Systems genetic analysis of lignin biosynthesis in Populus tremula.

GWAS HD‐Zip III Populus aspen eQTL lignin biosynthesis wood formation

Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
28 Jul 2024
Historique:
received: 28 01 2024
accepted: 02 07 2024
medline: 29 7 2024
pubmed: 29 7 2024
entrez: 29 7 2024
Statut: aheadofprint

Résumé

The genetic control underlying natural variation in lignin content and composition in trees is not fully understood. We performed a systems genetic analysis to uncover the genetic regulation of lignin biosynthesis in a natural 'SwAsp' population of aspen (Populus tremula) trees. We analyzed gene expression by RNA sequencing (RNA-seq) in differentiating xylem tissues, and lignin content and composition using Pyrolysis-GC-MS in mature wood of 268 trees from 99 genotypes. Abundant variation was observed for lignin content and composition, and genome-wide association study identified proteins in the pentose phosphate pathway and arabinogalactan protein glycosylation among the top-ranked genes that are associated with these traits. Variation in gene expression and the associated genetic polymorphism was revealed through the identification of 312 705 local and 292 003 distant expression quantitative trait loci (eQTL). A co-expression network analysis suggested modularization of lignin biosynthesis and novel functions for the lignin-biosynthetic CINNAMYL ALCOHOL DEHYDROGENASE 2 and CAFFEOYL-CoA O-METHYLTRANSFERASE 3. PHENYLALANINE AMMONIA LYASE 3 was co-expressed with HOMEOBOX PROTEIN 5 (HB5), and the role of HB5 in stimulating lignification was demonstrated in transgenic trees. The systems genetic approach allowed linking natural variation in lignin biosynthesis to trees´ responses to external cues such as mechanical stimulus and nutrient availability.

Identifiants

pubmed: 39072753
doi: 10.1111/nph.19993
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Fundação para a Ciência e Tecnologia
ID : CEEC/IND/00175/2017
Organisme : Fundação para a Ciência e Tecnologia
ID : UIDB/04551/2020
Organisme : Fundação para a Ciência e Tecnologia
ID : UIDP/04551/2020
Organisme : Knut och Alice Wallenbergs Stiftelse
ID : 2016.0341
Organisme : Knut och Alice Wallenbergs Stiftelse
ID : 2016.0352
Organisme : VINNOVA
ID : 2016-00504
Organisme : Svenska Forskningsrådet Formas
ID : 2018-01381
Organisme : Svenska Forskningsrådet Formas
ID : 2018-01611

Informations de copyright

© 2024 The Author(s). New Phytologist © 2024 New Phytologist Foundation.

Références

Akyol T. 2019. rvenn: set operations for many sets. R package v.1.1.0.
Anderson EM, Stone ML, Katahira R, Reed M, Muchero W, Ramirez KJ, Beckham GT, Román‐Leshkov Y. 2019. Differences in S/G ratio in natural poplar variants do not predict catalytic depolymerization monomer yields. Nature Communications 10: 2033.
Bailey TL, Johnson J, Grant CE, Noble WS. 2015. The MEME suite. Nucleic Acids Research 43: W39–W49.
Balmant KM, Noble JD, Alves FC, Dervinis C, Conde D, Schmidt HW, Vazquez AI, Barbazuk WB, de Los CG, Resende MF et al. 2020. Xylem systems genetics analysis reveals a key regulator of lignin biosynthesis in Populus deltoides. Genome Research 30: 1131–1143.
Barakate A, Stephens J, Goldie A, Hunter WN, Marshall D, Hancock RD, Lapierre C, Morreel K, Boerjan W, Halpin C. 2011. Syringyl lignin is unaltered by severe sinapyl alcohol dehydrogenase suppression in tobacco. Plant Cell 23: 4492–4506.
Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed‐effects models using lme4. Journal of Statistical Software 67: 1–48.
Boerjan W, Ralph J, Baucher M. 2003. Lignin biosynthesis. Annual Review of Plant Biology 54: 519–546.
Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114–2120.
Bryant N, Zhang J, Feng K, Shu M, Ployet R, Chen J‐G, Muchero W, Yoo CG, Tschaplinski TJ, Pu Y et al. 2023. Novel candidate genes for lignin structure identified through genome‐wide association study of naturally varying Populus trichocarpa. Frontiers in Plant Science 14: 1153113.
Buels R, Yao E, Diesh CM, Hayes RD, Munoz‐Torres M, Helt G, Goodstein DM, Elsik CG, Lewis SE, Stein L et al. 2016. JBrowse: a dynamic web platform for genome visualization and analysis. Genome Biology 17: 1–12.
Chanoca A, De Vries L, Boerjan W. 2019. Lignin engineering in forest trees. Frontiers in Plant Science 10: 912.
Chantreau M, Tuominen H. 2022. Spatio‐temporal regulation of lignification. Advances in Botanical Research 104: 271–316.
Chao N, Liu S‐X, Liu B‐M, Li N, Jiang X‐N, Gai Y. 2014. Molecular cloning and functional analysis of nine cinnamyl alcohol dehydrogenase family members in Populus tomentosa. Planta 240: 1097–1112.
Chen C, Meyermans H, Burggraeve B, De Rycke RM, Inoue K, De Vleesschauwer V, Steenackers M, Van Montagu MC, Engler GJ, Boerjan WA. 2000. Cell‐specific and conditional expression of caffeoyl‐coenzyme A‐3‐ O‐methyltransferase in poplar. Plant Physiology 123: 853–867.
Chomczynski P, Sacchi N. 2006. The single‐step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction: twenty‐something years on. Nature Protocols 1: 581–585.
Cooke J, Brown K, Wu R, Davis J. 2003. Gene expression associated with N‐induced shifts in resource allocation in poplar. Plant, Cell & Environment 26: 757–770.
Coscia M, Neffke FMH. 2017. Network backboning with noisy data. 2017 IEEE 33rd International Conference on Data Engineering (ICDE): pp. 425–436.
Crivellaro A, Piermattei A, Dolezal J, Dupree P, Büntgen U. 2022. Biogeographic implication of temperature‐induced plant cell wall lignification. Communications Biology 5: 767.
De Meester B, Vanholme R, Mota T, Boerjan W. 2022. Lignin engineering in forest trees: from gene discovery to field trials. Plant Communications 3: 100465.
Delhomme N, Mähler N, Schiffthaler B, Sundell D, Mannapperuma C, Hvidsten TR, Street NR. 2014. Guidelines for RNA‐Seq data analysis. Epigenesys Protocol 67: 1–24.
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. Star: ultrafast universal RNA‐seq aligner. Bioinformatics 29: 15–21.
Dohm M. 2002. Repeatability estimates do not always set an upper limit to heritability. Functional Ecology 16: 273–280.
Du J, Miura E, Robischon M, Martinez C, Groover A. 2011. The Populus Class III HD ZIP transcription factor POPCORONA affects cell differentiation during secondary growth of woody stems. PLoS ONE 6: e17458.
Edgar RE. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792–1797.
Escamez S, Robinson KM, Luomaranta M, Gandla ML, Mähler N, Yassin Z, Grahn T, Scheepers G, Stener L‐G, Jansson S et al. 2023. Genetic markers and tree properties predicting wood biorefining potential in aspen (Populus tremula) bioenergy feedstock. Biotechnology for Biofuels and Bioproducts 16: 1–16.
Ewels P, Magnusson M, Lundin S, Käller M. 2016. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics 32: 3047–3048.
Fahrenkrog AM, Neves LG, Resende MF Jr, Vazquez AI, de Los Campos G, Dervinis C, Sykes R, Davis M, Davenport R, Barbazuk WB et al. 2017. Genome‐wide association study reveals putative regulators of bioenergy traits in Populus deltoides. New Phytologist 213: 799–811.
Faith JJ, Hayete B, Thaden JT, Mogno I, Wierzbowski J, Cottarel G, Kasif S, Collins JJ, Gardner TS. 2007. Large‐scale mapping and validation of Escherichia coli transcriptional regulation from a compendium of expression profiles. PLoS Biology 5: e8.
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 Molecular Biology 27: 651–667.
Fornes O, Castro‐Mondragon JA, Khan A, Van der Lee R, Zhang X, Richmond PA, Modi BP, Correard S, Gheorghe M, Baranašić D et al. 2020. JASPAR 2020: update of the open‐access database of transcription factor binding profiles. Nucleic Acids Research 48: D87–D92.
Fracheboud Y, Luquez V, Bjorken L, Sjodin A, Tuominen H, Jansson S. 2009. The control of autumn senescence in European aspen. Plant Physiology 149: 1982–1991.
Furches A, Kainer D, Weighill D, Large A, Jones P, Walker AM, Romero J, Gazolla JGFM, Joubert W, Shah M et al. 2019. Finding new cell wall regulatory genes in Populus trichocarpa using multiple lines of evidence. Frontiers in Plant Science 10: 1249.
Geng P, Zhang S, Liu J, Zhao C, Wu J, Cao Y, Fu C, Han X, He H, Zhao Q. 2020. MYB20, MYB42, MYB43, and MYB85 regulate phenylalanine and lignin biosynthesis during secondary cell wall formation. Plant Physiology 182: 1272–1283.
Gerber L, Eliasson M, Trygg J, Moritz T, Sundberg B. 2012. Multivariate curve resolution provides a high‐throughput data processing pipeline for pyrolysis‐gas chromatography/mass spectrometry. Journal of Analytical and Applied Pyrolysis 95: 95–100.
Geshi N, Johansen JN, Dilokpimol A, Rolland A, Belcram K, Verger S, Kotake T, Tsumuraya Y, Kaneko S, Tryfona T et al. 2013. A galactosyltransferase acting on arabinogalactan protein glycans is essential for embryo development in Arabidopsis. The Plant Journal 76: 128–137.
Grant CE, Bailey TL, Noble WS. 2011. Fimo: scanning for occurrences of a given motif. Bioinformatics 27: 1017–1018.
Guerra FP, Wegrzyn JL, Sykes R, Davis MF, Stanton BJ, Neale DB. 2013. Association genetics of chemical wood properties in black poplar (Populus nigra). New Phytologist 197: 162–176.
Guo S, Jiang Q, Chen L, Guo D. 2016. Gene regulatory network inference using PLS‐based methods. BMC Bioinformatics 17: 1–10.
Haury A‐C, Mordelet F, Vera‐Licona P, Vert J‐P. 2012. Tigress: trustful inference of gene regulation using stability selection. BMC Systems Biology 6: 1–17.
Howles PA, Birch RJ, Collings DA, Gebbie LK, Hurley UA, Hocart CH, Arioli T, Williamson RE. 2006. A mutation in an Arabidopsis ribose 5‐phosphate isomerase reduces cellulose synthesis and is rescued by exogenous uridine. The Plant Journal 48: 606–618.
Huynh‐Thu VA, Irrthum A, Wehenkel L, Geurts P. 2010. Inferring regulatory networks from expression data using tree‐based methods. PLoS ONE 5: e12776.
Jones DT, Taylor WR, Thornton JM. 1992. The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8: 275–282.
Kim J, Jung J‐H, Reyes JL, Kim Y‐S, Kim S‐Y, Chung K‐S, Kim JA, Lee M, Lee Y, Kim VN et al. 2005. microRNA‐directed cleavage of ATHB15 mRNA regulates vascular development in Arabidopsis inflorescence stems. The Plant Journal 42: 84–94.
Kolde R. 2015. Package ‘pheatmap’. R package 1.
Kopylova E, Noé L, Touzet H. 2012. SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28: 3211–3217.
Kruijer W, Boer MP, Malosetti M, Flood PJ, Engel B, Kooke R, Keurentjes JJ, van Eeuwijk FA. 2015. Marker‐based estimation of heritability in immortal populations. Genetics 199: 379–398.
Kumar V, Hainaut M, Delhomme N, Mannapperuma C, Immerzeel P, Street NR, Henrissat B, Mellerowicz EJ. 2019. Poplar carbohydrate‐active enzymes: whole‐genome annotation and functional analyses based on RNA expression data. The Plant Journal 99: 589–609.
Langfelder P, Horvath S. 2008. wgcna: an R package for weighted correlation network analysis. BMC Bioinformatics 9: 1–13.
Li L, Cheng XF, Leshkevich J, Umezawa T, Harding SA, Chiang VL. 2001. The last step of syringyl monolignol biosynthesis in angiosperms is regulated by a novel gene encoding sinapyl alcohol dehydrogenase. Plant Cell 13: 1567–1586.
Li P, Xiao L, Du Q, Quan M, Song Y, He Y, Huang W, Xie J, Lv C, Wang D. 2023. Genomic insights into selection for heterozygous alleles and woody traits in Populus tomentosa. Plant Biotechnology Journal 21: 2002–2018.
Lihavainen J, Šimura J, Bag P, Fataftah N, Robinson KM, Delhomme N, Novák O, Ljung K, Jansson S. 2023. Salicylic acid metabolism and signalling coordinate senescence initiation in aspen in nature. Nature Communications 14: 4288.
Lin S, Miao Y, Huang H, Zhang Y, Huang L, Cao J. 2022. Arabinogalactan proteins: focus on the role in cellulose synthesis and deposition during plant cell wall biogenesis. International Journal of Molecular Sciences 23: 6578.
Liu K‐H, Liu M, Lin Z, Wang Z‐F, Chen B, Liu C, Guo A, Konishi M, Yanagisawa S, Wagner G et al. 2022. NIN‐like protein 7 transcription factor is a plant nitrate sensor. Science 377: 1419–1425.
Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real‐time quantitative PCR and the 2(−ΔΔC(T)) method. Methods 25: 402–408.
Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA‐seq data with DESeq2. Genome Biology 15: 1–21.
Luquez V, Hall D, Albrectsen BR, Karlsson J, Ingvarsson P, Jansson S. 2008. Natural phenological variation in aspen (Populus tremula): the SwAsp collection. Tree Genetics & Genomes 4: 279–292.
Mähler N, Schiffthaler B, Robinson KM, Terebieniec BK, Vučak M, Mannapperuma C, Bailey ME, Jansson S, Hvidsten TR, Street NR. 2020. Leaf shape in Populus tremula is a complex, omnigenic trait. Ecology and Evolution 10: 11922–11940.
Mähler N, Wang J, Terebieniec BK, Ingvarsson PK, Street NR, Hvidsten TR. 2017. Gene co‐expression network connectivity is an important determinant of selective constraint. PLoS Genetics 13: e1006402.
Margolin AA, Nemenman I, Basso K, Wiggins C, Stolovitzky G, Favera RD, Califano A. 2006. ARACNE: an algorithm for the reconstruction of gene regulatory networks in a mammalian cellular context. BMC Bioinformatics 7: S7.
Meng X, Pu Y, Yoo CG, Li M, Bali G, Park DY, Gjersing E, Davis MF, Muchero W, Tuskan GA. 2017. An in‐depth understanding of biomass recalcitrance using natural poplar variants as the feedstock. ChemSusChem 10: 139–150.
Muchero W, Guo J, DiFazio SP, Chen J‐G, Ranjan P, Slavov GT, Gunter LE, Jawdy S, Bryan AC, Sykes R et al. 2015. High‐resolution genetic mapping of allelic variants associated with cell wall chemistry in Populus. BMC Genomics 16: 1–14.
Nica AC, Dermitzakis ET. 2013. Expression quantitative trait loci: present and future. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 368: 20120362.
Nilsson O, Aldén T, Sitbon F, Anthony Little C, Chalupa V, Sandberg G, Olsson O. 1992. Spatial pattern of cauliflower mosaic virus 35S promoter‐luciferase expression in transgenic hybrid aspen trees monitored by enzymatic assay and non‐destructive imaging. Transgenic Research 1: 209–220.
Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. 2017. Salmon provides fast and bias‐aware quantification of transcript expression. Nature Methods 14: 417–419.
Peterson RA, Cavanaugh JE. 2019. Ordered quantile normalization: a semiparametric transformation built for the cross‐validation era. Journal of Applied Statistics 47: 2312–2327.
Pilate G, Chabbert B, Cathala B, Yoshinaga A, Leplé J‐C, Laurans F, Lapierre C, Ruel K. 2004. Lignification and tension wood. Comptes Rendus Biologies 327: 889–901.
Pitre FE, Pollet B, Lafarguette F, Cooke JE, MacKay JJ, Lapierre C. 2007. Effects of increased nitrogen supply on the lignification of poplar wood. Journal of Agricultural and Food Chemistry 55: 10306–10314.
Porth I, Klapšte J, Skyba O, Hannemann J, McKown AD, Guy RD, DiFazio SP, Muchero W, Ranjan P, Tuskan GA. 2013. Genome‐wide association mapping for wood characteristics in Populus identifies an array of candidate single nucleotide polymorphisms. New Phytologist 200: 710–726.
Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841–842.
Ragauskas AJ, Beckham GT, Biddy MJ, Chandra R, Chen F, Davis MF, Davison BH, Dixon RA, Gilna P, Keller M et al. 2014. Lignin valorization: improving lignin processing in the biorefinery. Science 344: 1246843.
Rauluseviciute I, Riudavets‐Puig R, Blanc‐Mathieu R, Castro‐Mondragon JA, Ferenc K, Kumar V, Lemma RB, Lucas J, Chèneby J, Baranasic D et al. 2024. JASPAR 2024: 20th anniversary of the open‐access database of transcription factor binding profiles. Nucleic Acids Research 52: D174–D182.
Renström A, Choudhary S, Gandla ML, Jönsson LJ, Hedenström M, Jämtgård S, Tuominen H. 2024. The effect of nitrogen source and levels on hybrid aspen tree physiology and wood formation. Physiologia Plantarum 176: e14219.
Robinson KM, Schiffthaler B, Liu H, Westman SM, Rendón‐Anaya M, Ahlgren Kalman T, Kumar V, Canovi C, Bernhardsson C, Delhomme N et al. 2024. An improved chromosome‐scale genome assembly and population genetics resource for Populus tremula. bioRxiv. doi: 10.1101/805614.
Rossi S, Anfodillo T, Menardi R. 2006. Trephor: a new tool for sampling microcores from tree stems. IAWA Journal 27: 89–97.
Rosvall M, Bergstrom CT. 2008. Maps of random walks on complex networks reveal community structure. Proceedings of the National Academy of Sciences, USA 105: 1118–1123.
Ruyssinck J, Huynh‐Thu VA, Geurts P, Dhaene T, Demeester P, Saeys Y. 2014. Nimefi: gene regulatory network inference using multiple ensemble feature importance algorithms. PLoS ONE 9: e92709.
Schiffthaler B, van Zalen E, Serrano AR, Street NR, Delhomme N. 2023. Seiðr: efficient calculation of robust ensemble gene networks. Heliyon 31: e16811.
Shabalin AA. 2012. Matrix eQTL: ultra fast eQTL analysis via large matrix operations. Bioinformatics 28: 1353–1358.
Shi R, Sun Y‐H, Li Q, Heber S, Sederoff R, Chiang VL. 2010. Towards a systems approach for lignin biosynthesis in Populus trichocarpa: transcript abundance and specificity of the monolignol biosynthetic genes. Plant and Cell Physiology 51: 144–163.
Song L, Langfelder P, Horvath S. 2012. Comparison of co‐expression measures: mutual information, correlation, and model based indices. BMC Bioinformatics 13: 1–21.
Stincone A, Prigione A, Cramer T, Wamelink MM, Campbell K, Cheung E, Olin‐Sandoval V, Grüning NM, Krüger A, Tauqeer Alam M et al. 2015. The return of metabolism: biochemistry and physiology of the pentose phosphate pathway. Biological Reviews 90: 927–963.
Storey J, Bass A, Dabney A, Robinson D. 2020. qvalue: Q-value estimation for false discovery rate control. R package v.2.22.0. [WWW document] URL http://github.com/jdstorey/qvalue [accessed 10 October 2020].
Storey JD, Tibshirani R. 2003. Statistical significance for genomewide studies. Proceedings of the National Academy of Sciences, USA 100: 9440–9445.
Stuart JM, Segal E, Koller D, Kim SK. 2003. A gene‐coexpression network for global discovery of conserved genetic modules. Science 302: 249–255.
Studer MH, DeMartini JD, Davis MF, Sykes RW, Davison B, Keller M, Tuskan GA, Wyman CE. 2011. Lignin content in natural Populus variants affects sugar release. Proceedings of the National Academy of Sciences, USA 108: 6300–6305.
Sulis DB, Jiang X, Yang C, Marques BM, Matthews ML, Miller Z, Lan K, Cofre‐Vega C, Liu B, Sun R. 2023. Multiplex CRISPR editing of wood for sustainable fiber production. Science 381: 216–221.
Sundell D, Mannapperuma C, Netotea S, Delhomme N, Lin Y‐C, Sjödin A, Van de Peer Y, Jansson S, Hvidsten TR, Street NR. 2015. The plant genome integrative explorer resource: PlantGenIE.org. New Phytologist 208: 1149–1156.
Sundell D, Street NR, Kumar M, Mellerowicz EJ, Kucukoglu M, Johnsson C, Kumar V, Mannapperuma C, Delhomme N, Nilsson O et al. 2017. AspWood: high‐spatial‐resolution transcriptome profiles reveal uncharacterized modularity of wood formation in Populus tremula. Plant Cell 29: 1585–1604.
Turner SD. 2014. qqman: an R package for visualizing GWAS results using QQ and Manhattan plots. bioRxiv. doi: 10.1101/005165.
Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG. 2012. Primer3—new capabilities and interfaces. Nucleic Acids Research 40: e115.
Vanholme R, De Meester B, Ralph J, Boerjan W. 2019. Lignin biosynthesis and its integration into metabolism. Current Opinion in Biotechnology 56: 230–239.
Vanholme R, Morreel K, Darrah C, Oyarce P, Grabber JH, Ralph J, Boerjan W. 2012. Metabolic engineering of novel lignin in biomass crops. New Phytologist 196: 978–1000.
Wang J, Ding J, Tan B, Robinson KM, Michelson IH, Johansson A, Nystedt B, Scofield DG, Nilsson O, Jansson S et al. 2018. A major locus controls local adaptation and adaptive life history variation in a perennial plant. Genome Biology 19: 1–17.
Wang JP, Naik PP, Chen H‐C, Shi R, Lin C‐Y, Liu J, Shuford CM, Li Q, Sun Y‐H, Tunlaya‐Anukit S. 2014. Complete proteomic‐based enzyme reaction and inhibition kinetics reveal how monolignol biosynthetic enzyme families affect metabolic flux and lignin in Populus trichocarpa. Plant Cell 26: 894–914.
Wei H, Song Z, Xie Y, Cheng H, Yan H, Sun F, Liu H, Shen J, Li L, He X. 2023. High temperature inhibits vascular development via the PIF4‐miR166‐HB15 module in Arabidopsis. Current Biology 33: 3203–3214.
Wickham H. 2011. ggplot2. Wiley Interdisciplinary Reviews: Computational Statistics 3: 180–185.
Xie M, Muchero W, Bryan AC, Yee K, Guo H‐B, Zhang J, Tschaplinski TJ, Singan VR, Lindquist E, Payyavula RS et al. 2018. A 5‐enolpyruvylshikimate 3‐phosphate synthase functions as a transcriptional repressor in Populus. Plant Cell 30: 1645–1660.
Xiong Y, DeFraia C, Williams D, Zhang X, Mou Z. 2009. Deficiency in a cytosolic ribose‐5‐phosphate isomerase causes chloroplast dysfunction, late flowering and premature cell death in Arabidopsis. Physiologia Plantarum 137: 249–263.
Yao T, Zhang J, Yates TB, Shrestha HK, Engle NL, Ployet R, John C, Feng K, Bewg WP, Chen MS et al. 2023. Expression quantitative trait loci mapping identified PtrXB38 as a key hub gene in adventitious root development in Populus. New Phytologist 239: 2248–2264.
Yoo CG, Yang Y, Pu Y, Meng X, Muchero W, Yee KL, Thompson OA, Rodriguez M, Bali G, Engle NL et al. 2017. Insights of biomass recalcitrance in natural Populus trichocarpa variants for biomass conversion. Green Chemistry 19: 5467–5478.
Zang L, Zheng T, Chu Y, Ding C, Zhang W, Huang Q, Su X. 2015. Genome‐wide analysis of the fasciclin‐like Arabinogalactan protein gene family reveals differential expression patterns, localization, and salt stress response in Populus. Frontiers in Plant Science 6: 1140.
Zhang J, Tuskan GA, Tschaplinski TJ, Muchero W, Chen JG. 2020. Transcriptional and post‐transcriptional regulation of lignin biosynthesis pathway genes in Populus. Frontiers in Plant Science 11: 652.
Zhang J, Yang Y, Zheng K, Xie M, Feng K, Jawdy SS, Gunter LE, Ranjan P, Singan VR, Engle N et al. 2018. Genome‐wide association studies and expression‐based quantitative trait loci analyses reveal roles of HCT 2 in caffeoylquinic acid biosynthesis and its regulation by defense‐responsive transcription factors in Populus. New Phytologist 220: 502–516.
Zhang L, Lu D, Ge X, Du J, Wen S, Xiang X, Du C, Zhou X, Hu J. 2023. Insight into growth and wood properties based on QTL and eQTL mapping in Populus deltoides ‘Danhong’× Populus simonii ‘Tongliao1’. Industrial Crops and Products 199: 116731.
Zhang X, Liu K, Liu Z‐P, Duval B, Richer J‐M, Zhao X‐M, Hao J‐K, Chen L. 2013. NARROMI: a noise and redundancy reduction technique improves accuracy of gene regulatory network inference. Bioinformatics 29: 106–113.
Zhao H, Qu C, Zuo Z, Cao L, Zhang S, Xu X, Xu Z, Liu G. 2022. Genome identification and expression profiles in response to nitrogen treatment analysis of the class I CCoAOMT gene family in Populus. Biochemical Genetics 60: 656–675.
Zhong R, Allen JD, Xiao G, Xie Y. 2014. Ensemble‐based network aggregation improves the accuracy of gene network reconstruction. PLoS ONE 9: e106319.
Zhong R, Lee C, Zhou J, McCarthy RL, Ye Z‐H. 2008. A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20: 2763–2782.
Zhou X, Stephens M. 2012. Genome‐wide efficient mixed‐model analysis for association studies. Nature Genetics 44: 821–824.

Auteurs

Mikko Luomaranta (M)

Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, 90187, Umeå, Sweden.

Carolin Grones (C)

Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, 90187, Umeå, Sweden.

Shruti Choudhary (S)

Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, 90183, Umeå, Sweden.

Ana Milhinhos (A)

Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, 90187, Umeå, Sweden.

Teitur Ahlgren Kalman (TA)

Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, 90187, Umeå, Sweden.

Ove Nilsson (O)

Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, 90183, Umeå, Sweden.

Kathryn M Robinson (KM)

Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, 90187, Umeå, Sweden.

Nathaniel R Street (NR)

Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, 90187, Umeå, Sweden.
SciLifeLab, Umeå University, 90187, Umeå, Sweden.

Hannele Tuominen (H)

Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, 90183, Umeå, Sweden.

Classifications MeSH