the lignification process (COMT, CCoAOMT, SAMS), another group (Kt, ptk2, SKOR) holds a key function in K+-dependent xylogenesis, while two more enzymes (endo-1,4-b-xylanase, Araf-ase) have a role in determining microfibril angle. 13 different marker regions were successfully amplified, and 188 sequences were analyzed, altogether resulting in 90 SNPs. The number of polymorphic sites, nucleotide diversity, the number of insertions/deletions, the minimum number of recombination events and the linkage disequilibrium were calculated, while the character of SNPs and conserved DNA regions were identified as well. Potential application fields are discussed along with the presented results.

Keywords: SNP markers, Populus, wood property

References44

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2.	Tribot A., Amer G., Alio M. A., de Baynast H., Delattre C., Pons A., Mathias J.-D., Callois J.-M., Vial C., Michaud P. & Dussap C.-G. 2019: Wood-lignin: Supply, extraction processes and use as bio-based material. European Polymer Journal 112: 228-240. DOI: 10.1016/j.eurpolymj.2019.01.007
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4.	Báder M., Németh R. & Konnerth J. 2019: Micromechanical properties of longitudinally compressed wood. European Journal of Wood and Wood Products 77: 341–351. DOI: 10.1007/s00107-019-01392-0
5.	Bak M. & Németh R. 2012: Changes in swelling properties and moisture uptake rate of oil-heat-treated poplar (Populus x euramericana cv. Pannonia) wood. BioResources 7(4): 5128-5137.
6.	Barnett J.R. & Bonham V.A. 2004: Cellulose microfibril angle in the cell wall of wood fibres. Biological Reviews 79: 461–472.
7.	Bradshaw H. D. & Stettler R. E. 1993: Molecular genetics of growth and development in Populus. In. Triploidy in hybrid poplars. Theoretical and Applied Genetics 86: 301–302.
8.	Brunner A. M., Busov V. B. & Strauss S. H. 2004: Poplar genome sequence : functional genomics in an ecologically dominant plant species. Trends in Plant Science 9(1): 49–56. DOI: 10.1016/j.tplants.2003.11.006
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10.	Davison B. H., Drescher S. R., Tuskan G. A., Davis M. F. & Nghiem N. P. 2006: Variation of S/G Ratio and Lignin Content in a Populus Family Influences the Release of Xylose by Dilute Acid Hydrolysis. Applied Biochemistry and Biotechnology 129-132: 427-435.
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26.	Lampugnani E.R., Khan G.A., Somssich M. & Persson S. 2018: Building a plant cell wall at a glance. Journal of Cell Science 131(2), jcs207373. DOI: 10.1242/jcs.207373
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28.	Li L., Lu S. & Chiang V. 2006: A genomic and molecular view of wood formation. Critical Reviews in Plant Sciences 25(3): 215–233. DOI: 10.1080/07352680600611519
29.	McFarlane H.E., Doring A. & Persson S. 2014: The cell biology of cellulose synthesis. The Annual Review of Plant Biology 65: 69–94.
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31.	Mellerowicz E. J. & Sundberg B. 2008: Wood cell walls: biosynthesis, developmental dynamics and their implications for wood properties. Current Opinion in Plant Biology 11(3): 293–300. DOI: 10.1016/j.pbi.2008.03.003
32.	Mizrachi E., Verbeke L., Christie N. et al. 2017: Network-based integration of systems genetics data reveals pathways associated with lignocellulosic biomass accumulation and processing. Proceedings of the National Academy of Sciences 114. 201620119. DOI: 10.1073/pnas.1620119114
33.	Mutwil M., Debolt S. & Persson S. 2008: Cellulose synthesis: a complex. Current Opinion in Plant Biology 11(3): 252–257. DOI: 10.1016/j.pbi.2008.03.007
34.	Neale D. B. & Kremer A. 2011: Forest tree genomics: growing resources and applications. Nature Reviews Genetics 12: 111-122.
35.	Oakley R. V., Wang Y. S., Ramakrishna W., Harding S. A. & Tsai C. J. 2007: Differential expansion and expression of alfa - and beta-tubulin gene families in Populus. Plant Physiology 145(3): 961–973. DOI: 10.1104/pp.107.107086
36.	Olson M. S., Robertson A. L., Takebayashi N., Silim S., Schroeder W. R. & Tiffin P. 2010: Nucleotide diversity and linkage disequilibrium in balsam poplar (Populus balsamifera). New Phytologist 186: 526–536.
37.	Plomion C., Leprovost G. & Stokes A. 2001: Wood formation in trees. Plant Physiology 127(12): 1513–1523.
38.	Rademacher P., Báder M., Németh R., Rousek R., Paril P., Baar J., Hornicek S., Dejmal A., Domeny J., Kudela J., Kutnar A., Neyses B. & Sandberg D. 2017: European co-operation in wood research – from native wood to engineered materials. Part 2: densification modification in product development. In: Gurau L., Campean M., Ispas M. (eds): Proceedings of the International Conference Wood Science and Engineering in the Third Millenium (ICWSE 2017). Transilvania University, Brasov, Romania, 02-04.11.2017.: 469-478. (ISSN 1843-2689).
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40.	Takab, K., Takeuchi M., Sato T., Ito M. & Fujita M. 2001: lmmunocytochemical localization of enzymes involved in lignification of the cell wall. The Journal of Plant Research 114: 509–515. DOI: 10.1007/PL00014018
41.	Tenney A. E., Wu J. Q., Langton L., Klueh P., Quatrano R. & Brent M. R. 2007: A tale of two templates: Automatically resolving double traces has many applications, including efficient PCR-based elucidation of alternative splices. Genome Research 17(2): 212–218. DOI: 10.1101/gr.5661407
42.	Vander Mijnsbrugge K., Meyermans H., Van Montagu M., Bauw G. & Boerjan W. 2000: Wood formation in poplar: identification, characterization, and seasonal variation of xylem proteins. Planta 210(4): 589–598. DOI: 10.1007/s004250050048
43.	Wright S. I. & Andolfatto P. 2008: The impact of natural selection on the genome: emerging patterns in Drosophila and Arabidopsis. The Annual Review of Ecology, Evolution, and Systematics 39: 193–213. DOI: 10.1146/annurev.ecolsys.39.110707.173342
44.	Zhong R. & Ye Z. H. 2007: Regulation of cell wall biosynthesis. Current Opinion in Plant Biology 10(6): 564–572. DOI: 10.1016/j.pbi.2007.09.001

Ache P., Fromm J. & Hedrich R. 2010: Potassium-dependent wood formation in poplar: Seasonal aspects and environmental limitations. Plant Biology 12(2): 259–267. DOI: 10.1111/j.1438-8677.2009.00282.x

Tribot A., Amer G., Alio M. A., de Baynast H., Delattre C., Pons A., Mathias J.-D., Callois J.-M., Vial C., Michaud P. & Dussap C.-G. 2019: Wood-lignin: Supply, extraction processes and use as bio-based material. European Polymer Journal 112: 228-240. DOI: 10.1016/j.eurpolymj.2019.01.007

Arend M., Stinzing A., Wind C., Langer K., Latz A., Ache P. & Hedrich R. 2005: Polar-localised poplar K+channel capable of controlling electrical properties of wood-forming cells. Planta 223(1): 140–148. DOI: 10.1007/s00425-005-0122-y

Báder M., Németh R. & Konnerth J. 2019: Micromechanical properties of longitudinally compressed wood. European Journal of Wood and Wood Products 77: 341–351. DOI: 10.1007/s00107-019-01392-0

Bak M. & Németh R. 2012: Changes in swelling properties and moisture uptake rate of oil-heat-treated poplar (Populus x euramericana cv. Pannonia) wood. BioResources 7(4): 5128-5137.

Barnett J.R. & Bonham V.A. 2004: Cellulose microfibril angle in the cell wall of wood fibres. Biological Reviews 79: 461–472.

Bradshaw H. D. & Stettler R. E. 1993: Molecular genetics of growth and development in Populus. In. Triploidy in hybrid poplars. Theoretical and Applied Genetics 86: 301–302.

Brunner A. M., Busov V. B. & Strauss S. H. 2004: Poplar genome sequence : functional genomics in an ecologically dominant plant species. Trends in Plant Science 9(1): 49–56. DOI: 10.1016/j.tplants.2003.11.006

Christensen J. H., Baucher M., O’Connell A., Van Montagu M. & Boerjan W. 2000: Control of lignin biosynthesis. Molecular biology of woody plants. Dordrecht, Springer: 227–228.

Davison B. H., Drescher S. R., Tuskan G. A., Davis M. F. & Nghiem N. P. 2006: Variation of S/G Ratio and Lignin Content in a Populus Family Influences the Release of Xylose by Dilute Acid Hydrolysis. Applied Biochemistry and Biotechnology 129-132: 427-435.

Donaldson L. 2008: Microfibril angle: Measurement, variation and relationships - A review. International Association of Wood Anatomists Journal 29: 345–386.

Dumolin S., Demesure B. & Petit R. J. 1995: Inheritance of chloroplast and mitochondrial genomes in pedunculate oak investigated with an efficient PCR method. Theoretical and Applied Genetics 91(8): 1253–1256. DOI: 10.1007/BF00220937

Evans R. & Ilic J. 2001: Rapid prediction of wood stiffness from microfibril angle and density. Forest Products Journal 51: 53–57.

Fromm J. 2010: Wood formation of trees in relation to potassium and calcium nutrition. Tree Physiology 30(9): 1140–1147. DOI: 10.1093/treephys/tpq024

Geisler-Lee J., Geisler M., Coutinho P. M., Segerman B., Nishikubo N., Takahashi J. & Sundberg B. 2006: Poplar carbohydrate-active enzymes. Gene identification and expression analyses. Plant Physiology 140(3): 946–962. DOI: 10.1104/pp.105.072652

Gencsi L. & Vancsura R. 1992: Dendrológia – Erdészeti Növénytan II. Mezőgazda Kiadó, Budapest: 29, 330.

Glasser W.G. 2019: About Making Lignin Great Again – Some Lessons From the Past. Frontiers in Chemistry 7: 565. DOI: 10.3389/fchem.2019.00565

González-Martínez S. C., Krutovsky K. V. & Neale D. B. 2006: Forest-tree population genomics and adaptive evolution. New Phytologist 170: 227-238.

Hall T. A. 1999: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41 (41): 95–98.

Halpin C. 2004: Re-designing lignin for industry and agriculture. Biotechnology and Genetic Engineering 21(1): 229–248. DOI: 10.1080/02648725.2004.10648057

Henry I. M., Zinkgraf M. S., Groover A. T. & Comai L. 2015: A system for dosage-based functional genomics in poplar. The Plant Cell 27(9): 2370–2383. DOI: 10.1105/tpc.15.00349

Horváth N., Bak M. & Németh R. 2012: Modification of poplar wood by different heat treatments. Poster presentation, 7. Thermowood Workshop, Drezda, 2012.04.26-27.

Isabel N., Lamothe M. & Thompson S. L. 2013: A second-generation diagnostic single nucleotide polymorphism (SNP)-based assay, optimized to distinguish among eight poplar (Populus L.) species and their early hybrids. Tree Genetics and Genomes 9(2): 621–626. DOI: 10.1007/s11295-012-0569-5

Komán Sz. 2012: Nemesnyár-fajták korszerű ipari és energetikai hasznosítását befolyásoló faanatómiai és fizikai jellemzők. Doktori értekezés, Nyugat-Magyarországi Egyetem, Sopron, 85 p.

Köbölkuti Z., Cseke K., Benke A., Báder M., Borovics A. & Németh R. 2019: Allelic variation in candidate genes associated with wood properties of cultivated poplars (Populus), Biologia Futura 70(4): 286-294.

Lampugnani E.R., Khan G.A., Somssich M. & Persson S. 2018: Building a plant cell wall at a glance. Journal of Cell Science 131(2), jcs207373. DOI: 10.1242/jcs.207373

Langer K., Ache P., Geiger D. et al. 2002: Poplar potassium transporters capable of controlling K+ homeostasis and K+-dependent xylogenesis. The Plant Journal 32(6): 997-1009. DOI: 10.1046/j.1365-313x.2002.01487.x

Li L., Lu S. & Chiang V. 2006: A genomic and molecular view of wood formation. Critical Reviews in Plant Sciences 25(3): 215–233. DOI: 10.1080/07352680600611519

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

Meents M.J., Watanabe Y. & Samuels A.L. 2018: The cell biology of secondary cell wall biosynthesis. Annals of Botany 121: 1107–1125.

Mellerowicz E. J. & Sundberg B. 2008: Wood cell walls: biosynthesis, developmental dynamics and their implications for wood properties. Current Opinion in Plant Biology 11(3): 293–300. DOI: 10.1016/j.pbi.2008.03.003

Mizrachi E., Verbeke L., Christie N. et al. 2017: Network-based integration of systems genetics data reveals pathways associated with lignocellulosic biomass accumulation and processing. Proceedings of the National Academy of Sciences 114. 201620119. DOI: 10.1073/pnas.1620119114

Mutwil M., Debolt S. & Persson S. 2008: Cellulose synthesis: a complex. Current Opinion in Plant Biology 11(3): 252–257. DOI: 10.1016/j.pbi.2008.03.007

Neale D. B. & Kremer A. 2011: Forest tree genomics: growing resources and applications. Nature Reviews Genetics 12: 111-122.

Oakley R. V., Wang Y. S., Ramakrishna W., Harding S. A. & Tsai C. J. 2007: Differential expansion and expression of alfa - and beta-tubulin gene families in Populus. Plant Physiology 145(3): 961–973. DOI: 10.1104/pp.107.107086

Olson M. S., Robertson A. L., Takebayashi N., Silim S., Schroeder W. R. & Tiffin P. 2010: Nucleotide diversity and linkage disequilibrium in balsam poplar (Populus balsamifera). New Phytologist 186: 526–536.

Plomion C., Leprovost G. & Stokes A. 2001: Wood formation in trees. Plant Physiology 127(12): 1513–1523.

Rademacher P., Báder M., Németh R., Rousek R., Paril P., Baar J., Hornicek S., Dejmal A., Domeny J., Kudela J., Kutnar A., Neyses B. & Sandberg D. 2017: European co-operation in wood research – from native wood to engineered materials. Part 2: densification modification in product development. In: Gurau L., Campean M., Ispas M. (eds): Proceedings of the International Conference Wood Science and Engineering in the Third Millenium (ICWSE 2017). Transilvania University, Brasov, Romania, 02-04.11.2017.: 469-478. (ISSN 1843-2689).

Song J., Chen C., Zhu S. et al. 2018: Processing bulk natural wood into a high-performance structural material. Nature 554: 224–228. DOI: 10.1038/nature25476

Takab, K., Takeuchi M., Sato T., Ito M. & Fujita M. 2001: lmmunocytochemical localization of enzymes involved in lignification of the cell wall. The Journal of Plant Research 114: 509–515. DOI: 10.1007/PL00014018

Tenney A. E., Wu J. Q., Langton L., Klueh P., Quatrano R. & Brent M. R. 2007: A tale of two templates: Automatically resolving double traces has many applications, including efficient PCR-based elucidation of alternative splices. Genome Research 17(2): 212–218. DOI: 10.1101/gr.5661407

Vander Mijnsbrugge K., Meyermans H., Van Montagu M., Bauw G. & Boerjan W. 2000: Wood formation in poplar: identification, characterization, and seasonal variation of xylem proteins. Planta 210(4): 589–598. DOI: 10.1007/s004250050048

Wright S. I. & Andolfatto P. 2008: The impact of natural selection on the genome: emerging patterns in Drosophila and Arabidopsis. The Annual Review of Ecology, Evolution, and Systematics 39: 193–213. DOI: 10.1146/annurev.ecolsys.39.110707.173342

Zhong R. & Ye Z. H. 2007: Regulation of cell wall biosynthesis. Current Opinion in Plant Biology 10(6): 564–572. DOI: 10.1016/j.pbi.2007.09.001

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Cseke, K., Köbölkuti, Z. A., Benke, A., Rumi, A., Báder, M., Borovics, A. & Németh, R. (2020): Allelic variation in candidate genes associated with wood properties of cultivated poplars. Bulletin of Forestry Science, 10(1): 5-16. (in Hungarian) DOI: 10.17164/EK.2020.001

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Volume 10, Issue 1
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DOI: 10.17164/EK.2020.001

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Cseke, K., Jobb, Sz., Koltay, A. & Borovics, A. (2014): The genetic pattern of oak decline. Bulletin of Forestry Science, 4(2): 135-147.

Báder, M. & Komán, H. (2022): Determining the juvenile age of different wood species using a mathematical model. Bulletin of Forestry Science, 12(2): 113-119.

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