Nothing Special   »   [go: up one dir, main page]

Skip to main content

Advertisement

Log in

Comparative transcriptomic analysis uncovers conserved pathways involved in adventitious root formation in poplar

  • Research Article
  • Published:
Physiology and Molecular Biology of Plants Aims and scope Submit manuscript

Abstract

Cutting propagation is widely used in establishing poplar plantations, and this approach requires efficient adventitious root (AR) forming capacities. Although poplar species are considered to form roots easily, interspecific variations in AR formation are still observed. To better understand the gene regulatory network underlying the conserved modified pathways that are essential for AR formation in poplar species, comparative transcriptomic approaches were applied to identify the conserved common genes that were differentially expressed during the AR formation processes in two poplar species (Populus × euramericana and P. simonii) in woody plant medium (WPM). A total of 2146 genes were identified as conserved genes that shared similar gene expression profiles in at least one comparison. These conserved genes were enriched in diverse hormone signaling pathways, as well as the mitogen-associated protein kinase (MAPK) signaling pathway, suggesting an important role for signaling transduction in coordinating external stimuli and endogenous physiological status during AR regulation in poplar. Furthermore, the co-expression network analysis of conserved genes allowed identification of several co-expressed modules (CM) that are co-expressed with distinct biological functions, for instance, CM1 was enriched in defense response and hormone signaling, CM2 and CM3 were overrepresented in defense response-related pathways and for cell cycle, respectively. These results suggest that the AR formation processes in poplar were finely tuned at the transcriptomic level by integrating multiple biological processes essential for AR formation. Our results suggest conserved machinery for AR formation in poplar and generated informative gene co-expression networks that describe the basis of AR formation in these species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

adapted from the MAPK signaling pathway in the KEGG pathway. The gene expression levels in P. × euramericana (Pe) and P. simonii (Ps) of each time point during AR formation are shown in different columns in the colored grids, and the different rows represent the different genes. The colors indicate the levels of gene expression with red representing upregulation and blue representing downregulation. The gene expression levels of Pe and Ps during the different time points were normalized to 0 days after excision (DAE0) of the corresponding poplar species

Fig. 4

adapted from the phytohormone signaling pathways in the KEGG pathway. The gene expression levels in P. × euramericana (Pe) and P. simonii (Ps) of each time point during AR formation are shown in different columns in the colored grids, and the different rows represent the different genes. The colors indicate the levels of gene expression with red representing upregulation and blue representing downregulation. The gene expression levels of Pe and Ps during the different time points were normalized to 0 days after excision (DAE0) of the corresponding poplar species

Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Availability of data and material

Not applicable.

Code availability

Not applicable.

References

  • Abu-Abied M, Szwerdszarf D, Mordehaev I, Levy A, Stelmakh OR, Belausov E, Yaniv Y, Uliel S, Katzenellenbogen M, Riov J, Ophir R, Sadot E (2012) Microarray analysis revealed upregulation of nitrate reductase in juvenile cuttings of Eucalyptus grandis, which correlated with increased nitric oxide production and adventitious root formation. Plant J 71:787–799

    Article  CAS  PubMed  Google Scholar 

  • Agulló-Antón MÁ, Ferrández-Ayela A, Fernández-García N, Nicolás C, Albacete A, Pérez-Alfocea F, Sánchez-Bravo J, Pérez-Pérez JM, Acosta M (2014) Early steps of adventitious rooting: morphology, hormonal profiling and carbohydrate turnover in carnation stem cuttings. Physiol Plant 150:446–462

    Article  PubMed  CAS  Google Scholar 

  • Allfrey V, Faulkner R, Mirsky A (1964) Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc Natl Acad Sci USA 51:786–794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anders S, Pyl PT, Huber W (2015) HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31:166–169

    Article  CAS  PubMed  Google Scholar 

  • Astier J, Gross I, Durner J (2017) Nitric oxide production in plants: an update. J Exp Bot 69:3401–3411

    Article  CAS  Google Scholar 

  • Astier J, Besson-Bard A, Wawer I, Parent C, Rasul S, Jeandroz S, Dat J, Wendehenne D (2018) Nitric oxide signalling in plants: cross-talk with Ca2+, protein kinases and reactive oxygen species. In: Roberts JA (ed) Annual Plant Reviews online. Wiley Online Library, New York, pp 147–170

    Chapter  Google Scholar 

  • Bai L, Ma X, Zhang G, Song S, Zhou Y, Gao L, Miao Y, Song C-P (2014) A receptor-like kinase mediates ammonium homeostasis and is important for the polar growth of root hairs in Arabidopsis. Plant Cell 26:1497–1511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bannoud F, Bellini C (2021) Adventitious rooting in Populus species: Update and perspectives. Front Plant Sci 12:668837

    Article  PubMed  PubMed Central  Google Scholar 

  • Bellini C, Pacurar DI, Perrone I (2014) Adventitious roots and lateral roots: similarities and differences. Annu Rev Plant Biol 65:639–666

    Article  CAS  PubMed  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao X, Du W, Shang C, Shen Q, Liu L, Cheng J (2018) Comparative transcriptome reveals circadian and hormonal control of adventitious rooting in mulberry hardwood cuttings. Acta Physiol Plant 40:197

    Article  CAS  Google Scholar 

  • Da Costa C, De Almeida M, Ruedell C, Schwambach J, Maraschin F, Fett-Neto A (2013) When stress and development go hand in hand: main hormonal controls of adventitious rooting in cuttings. Front Plant Sci 4:133

    Article  PubMed  PubMed Central  Google Scholar 

  • De Klerk G-J, Guan H, Huisman P, Marinova S (2011) Effects of phenolic compounds on adventitious root formation and oxidative decarboxylation of applied indoleacetic acid in Malus ‘Jork 9.’ Plant Growth Regul 63:175–185

    Article  CAS  Google Scholar 

  • Druege U, Franken P, Hajirezaei MR (2016) Plant hormone homeostasis, signaling, and function during adventitious root formation in cuttings. Front Plant Sci 7:381

    Article  PubMed  PubMed Central  Google Scholar 

  • Du XL, Cao X, Yin CR, Tang Z, Du W, Ban YY, Cheng JL (2017) Comprehensive analysis of R2R3-MYB genes during adventitious root formation in cuttings of Morus alba. J Plant Growth Reg 36:290–299

    Article  CAS  Google Scholar 

  • Duclercq J, Sangwan-Norreel B, Catterou M, Sangwan RS (2011) De novo shoot organogenesis: from art to science. Trends Plant Sci 16:597–606

    Article  CAS  PubMed  Google Scholar 

  • Eliasson L (1978) Effects of nutrients and light on growth and root formation in Pisum sativum cuttings. Physiol Plant 43:13–18

    Article  CAS  Google Scholar 

  • Fett-Neto AG, Fett JP, Goulart LWV, Pasquali G, Termignoni RR, Ferreira AG (2001) Distinct effects of auxin and light on adventitious root development in Eucalyptus saligna and Eucalyptus globulus. Tree Physiol 21:457–464

    Article  CAS  PubMed  Google Scholar 

  • Gao Y, Zhang G (2019) A calcium sensor calcineurin B-like 9 negatively regulates cold tolerance via calcium signaling in Arabidopsis thaliana. Plant Signal Behav 14:e1573099

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Geiss G, Gutierrez L, Bellini C (2018) Adventitious root formation: new insights and perspectives. In: Roberts JA (ed) Annual plant reviews online. Wiley Online Library, New York, pp 127–156

    Chapter  Google Scholar 

  • Ghosh S, Chan C-KK (2016) Analysis of RNA-Seq data using TopHat and Cufflinks. In: Edwards D (ed) Plant bioinformatics. Humana Press, New York, pp 339–361

    Chapter  Google Scholar 

  • Ginestet C (2011) ggplot2: elegant graphics for data analysis. J R Stat Soc A Stat 174:245–246

    Article  Google Scholar 

  • Han H, Sun X, Xie Y, Feng J, Zhang S (2014a) Transcriptome and proteome profiling of adventitious root development in hybrid larch (Larix kaempferi × Larix olgensis). BMC Plant Biol 14:305

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Han S, Wang C-W, Jiang J (2014b) Mitogen-activated protein kinase 6 controls root growth in Arabidopsis by modulating Ca2+-based Na+ flux in root cell under salt stress. J Plant Physiol 171:26–34

    Article  CAS  PubMed  Google Scholar 

  • Han S, Fang L, Ren X, Wang W, Jiang J (2015) MPK6 controls H2O2-induced root elongation by mediating Ca2+ influx across the plasma membrane of root cells in Arabidopsis seedlings. New Phytol 205:695–706

    Article  CAS  PubMed  Google Scholar 

  • Hedayati V, Mousavi A, Razavi K, Cultrera N, Alagna F, Mariotti R, Hosseini-Mazinani M, Baldoni L (2015) Polymorphisms in the AOX2 gene are associated with the rooting ability of olive cuttings. Plant Cell Rep 34:1151–1164

    Article  CAS  PubMed  Google Scholar 

  • Jiao Y, Sun L, Song Y, Wang L, Liu L, Zhang L, Liu B, Li N, Miao C, Hao F (2013) AtrbohD and AtrbohF positively regulate abscisic acid-inhibited primary root growth by affecting Ca2+ signalling and auxin response of roots in Arabidopsis. J Exp Bot 64:4183–4192

    Article  CAS  PubMed  Google Scholar 

  • Jin J, Tian F, Yang D-C, Meng Y-Q, Kong L, Luo J, Gao G (2016) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res 2016:D1040–D1045

    Google Scholar 

  • Kolde R (2019) pheatmap: Pretty Heatmaps. R package version 1.0.12. https://CRAN.R-project.org/package=pheatmap

  • Krabel D, Meyer M, Solger A, Müller R, Carvalho P, Foulkes J (2015) Early root and aboveground biomass development of hybrid poplars (Populus spp.) under drought conditions. Can J Forest Res 45:1289–1298

    Article  Google Scholar 

  • Kumar Patel M, Pandey S, Burritt DJ, Phan Tran L-S (2019) Plant responses to low-oxygen stress: interplay between ROS and NO signaling pathways. Environ Exp Bot 161:131–142

    Google Scholar 

  • Lakehal A, Bellini C (2019) Control of adventitious root formation: insights into synergistic and antagonistic hormonal interactions. Physiol Plant 165:90–100

    Article  CAS  PubMed  Google Scholar 

  • Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinform 9:559

    Article  CAS  Google Scholar 

  • Lanteri L, Pagnussat G, Laxalt A, Lamattina L (2009) Nitric oxide is downstream of auxin and is required for inducing adventitious root formation in herbaceous and woody plants. In: Niemi K, Scagel C (eds) Adventitious root formation of forest trees and horticultural plants–from genes to applications. Research Signpost, Kerala, pp 222–245

    Google Scholar 

  • Li S-W, Xue L (2010) The interaction between H2O2 and NO, Ca2+, cGMP, and MAPKs during adventitious rooting in mung bean seedlings. Vitro Cell Dev-Pl 46:142–148

    Article  CAS  Google Scholar 

  • Li S, Xue L, Xu S, Feng H, An L (2007) Hydrogen peroxide involvement in formation and development of adventitious roots in cucumber. Plant Growth Reg 52:173–180

    Article  CAS  Google Scholar 

  • Li S-W, Xue L, Xu S, Feng H, An L (2009) Mediators, genes and signaling in adventitious rooting. Bot Rev 75:230–247

    Article  Google Scholar 

  • Li N, Sun L, Zhang L, Song Y, Hu P, Li C, Hao FS (2015) AtrbohD and AtrbohF negatively regulate lateral root development by changing the localized accumulation of superoxide in primary roots of Arabidopsis. Planta 241:591–602

    Article  CAS  PubMed  Google Scholar 

  • Li J, Zhang J, Jia H, Liu B, Sun P, Hu J, Wang L, Lu M (2017a) The WUSCHEL-related homeobox 5a (PtoWOX5a) is involved in adventitious root development in poplar. Tree Physiol 38:139–153

    Article  CAS  Google Scholar 

  • Li S-W, Leng Y, Shi R-F (2017b) Transcriptomic profiling provides molecular insights into hydrogen peroxide-induced adventitious rooting in mung bean seedlings. BMC Genomics 18:188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li C, Bian B, Gong T, Liao W (2018a) Comparative proteomic analysis of key proteins during abscisic acid-hydrogen peroxide-induced adventitious rooting in cucumber (Cucumis sativus L.) under drought stress. J Plant Physiol 229:185–194

    Article  CAS  PubMed  Google Scholar 

  • Li S-W, Zeng X-Y, Leng Y, Feng L, Kang X-H (2018b) Indole-3-butyric acid mediates antioxidative defense systems to promote adventitious rooting in mung bean seedlings under cadmium and drought stresses. Ecotox Environ Safe 161:332–341

    Article  CAS  Google Scholar 

  • Liao W-B, Zhang M-L, Huang G-B, Yu J-H (2012) Ca2+ and CaM are involved in NO- and H2O2-induced adventitious root development in marigold. J Plant Growth Reg 31:253–264

    Article  CAS  Google Scholar 

  • Lin W-D, Liao Y-Y, Yang TJ, Pan C-Y, Buckhout TJ, Schmidt W (2011) Coexpression-based clustering of Arabidopsis root genes predicts functional modules in early phosphate deficiency signaling. Plant Physiol 155:1383–1402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu B, Rennenberg H, Kreuzwieser J (2015) Hypoxia affects nitrogen uptake and distribution in young poplar (Populus × canescens) trees. PLoS ONE 10:e0136579

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Luo W, Brouwer C (2013) Pathview: an R/Bioconductor package for pathway-based data integration and visualization. Bioinformatics 29:1830–1831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo J, Zhou JJ (2019) Growth performance, photosynthesis, and root characteristics are associated with nitrogen use efficiency in six poplar species. Environ Exp Bot 164:40–51

    Article  CAS  Google Scholar 

  • Luo J, Li H, Liu T, Polle A, Peng C, Luo Z-B (2013a) Nitrogen metabolism of two contrasting poplar species during acclimation to limiting nitrogen availability. J Exp Bot 64:4207–4224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo J, Qin J, He F, Li H, Liu T, Polle A, Peng C, Luo Z-B (2013b) Net fluxes of ammonium and nitrate in association with H+ fluxes in fine roots of Populus popularis. Planta 237:919–931

    Article  CAS  PubMed  Google Scholar 

  • Luo J, Zhou J, Li H, Shi W, Polle A, Lu M, Sun X, Luo Z-B (2015) Global poplar root and leaf transcriptomes reveal links between growth and stress responses under nitrogen starvation and excess. Tree Physiol 35:1283–1302

    Article  CAS  PubMed  Google Scholar 

  • Luo J, Shi W, Li H, Janz D, Luo Z-B (2016) The conserved salt-responsive genes in the roots of Populus × canescens and Arabidopsis thaliana. Environ Exp Bot 129:48–56

    Article  CAS  Google Scholar 

  • Luo J, Zhou J-J, Zhang J-Z (2018) Aux/IAA gene family in plants: molecular structure, regulation, and function. Int J Mol Sci 19:259

    Article  PubMed Central  CAS  Google Scholar 

  • Luo J, Liang Z, Wu M, Mei L (2019a) Genome-wide identification of BOR genes in poplar and their roles in response to various environmental stimuli. Environ Exp Bot 164:101–113

    Article  CAS  Google Scholar 

  • Luo J, Xia W, Cao P, Xiao ZA, Zhang Y, Liu M, Zhan C, Wang N (2019b) Integrated transcriptome analysis reveals plant hormones jasmonic acid and salicylic acid coordinate growth and defense responses upon fungal infection in poplar. Biomolecules 9:12

    Article  PubMed Central  CAS  Google Scholar 

  • Ma X, Zhang C, Zhang B, Yang C, Li S (2016) Identification of genes regulated by histone acetylation during root development in Populus trichocarpa. BMC Genomics 17:96

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mauriat M, Petterle A, Bellini C, Moritz T (2014) Gibberellins inhibit adventitious rooting in hybrid aspen and Arabidopsis by affecting auxin transport. Plant J 78:372–384

    Article  CAS  PubMed  Google Scholar 

  • Moriya S, Iwanami H, Haji T, Okada K, Yamada M, Yamamoto T, Abe K (2015) Identification and genetic characterization of a quantitative trait locus for adventitious rooting from apple hardwood cuttings. Tree Genet Genomes 11:59

    Article  Google Scholar 

  • Pacurar DI, Perrone I, Bellini C (2014) Auxin is a central player in the hormone cross-talks that control adventitious rooting. Physiol Plant 151:83–96

    Article  CAS  PubMed  Google Scholar 

  • Pagnussat GC, Lanteri ML, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol 132:1241–1248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng Y, Zhou Z, Zhang Z, Yu X, Zhang X, Du K (2018) Molecular and physiological responses in roots of two full-sib poplars uncover mechanisms that contribute to differences in partial submergence tolerance. Sci Rep 8:12829

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Plomion C, Bastien C, Bogeat-Triboulot M-B, Bouffier L, Déjardin A, Duplessis S, Fady B, Heuertz M, Le Gac A-L, Le Provost G, Legué V, Lelu-Walter M-A, Leplé J-C, Maury S, Morel A, Oddou-Muratorio S, Pilate G, Sanchez L, Scotti I, Scotti-Saintagne C, Segura V, Trontin J-F, Vacher C (2016) Forest tree genomics: 10 achievements from the past 10 years and future prospects. An for Sci 73:77–103

    Article  Google Scholar 

  • Qi X, Li Q, Ma X, Qian C, Wang H, Ren N, Shen C, Huang S, Xu X, Xu Q (2018) Waterlogging-induced adventitious root formation in cucumber is regulated by ethylene and auxin through reactive oxygen species signalling. Plant Cell Environ 42:1458–1470

    Article  CAS  Google Scholar 

  • Quan J, Meng S, Guo E, Zhang S, Zhao Z, Yang X (2017) De novo sequencing and comparative transcriptome analysis of adventitious root development induced by exogenous indole-3-butyric acid in cuttings of tetraploid black locust. BMC Genomics 18:179

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ramírez-Carvajal GA, Morse AM, Dervinis C, Davis JM (2009) The cytokinin type-B response regulator PtRR13 is a negative regulator of adventitious root development in Populus. Plant Physiol 150:759–771

    Article  PubMed  PubMed Central  Google Scholar 

  • Ribeiro CL, Silva CM, Drost DR, Novaes E, Novaes CRDB, Dervinis C, Kirst M (2016) Integration of genetic, genomic and transcriptomic information identifies putative regulators of adventitious root formation in Populus. BMC Plant Biol 16:66

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rigal A, Yordanov YS, Perrone I, Karlberg A, Tisserant E, Bellini C, Busov VB, Martin F, Kohler A, Bhalerao R (2012) The AINTEGUMENTA LIKE1 homeotic transcription factor PtAIL1 controls the formation of adventitious root primordia in poplar. Plant Physiol 160:1996–2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140

    Article  CAS  PubMed  Google Scholar 

  • Ronald S Jr, Zalesny JA (2009) Selecting Populus with different adventitious root types for environmental benefits, fiber, and energy. In: Niemi K, Seagel C (eds) Adventitious root formation of forest trees and horticultural plants-from genes to applications. Research Signpost, Kerala, pp 359–384

    Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steffens B, Rasmussen A (2016) The physiology of adventitious roots. Plant Physiol 170:603–617

    Article  CAS  PubMed  Google Scholar 

  • Sun LR, Wang YB, He SB, Hao FS (2018) Mechanisms for abscisic acid inhibition of primary root growth. Plant Signal Behav 13:e1500069

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sun P, Jia HX, Zhang YH, Li JB, Lu MZ, Hu JJ (2019) Deciphering genetic architecture of adventitious root and related shoot traits in Populus using QTL mapping and RNA-Seq data. Int J Mol Sci 20:6114

    Article  CAS  PubMed Central  Google Scholar 

  • Supek F, Bošnjak M, Škunca N, Šmuc T (2011) REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE 6:21800

    Article  CAS  Google Scholar 

  • Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939

    Article  CAS  PubMed  Google Scholar 

  • Thomas P, Schiefelbein J (2002) Cloning and characterization of an actin depolymerizing factor gene from grape (Vitis vinifera L.) expressed during rooting in stem cuttings. Plant Sci 162:283–288

    Article  CAS  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protoc 7:562

    Article  CAS  Google Scholar 

  • Trupiano D, Yordanov Y, Regan S, Meilan R, Tschaplinski T, Scippa GS, Busov V (2013) Identification, characterization of an AP2/ERF transcription factor that promotes adventitious, lateral root formation in Populus. Planta 238:271–282

    Article  CAS  PubMed  Google Scholar 

  • Vielba JM, Díaz-Sala C, Ferro E, Rico S, Lamprecht M, Abarca D, Ballester A, Sánchez C (2011) CsSCL1 is differentially regulated upon maturation in chestnut microshoots and is specifically expressed in rooting-competent cells. Tree Physiol 31:1152–1160

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Du Y, Li Y, Ren D, Song C-P (2010) Hydrogen peroxide-mediated activation of MAP Kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. Plant Cell 22:2981–2998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang M, Zhao Y, Zhang B (2015) Efficient test and visualization of multi-set intersections. Sci Rep 5:16923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang N, Cao P, Xia W, Fang L, Yu H (2017) Identification and characterization of long non-coding RNAs in response to early infection by Melampsora larici-populina using genome-wide high-throughput RNA sequencing. Tree Genet Genomes 13:34

    Article  Google Scholar 

  • Wei M, Liu QG, Wang ZC, Yang JL, Li WL, Chen YX, Lu H, Nie JF, Liu BG, Lv KW, Mao XL, Chen S, Sanders J, Wei HR, Li CH (2020) PuHox52-mediated hierarchical multilayered gene regulatory network promotes adventitious root formation in Populus ussuriensis. New Phytol 228:1369–1385

    Article  CAS  PubMed  Google Scholar 

  • Xia W, Yu H, Cao P, Luo J, Wang N (2017) Identification of TIFY family genes and analysis of their expression profiles in response to phytohormone treatments and Melampsora larici-populina infection in poplar. Front Plant Sci 8:493

    PubMed  PubMed Central  Google Scholar 

  • Xiao ZA, Zhang Y, Liu MF, Zhan C, Yang XQ, Nvsvrot T, Yan ZG, Wang N (2020) Coexpression analysis of a large-scale transcriptome identified a calmodulin-like protein regulating the development of adventitious roots in poplar. Tree Physiol 40:1405–1419

    Article  CAS  PubMed  Google Scholar 

  • Xu L (2018) De novo root regeneration from leaf explants: wounding, auxin, and cell fate transition. Curr Opin Plant Biol 41:39–45

    Article  CAS  PubMed  Google Scholar 

  • Xu M, Xie W, Huang M (2012) Overexpression of PeRHD3 alters the root architecture in Populus. Biochem Bioph Res Co 424:239–244

    Article  CAS  Google Scholar 

  • Xu M, Xie W, Huang M (2015) Two WUSCHEL-related HOMEOBOX genes, PeWOX11a and PeWOX11b, are involved in adventitious root formation of poplar. Physiol Plant 155:446–456

    Article  CAS  PubMed  Google Scholar 

  • Xuan W, Xu S, Li M, Han B, Zhang B, Zhang J, Lin Y, Huang J, Shen W, Cui J (2012) Nitric oxide is involved in hemin-induced cucumber adventitious rooting process. J Plant Physiol 169:1032–1039

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Wu Y, Ma L, Yang Z, Dong Q, Li Q, Ni X, Kudla J, Song C, Guo Y (2019) The Ca2+ sensor SCaBP3/CBL7 modulates plasma membrane H+-ATPase activity and promotes alkali tolerance in Arabidopsis. Plant Cell 31:1367–1384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yordanov YS, Ma C, Yordanova E, Meilan R, Strauss SH, Busov VB (2017) BIG LEAF is a regulator of organ size and adventitious root formation in poplar. PLoS ONE 12:e0180527

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yu G, Wang L-G, Han Y, He Q-Y (2012) clusterProfiler: an R package for comparing biological themes among gene clusters. Omics J Integr Biol 16:284–287

    Article  CAS  Google Scholar 

  • Zhang S, Zhao Z, Zhang L, Zhou Q (2015) Comparative proteomic analysis of tetraploid black locust (Robinia pseudoacacia L.) cuttings in different phases of adventitious root development. Trees 29:367–384

    Article  Google Scholar 

  • Zhang Y, Xiao ZA, Zhan C, Liu M, Xia W, Wang N (2019) Comprehensive analysis of dynamic gene expression and investigation of the roles of hydrogen peroxide during adventitious rooting in poplar. BMC Plant Biol 19:99

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Yang X, Cao P, Xiao Z, Zhan C, Liu M, Nvsvrot T, Wang N (2020) The bZIP53-IAA4 module negatively regulates adventitious root development in poplar. J Exp Bot 71:3485–3498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao X, Zhao X-W, He H, Wang Y-X, Zhang X (2010) Mechanisms of extracellular NO and Ca2+ regulating the growth of wheat seedling roots. Journal Plant Biol 53:275–281

    Article  CAS  Google Scholar 

  • Zhao X, Wang Y-L, Qiao X-R, Wang J, Wang L-D, Xu C-S, Zhang X (2013) Phototropins function in high-intensity blue light-induced hypocotyl phototropism in Arabidopsis by altering cytosolic calcium. Plant Physiol 162:1539–1551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou J-J, Luo J (2018) The PIN-FORMED auxin efflux carriers in plants. Int J Mol Sci 19:2759

    Article  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

This Project was financially supported by the National Natural Science Foundation of China (NSFC accession No. 31901282), and the Fundamental Research Funds for the Central Universities (No. 2662019PY047).

Author information

Authors and Affiliations

Authors

Contributions

J. Luo and N. Wang designed experiments; J. Luo and T. Nvsvrot carried out experiments; J. Luo and N. Wang conducted the bioinformation analysis; J. Luo and N. Wang wrote and revised the manuscript; N. Wang supervised the entire work.

Corresponding author

Correspondence to Nian Wang.

Ethics declarations

Conflict of interest

There are no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PPTX 22813 kb)

Supplementary file2 (XLSX 2010 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Luo, J., Nvsvrot, T. & Wang, N. Comparative transcriptomic analysis uncovers conserved pathways involved in adventitious root formation in poplar. Physiol Mol Biol Plants 27, 1903–1918 (2021). https://doi.org/10.1007/s12298-021-01054-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12298-021-01054-7

Keywords

Navigation