Cannabis sativa L. is an annual herbaceous crop grown for the production of long extraxylary fibers, the bast fibers, rich in cellulose and used both in the textile and biocomposite sectors. Despite being herbaceous, hemp undergoes secondary growth and this is well exemplified by the hypocotyl. The hypocotyl was already shown to be a suitable model to study secondary growth in other herbaceous species, namely Arabidopsis thaliana and it shows an important practical advantage, i.e., elongation and radial thickening are temporally separated. This study focuses on the mechanisms marking the transition from primary to secondary growth in the hemp hypocotyl by analysing the suite of events accompanying vascular tissue and bast fiber development. Transcriptomics, imaging and quantification of phytohormones were carried out on four representative developmental stages (i.e., 6-9-15-20 days after sowing) to provide a comprehensive overview of the events associated with primary and secondary growth in hemp. This multidisciplinary approach provides cell wall-related snapshots of the growing hemp hypocotyl and identifies marker genes associated with the young (expansins, β-galactosidases, and transcription factors involved in light-related processes) and the older hypocotyl (secondary cell wall biosynthetic genes and transcription factors).

Environmental Research and Innovation Department Luxembourg Institute of Science and Technology Esch sur Alzette Luxembourg

Environmental Research and Innovation Department Luxembourg Institute of Science and TechnologyEsch sur Alzette Luxembourg; Groupe de Recherche en Physiologie Végétale Earth and Life Institute Agronomy Université catholique de LouvainLouvain la Neuve Belgium

Groupe de Recherche en Physiologie Végétale Earth and Life Institute Agronomy Université catholique de Louvain Louvain la Neuve Belgium

Institute of Experimental Botany The Czech Academy of Sciences Prague Czechia

Zobrazit více v PubMed

Andre C. M., Hausman J.-F., Guerriero G. (2016). Cannabis sativa: the plant of the thousand and one molecules. Front. Plant Sci. 7:19 10.3389/fpls.2016.00019 PubMed DOI PMC

Berthet S., Thevenin J., Baratiny D., Mont-Caulet N., Debeaujon I., Bidzinski P., et al. (2012). “Chapter 5 – Role of plant laccases in lignin polymerization,” in Advances in Botanical Research. Lignins Biosynthesis, Biodegradation and Bioengineering eds Jouanin L., Lapierre C. (London: Academic Press; ) 145–172.

Bieniawska Z., Paul Barratt D. H., Garlick A. P., Thole V., Kruger N. J., Martin C., et al. (2007). Analysis of the sucrose synthase gene family in Arabidopsis. Plant J. 49 810–828. 10.1111/j.1365-313X.2006.03011.x PubMed DOI

Bindea G., Galon J., Mlecnik B. (2013). CluePedia Cytoscape plugin: pathway insights using integrated experimental and in silico data. Bioinformatics 29 661–663. 10.1093/bioinformatics/btt019 PubMed DOI PMC

Bindea G., Mlecnik B., Hackl H., Charoentong P., Tosolini M., Kirilovsky A., et al. (2009). ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 25 1091–1093. 10.1093/bioinformatics/btp101 PubMed DOI PMC

Blake A. W., Marcus S. E., Copeland J. E., Blackburn R. S., Knox J. P. (2008). In situ analysis of cell wall polymers associated with phloem fiber cells in stems of hemp, Cannabis sativa L. Planta 228 1–13. 10.1007/s00425-008-0713-5 PubMed DOI

Bourquin V., Nishikubo N., Abe H., Brumer H., Denman S., Eklund M., et al. (2002). Xyloglucan endotransglycosylases have a function during the formation of secondary cell walls of vascular tissues. Plant Cell 14 3073–3088. 10.1105/tpc.007773 PubMed DOI PMC

Brown D. M., Zeef L. A. H., Ellis J., Goodacre R., Turner S. R. (2005). Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17 2281–2295. 10.1105/tpc.105.031542 PubMed DOI PMC

Cosgrove D. J. (2005). Growth of the plant cell wall. Nat. Rev. Mol. Cell Biol. 6 850–861. 10.1038/nrm1746 PubMed DOI

Crônier D., Monties B., Chabbert B. (2005). Structure and chemical composition of bast fibers isolated from developing hemp stem. J. Agric. Food Chem. 53 8279–8289. 10.1021/jf051253k PubMed DOI

Daub C. O., Kloska S., Selbig J. (2003). MetaGeneAlyse: analysis of integrated transcriptional and metabolite data. Bioinformatics 19 2332–2333. 10.1093/bioinformatics/btg321 PubMed DOI

De Pauw M. A., Vidmar J. J., Collins J., Bennett R. A., Deyholos M. K. (2007). Microarray analysis of bast fiber producing tissues of Cannabis sativa identifies transcripts associated with conserved and specialised processes of secondary wall development. Funct. Plant Biol. 34 737–749. 10.1071/FP07014 PubMed DOI

De Rybel B., Mahonen A. P., Helariutta Y., Weijers D. (2016). Plant vascular development: from early specification to differentiation. Nat. Rev. Mol. Cell Biol. 17 30–40. 10.1038/nrm.2015.6 PubMed DOI

Derbyshire P., Ménard D., Green P., Saalbach G., Buschmann H., Lloyd C. W., et al. (2015). Proteomic analysis of microtubule interacting proteins over the course of xylem tracheary element formation in Arabidopsis. Plant Cell 27 2709–2726. 10.1105/tpc.15.00314 PubMed DOI PMC

Didi V., Jackson P., Hejátko J. (2015). Hormonal regulation of secondary cell wall formation. J. Exp. Bot. 66 5015–5027. 10.1093/jxb/erv222 PubMed DOI

Djilianov D. L., Dobrev P. I., Moyankova D. P., Vankova R., Georgieva D. T., Gajdosova S., et al. (2013). Dynamics of endogenous phytohormones during desiccation and recovery of the resurrection plant species Haberlea rhodopensis. J. Plant Growth Regul. 32 564–574. 10.1007/s00344-013-9323-y DOI

Doblin M. S., Kurek I., Jacob-Wilk D., Delmer D. P. (2002). Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol. 43 1407–1420. 10.1093/pcp/pcf164 PubMed DOI

Dobrev P. I., Vankova R. (2012). “Quantification of abscisic acid, cytokinin, and auxin content in salt-stressed plant tissues,” in Plant Salt Tolerance: Methods and Protocols eds Shabala S., Cuin A. T. (Totowa, NJ: Humana Press; ) 251–261. PubMed

Eklöf J. M., Brumer H. (2010). The XTH gene family: an update on enzyme structure, function, and phylogeny in xyloglucan remodeling. Plant Physiol. 153 456–466. 10.1104/pp.110.156844 PubMed DOI PMC

Eudes A., Pollet B., Sibout R., Do C. T., Séguin A., Lapierre C., et al. (2006). Evidence for a role of AtCAD 1 in lignification of elongating stems of Arabidopsis thaliana. Planta 225 23–39. 10.1007/s00425-006-0326-9 PubMed DOI

Fernández-Pérez F., Pomar F., Pedreno M. A., Novo-Uzal E. (2014). The suppression of AtPrx52 affects fibers but not xylem lignification in Arabidopsis by altering the proportion of syringyl units. Physiol. Plant. 154 395–406. 10.1111/ppl.12310 PubMed DOI

Francoz E., Ranocha P., Nguyen-Kim H., Jamet E., Burlat V., Dunand C. (2015). Roles of cell wall peroxidases in plant development. Phytochemistry 112 15–21. 10.1016/j.phytochem.2014.07.020 PubMed DOI

Franková L., Fry S. C. (2013). Biochemistry and physiological roles of enzymes that cut and paste plant cell-wall polysaccharides. J. Exp. Bot. 64 3519–3550. 10.1093/jxb/ert201 PubMed DOI

Gorshkova T., Morvan C. (2006). Secondary cell-wall assembly in flax phloem fibres: role of galactans. Planta 223 149–158. 10.1007/s00425-005-0118-7 PubMed DOI

Gorshkova T. A., Sal’nikov V. V., Chemikosova S. B., Ageeva M. V., Pavlencheva N. V., van Dam J. E. G. (2003). The snap point: a transition point in Linum usitatissimum bast fiber development. Ind. Crops Prod. 18 213–221. 10.1016/S0926-6690(03)00043-8 DOI

Gray-Mitsumune M., Mellerowicz E. J., Abe H., Schrader J., Winzéll A., Sterky F., et al. (2004). Expansins abundant in secondary xylem belong to subgroup A of the α-expansin gene family. Plant Physiol. 135 1552–1564. 10.1104/pp.104.039321 PubMed DOI PMC

Guerriero G., Hausman J. F., Strauss J., Ertan H., Siddiqui K. S. (2016). Lignocellulosic biomass: biosynthesis, degradation, and industrial utilization. Eng. Life Sci. 16 1–16. 10.1002/elsc.201400196 DOI

Guerriero G., Sergeant K., Hausman J. F. (2013). Integrated -omics: a powerful approach to understanding the heterogeneous lignification of fiber crops. Int. J. Mol. Sci. 14 10958–10978. 10.3390/ijms140610958 PubMed DOI PMC

Guerriero G., Sergeant K., Hausman J. F. (2014). Wood biosynthesis and typologies: a molecular rhapsody. Tree Physiol. 34 839–855. 10.1093/treephys/tpu031 PubMed DOI

Han L. B., Li Y. B., Wang H. Y., Wu X. M., Li C. L., Luo M., et al. (2013). The dual functions of WLIM1a in cell elongation and secondary wall formation in developing cotton fibers. Plant Cell 25 4421–4438. 10.1105/tpc.113.116970 PubMed DOI PMC

Hao Z., Mohnen D. (2014). A review of xylan and lignin biosynthesis: foundation for studying Arabidopsis irregular xylem mutants with pleiotropic phenotypes. Crit. Rev. Biochem. Mol. Biol. 49 212–241. 10.3109/10409238.2014.889651 PubMed DOI

Havlová M., Dobrev P. I., Motyka V., Storchová H., Libus J., Dobrá J., et al. (2008). The role of cytokinins in responses to water deficit in tobacco plants over-expressing trans-zeatin O-glucosyltransferase gene under 35S or SAG12 promoters. Plant Cell Environ. 31 341–353. 10.1111/j.1365-3040.2007.01766.x PubMed DOI

Herrero J., Esteban Carrasco A., Zapata J. M. (2014). Arabidopsis thaliana peroxidases involved in lignin biosynthesis: in silico promoter analysis and hormonal regulation. Plant Physiol. Biochem. 80 192–202. 10.1016/j.plaphy.2014.03.027 PubMed DOI

Hirose N., Takei K., Kuroha T., Kamada-Nobusada T., Hayashi H., Sakakibara H. (2008). Regulation of cytokinin biosynthesis, compartmentalization and translocation. J. Exp. Bot. 59 75–83. 10.1093/jxb/erm157 PubMed DOI

Hobson N., Roach M. J., Deyholos M. K. (2010). Gene expression in tension wood and bast fibers. Russ. J. Plant Physl. 57 321–327. 10.1104/pp.111.172676 DOI

Ikeda M., Mitsuda N., Ohme-Takagi M. (2013). ATBS1 INTERACTING FACTORs negatively regulate Arabidopsis cell elongation in the triantagonistic bHLH system. Plant Signal. Behav. 8:e23448 10.4161/psb.23448 PubMed DOI PMC

Ito S., Suzuki Y., Miyamoto K., Ueda J., Yamaguchi I. (2005). AtFLA11, a fasciclin-like arabinogalactan-protein, specifically localized in screlenchyma cells. Biosci. Biotechnol. Biochem. 69 1963–1969. 10.1271/bbb.69.1963 PubMed DOI

Jensen J. K., Kim H., Cocuron J. C., Orler R., Ralph J., Wilkerson C. G. (2011). The DUF579 domain containing proteins IRX15 and IRX15-L affect xylan synthesis in Arabidopsis. Plant J. 66 387–400. 10.1111/j.1365-313X.2010.04475.x PubMed DOI

Jin J., Zhang H., Kong L., Gao G., Luo J. (2014). PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res. 42 D1182–D1187. 10.1093/nar/gkt1016 PubMed DOI PMC

Johnson K. L., Jones B. J., Bacic A., Schultz C. J. (2003). The fasciclin-like arabinogalactan proteins of Arabidopsis. A multigene family of putative cell adhesion molecules. Plant Physiol. 133 1911–1925. 10.1104/pp.103.031237 PubMed DOI PMC

Lombard V., GolacondaRamulu H., Drula E., Coutinho P. M., Henrissat B. (2014). The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42 D490–D495. 10.1093/nar/gkt1178 PubMed DOI PMC

MacMillan C. P., Taylor L., Bi Y., Southerton S. G., Evans R., Spokevicius A. (2015). The fasciclin-like arabinogalactan protein family of Eucalyptus grandis contains members that impact wood biology and biomechanics. New Phytol. 206 1314–1327. 10.1111/nph.13320 PubMed DOI

Men L., Yan S., Liu G. (2013). De novo characterization of Larix gmelinii (Rupr.) Rupr. transcriptome and analysis of its gene expression induced by jasmonates. BMC Genomics 14:548 10.1186/1471-2164-14-548 PubMed DOI PMC

Mikshina P., Chernova T., Chemikosova S. B., Ibragimova N., Mokshina N., Gorshkova T. (2013). “Cellulosic fibers: role of matrix polysaccharides in structure and function,” in Cellulose – Fundamental Aspects eds van de Ven T., Godbout L. (Rijeka: InTech; ) 91–112.

Mokshina N., Gorshkova T., Deyholos M. K. (2014). Chitinase-like and cellulose synthase gene expression in gelatinous-type cellulosic walls of flax (Linum usitatissimum L.) bast fibers. PLoS ONE 9:e97949 10.1371/journal.pone.0097949 PubMed DOI PMC

Mortazavi A., Williams B. A., McCue K., Schaeffer L., Wold B. (2008). Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5 621–628. 10.1038/nmeth.1226 PubMed DOI

Mortimer J. C., Faria-Blanc N., Yu X., Tryfona T., Sorieul M., Ng Y. Z., et al. (2015). An unusual xylan in Arabidopsis primary cell walls is synthesised by GUX3, IRX9L, IRX10L and IRX14. Plant J. 83 413–426. 10.1111/tpj.12898 PubMed DOI PMC

Moura J. C. M. S., Bonine C. A. V., FernandesViana J., Dornelas M. C., Mazzafera P. (2010). Abiotic and biotic stresses and changes in the lignin content and composition in plants. J. Integr. Plant Biol. 52 360–376. 10.1111/j.1744-7909.2010.00892.x PubMed DOI

Nanao M. H., Vinos-Poyo T., Brunoud G., Thévenon E., Mazzoleni M., Mast D., et al. (2014). Structural basis for oligomerization of auxin transcriptional regulators. Nat. Commun. 5:3617 10.1038/ncomms4617 PubMed DOI

Nieminen K., Blomster T., Helariutta Y., Mähönen A. P. (2015). Vascular cambium development. Arabidopsis Book 11:e0177 10.1199/tab.0177 PubMed DOI PMC

Oh E., Zhu J. Y., Bai M. Y., Arenhart R. A., Sun Y., Wang Z. Y. (2014). Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. Elife 3:e03031 10.7554/eLife.03031 PubMed DOI PMC

Park Y. B., Cosgrove D. J. (2015). Xyloglucan and its interactions with other components of the growing cell wall. Plant Cell Physiol. 56 180–194. 10.1093/pcp/pcu204 PubMed DOI

Pauwels L., Morreel K., De Witte E., Lammertyn F., Van Montagu M., Boerjan W., et al. (2008). Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells. Proc. Natl. Acad. Sci. U.S.A. 105 1380–1385. 10.1073/pnas.0711203105 PubMed DOI PMC

Ragni L., Hardtke C. S. (2014). Small but thick enough-the Arabidopsis hypocotyl as a model to study secondary growth. Physiol. Plant. 151 164–171. 10.1111/ppl.12118 PubMed DOI

Ragni L., Nieminen K., Pacheco-Villalobos D., Sibout R., Schwechheimer C., Hardtke C. S. (2011). Mobile gibberellin directly stimulates Arabidopsis hypocotyl xylem expansion. Plant Cell 23 1322–1336. 10.1105/tpc.111.084020 PubMed DOI PMC

Rajkumar A., Qvist P., Lazarus R., Lescai F., Ju J., Nyegaard M., et al. (2015). Experimental validation of methods for differential gene expression analysis and sample pooling in RNA-seq. BMC Genomics 16:548 10.1186/s12864-015-1767-y PubMed DOI PMC

Ranocha P., Dima O., Nagy R., Felten J., Corratgé-Faillie C., Novák O., et al. (2013). Arabidopsis WAT1 is a vacuolar auxin transport facilitator required for auxin homoeostasis. Nat. Commun. 4:2625 10.1038/ncomms3625 PubMed DOI PMC

Roach M. J., Deyholos M. K. (2007). Microarray analysis of flax (Linum usitatissimum L.) stems identifies transcripts enriched in fiber-bearing phloem tissues. Mol. Genet. Genomics 278 149–165. 10.1007/s00438-007-0241-1 PubMed DOI

Roach M. J., Deyholos M. K. (2008). Microarray analysis of developing flax hypocotyls identifies novel transcripts correlated with specific stages of phloem fiber differentiation. Ann. Bot. 102 317–330. 10.1093/aob/mcn110 PubMed DOI PMC

Roach M. J., Mokshina N. Y., Badhan A., Snegireva A. V., Hobson N., Deyholos M. K., et al. (2011). Development of cellulosic secondary walls in flax fibers requires ß-galactosidase. Plant Physiol. 156 1351–1363. 10.1104/pp.111.172676 PubMed DOI PMC

Sakakibara H. (2006). CYTOKININS: activity, biosynthesis, and translocation. Annu. Rev. Plant Biol. 57 431–449. 10.1146/annurev.arplant.57.032905.105231 PubMed DOI

Sampedro J., Gianzo C., Iglesias N., Guitián E., Revilla G., Zarra I. (2012). AtBGAL10 is the main xyloglucan ß-galactosidase in Arabidopsis, and its absence results in unusual xyloglucan subunits and growth defects. Plant Physiol. 158 1146–1157. 10.1104/pp.111.192195 PubMed DOI PMC

Sánchez-Rodríguez C., Rubio-Somoza I., Sibout R., Persson S. (2010). Phytohormones and the cell wall in Arabidopsis during seedling growth. Trends Plant Sci. 15 291–301. 10.1016/j.tplants.2010.03.002 PubMed DOI

Sehr E. M., Agusti J., Lehner R., Farmer E. E., Schwarz M., Greb T. (2010). Analysis of secondary growth in the Arabidopsis shoot reveals a positive role of jasmonate signalling in cambium formation. Plant J. 63 811–822. 10.1111/j.1365-313X.2010.04283.x PubMed DOI PMC

Shaipulah N. F., Muhlemann J. K., Woodworth B. D., Van Moerkercke A., Verdonk J. C., Ramirez A. A., et al. (2016). CCoAOMT down-regulation activates anthocyanin biosynthesis in Petunia. Plant Physiol. 170 717–731. 10.1104/pp.15.01646 PubMed DOI PMC

Shen B., Li C., Tarczynski M. C. (2002). High free-methionine and decreased lignin content result from a mutation in the Arabidopsis S-adenosyl-L-methionine synthetase 3 gene. Plant J. 29 371–380. 10.1046/j.1365-313X.2002.01221.x PubMed DOI

Shibaoka H. (1994). Plant hormone-induced changes in the orientation of cortical microtubules: alterations in the cross-linking between microtubules and the plasma membrane. Annu. Rev. Plant Phys. 45 527–544. 10.1146/annurev.pp.45.060194.002523 DOI

Sibout R., Plantegenet S., Hardtke C. S. (2008). Flowering as a condition for xylem expansion in Arabidopsis hypocotyl and root. Curr. Biol. 18 458–463. 10.1016/j.cub.2008.02.070 PubMed DOI

Snegireva A., Chernova T., Ageeva M., Lev-Yadun S., Gorshkova T. (2015). Intrusive growth of primary and secondary phloem fibers in hemp stem determines fiber-bundle formation and structure. AoB Plants 7: plv061 10.1093/aobpla/plv061 PubMed DOI PMC

Soyano T., Thitamadee S., Machida Y., Chua N. H. (2008). ASYMMETRIC LEAVES2-LIKE19/LATERAL ORGAN BOUNDARIES DOMAIN30 and ASL20/LBD18 regulate tracheary element differentiation in Arabidopsis. Plant Cell 20 3359–3373. 10.1105/tpc.108.061796 PubMed DOI PMC

Steyn W. J., Wand S. J. E., Holcroft D. M., Jacobs G. (2002). Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. New Phytol. 155 349–361. 10.1046/j.1469-8137.2002.00482.x PubMed DOI

Sugawara S., Mashiguchi K., Tanaka K., Hishiyama S., Sakai T., Hanada K., et al. (2015). Distinct characteristics of indole-3-acetic acid and phenylacetic acid, two common auxins in plants. Plant Cell Physiol. 56 1641–1654. 10.1093/pcp/pcv088 PubMed DOI PMC

Taki N., Sasaki-Sekimoto Y., Obayashi T., Kikuta A., Kobayashi K., Ainai T., et al. (2005). 12-oxo-phytodienoic acid triggers expression of a distinct set of genes and plays a role in wound-induced gene expression in Arabidopsis. Plant Physiol. 139 1268–1283. 10.1104/pp.105.067058 PubMed DOI PMC

Taylor-Teeples M., Lin L., de Lucas M., Turco G., Toal T. W., Gaudinier A., et al. (2015). An Arabidopsis gene regulatory network for secondary cell wall synthesis. Nature 517 571–575. 10.1038/nature14099 PubMed DOI PMC

Titapiwatanakun B., Blakeslee J. J., Bandyopadhyay A., Yang H., Mravec J., Sauer M., et al. (2009). ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis. Plant J. 57 27–44. 10.1111/j.1365-313X.2008.03668.x PubMed DOI

Tocquard K., Lafon-Placette C., Auguin D., Muries B., Bronner G., Lopez D., et al. (2014). In silico study of wall-associated kinase family reveals large-scale genomic expansion potentially connected with functional diversification in Populus. Tree Genet. Genomes 10 1135–1147. 10.1007/s11295-014-0748-7 DOI

Tokunaga N., Kaneta T., Sato S., Sato Y. (2009). Analysis of expression profiles of three peroxidase genes associated with lignification in Arabidopsis thaliana. Physiol. Plant. 136 237–249. 10.1111/j.1399-3054.2009.01233.x PubMed DOI

Turlapati P., Kim K. W., Davin L., Lewis N. (2011). The laccase multigene family in Arabidopsis thaliana: towards addressing the mystery of their gene function(s). Planta 233 439–470. 10.1007/s00425-010-1298-3 PubMed DOI

van Bakel H., Stout J. M., Cote A. G., Tallon C. M., Sharpe A. G., Hughes T. R., et al. (2011). The draft genome and transcriptome of Cannabis sativa. Genome Biol. 12:R102 10.1186/gb-2011-12-10-r102 PubMed DOI PMC

van den Broeck H. C., Maliepaard C., Ebskamp M. J. M., Toonen M. A. J., Koops A. J. (2008). Differential expression of genes involved in C1 metabolism and lignin biosynthesis in wooden core and bast tissues of fiber hemp (Cannabis sativa L.). Plant Sci. 174 205–220. 10.1016/j.plantsci.2007.11.008 DOI

van Raemdonck D., Pesquet E., Cloquet S., Beeckman H., Boerjan W., Goffner D., et al. (2005). Molecular changes associated with the setting up of secondary growth in aspen. J. Exp. Bot. 56 2211–2227. 10.1093/jxb/eri221 PubMed DOI

Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., et al. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3:RESEARCH0034. PubMed PMC

Wang Y., Chantreau M., Sibout R., Hawkins S. (2013). Plant cell wall lignification and monolignol metabolism. Front. Plant Sci. 4:220 10.3389/fpls.2013.00220 PubMed DOI PMC

Wang Y., Zhou B., Sun M., Li Y., Kawabata S. (2012). UV-A light induces anthocyanin biosynthesis in a manner distinct from synergistic blue + UV-B light and UV-A/blue light responses in different parts of the hypocotyls in turnip seedlings. Plant Cell Physiol. 53 1470–1480. 10.1093/pcp/pcs088 PubMed DOI

Zhang Q., Cheetamun R., Dhugga K., Rafalski J., Tingey S., Shirley N., et al. (2014). Spatial gradients in cell wall composition and transcriptional profiles along elongating maize internodes. BMC Plant Biol. 14:27 10.1186/1471-2229-14-27 PubMed DOI PMC

Zhao C., Avci U., Grant E. H., Haigler C. H., Beers E. P. (2008). XND1, a member of the NAC domain family in Arabidopsis thaliana, negatively regulates lignocellulose synthesis and programmed cell death in xylem. Plant J. 53 425–436. 10.1111/j.1365-313X.2007.03350.x PubMed DOI

Zhao C., Craig J. C., Petzold H. E., Dickerman A. W., Beers E. P. (2005). The xylem and phloem transcriptomes from secondary tissues of the Arabidopsis root-hypocotyl. Plant Physiol. 138 803–818. 10.1104/pp.105.060202 PubMed DOI PMC

Zhong R., Lee C., Zhou J., McCarthy R. L., 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. 10.1105/tpc.108.061325 PubMed DOI PMC

Zhong R., Ye Z. H. (2007). Regulation of cell wall biosynthesis. Curr. Opin. Plant Biol. 10 564–572. 10.1016/j.pbi.2007.09.001 PubMed DOI

Zhong R., Ye Z. H. (2009). Transcriptional regulation of lignin biosynthesis. Plant Signal. Behav. 4 1028–1034. 10.4161/psb.4.11.9875 PubMed DOI PMC

Zhong R., Ye Z. H. (2014). Complexity of the transcriptional network controlling secondary wall biosynthesis. Plant Sci. 229 193–207. 10.1016/j.plantsci.2014.09.009 PubMed DOI

Zhong R., Ye Z. H. (2015). Secondary cell walls: biosynthesis, patterned deposition and transcriptional regulation. Plant Cell Physiol. 56 195–214. 10.1093/pcp/pcu140 PubMed DOI

Zúñiga-Sánchez E., Soriano D., Martinez-Barajas E., Orozco-Segovia A., Gamboa-deBuen A. (2014). BIIDXI, the At4g32460 DUF642 gene, is involved in pectin methyl esterase regulation during Arabidopsis thaliana seed germination and plant development. BMC Plant Biol. 14:338 10.1186/s12870-014-0338-8 PubMed DOI PMC

Impact of jasmonic acid on lignification in the hemp hypocotyl