Abstract
Taxus cuspidata S. et Z is a perennial tree with significant economic and medicinal values. T. cuspidata propagation using cuttings is one of the most efficient approaches to solve its propagation material production on a larger scale. Its adventitious roots play a crucial role in the hardwood cutting propagation. To understand the molecular mechanisms involved in T. cuspidata adventitious root development and thus improve the effectiveness of propagation techniques, we investigated the optimal exogenous hormone applications that can rapidly induce adventitious roots in T. cuspidata hardwood cuttings. The best rooting responses were observed in cuttings treated with indole butyric acid (IBA). Moreover, biochemical and molecular profiling analyses of cuttings treated with different IBA concentrations were carried out. Peroxidase and polyphenol oxidase activities consistently increased with IBA concentration increase, except for a decrease observed at IBA150. Indole-3-acetic acid, gibberellin, and ethylene concentrations were significantly higher in all IBA-treated samples compared with the control group. Comparative transcriptome analysis revealed thousands of differentially expressed genes among the four samples (IBA0, IBA50, IBA100, and IBA150) evaluated. Most differentially expressed genes were assigned to phytohormone signaling pathways and sugar metabolism. The AP2/ERF, bHLH, and MYB transcription factor families and genes involved in root development and cell division were also overrepresented during adventitious root formation. This study provides insights into establishing improved asexual propagation protocols and elucidating into the molecular mechanisms underlying root development in T. cuspidata hardwood cuttings.
Similar content being viewed by others
Data availability
RNA-Seq raw data from four samples were deposited in the National Center for Biotechnology Information (NCBI) under the accession number PRJNA797697.
Abbreviations
- ARs:
-
Adventitious roots
- NAA:
-
Naphthalene acetic acid
- IAA:
-
Indole acetic acid
- CK:
-
Cytokinins
- GA:
-
Gibberellic acid
- JA:
-
Jasmonic acid
- ETH:
-
Ethylene
- POD:
-
Peroxidase
- IAAO:
-
Indoleacetic acid oxidase
- PPO:
-
Polyphenol oxidase
- KEGG:
-
Kyoto Encyclopedia of Genes and Genomes
- qRT-PCR:
-
Quantitative real-time polymerase chain reaction
- TFs:
-
Transcription factors
References
An H, Meng J, Xu F, Jiang S, Wang X, Shi C, Zhou B, Luo J, Zhang X (2018) Rooting ability of hardwood cuttings in highbush blueberry (Vaccinium corymbosum L.) using different indole-butyric acid concentrations. HortScience 54(2):194–199. https://doi.org/10.21273/HORTSCI13691-18
An H, Zhang J, Xu F, Jiang S, Zhang X (2020) Transcriptomic profiling and discovery of key genes involved in adventitious root formation from green cuttings of highbush blueberry (Vaccinium corymbosum L.). BMC Plant Biol 20(1):1–14. https://doi.org/10.1186/s12870-020-02398-0
Bai X, Todd CD, Desikan R, Yang Y, Hu X (2012) N-3-oxo-decanoyl-l-homoserine-lactone activates auxin-induced adventitious root formation via hydrogen peroxide-and nitric oxide-dependent cyclic GMP signaling in mung bean. Plant Physiol 158(2):725–736. https://doi.org/10.1104/pp.111.185769
Bassuk NL, Hunter L, Howard B (1981) The apparent involvement of polyphenol oxidase and phloridzin in the production of apple rooting cofactors. J Hortic Sci 56(4):313–322. https://doi.org/10.1080/00221589.1981.11515007
Bellini C, Pacurar DI, Perrone I (2014) Adventitious roots and lateral roots: similarities and differences. Annu Rev Plant Biol 65:639–666. https://doi.org/10.1146/annurev-arplant-050213-035645
Cai Z, Li C-F, Han F, Liu C, Zhang A, Hsu C-C, Peng D, Zhang X, Jin G, Rezaeian A-H (2020) Phosphorylation of PDHA by AMPK drives TCA cycle to promote cancer metastasis. Mol Cell 80(2):263–278. https://doi.org/10.1016/j.molcel.2020.09.018
Cai K, Liu H, Chen S, Liu Y, Zhao X, Chen S (2021a) Genome-wide identification and analysis of class III peroxidases in Betula pendula. BMC Genomics 22(1):1–19. https://doi.org/10.1186/s12864-021-07622-1
Cai K, Zhou X, Li X, Kang Y, Yang X, Cui Y, Li G, Pei X, Zhao X (2021) Insight into the multiple branches’ traits of a mutant in Larix olgensis by morphological, cytological and transcriptional analyses. Front Plant Sci. https://doi.org/10.3389/fpls.2021b.787661
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(11):1–16. https://doi.org/10.1007/s11738-018-2772-y
Chang Y, Huh W-K (2018) Ksp1-dependent phosphorylation of eIF4G modulates post-transcriptional regulation of specific mRNAs under glucose deprivation conditions. Nucleic Acids Res 46(6):3047–3060. https://doi.org/10.1093/nar/gky097
Chee PP (1995) Stimulation of adventitious rooting of Taxus species by thiamine. Plant Cell Rep 14(12):753–757. https://doi.org/10.1007/BF00232916
Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34(17):i884–i890. https://doi.org/10.1093/bioinformatics/bty560
Cheng J, Wang X, Liu X, Zhu X, Li Z, Chu H, Wang Q, Lou Q, Cai B, Yang Y (2021) Chromosome-level genome of Himalayan yew provides insights into the origin and evolution of the paclitaxel biosynthetic pathway. Mol Plant 14(7):1199–1209. https://doi.org/10.1016/j.molp.2021.04.015
Concellon A, Anón MC, Chaves AR (2004) Characterization and changes in polyphenol oxidase from eggplant fruit (Solanum melongena L.) during storage at low temperature. Food Chem 88(1):17–24. https://doi.org/10.1016/j.foodchem.2004.01.017
Cooper WC (1936) Transport of root-forming hormone in woody cuttings. Plant Physiol 11(4):779. https://doi.org/10.1104/pp.11.4.779
Cvrčková F, Bezvoda R, Žárský V (2010) Computational identification of root hair-specific genes in Arabidopsis. Plant Sign Beha 5(11):1407–1418. https://doi.org/10.4161/psb.5.11.13358
Damiano C, Padro MDA, Frattarelli A (2008) Propagation and establishment in vitro of myrtle (Myrtus communis L.), pomegranate (Punica granatum L.) and mulberry (Morus alba L.). Prop Orna Plants 8(1):3–8
Dave A, Vaistij FE, Gilday AD, Penfield SD, Graham IA (2016) Regulation of Arabidopsis thaliana seed dormancy and germination by 12-oxo-phytodienoic acid. J Exp Bot 67(8):2277–2284. https://doi.org/10.1093/jxb/erw028
Debi BR, Taketa S, Ichii M (2005) Cytokinin inhibits lateral root initiation but stimulates lateral root elongation in rice (Oryza sativa). J Plant Physiol 162(5):507–515. https://doi.org/10.1016/j.jplph.2004.08.007
Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143(4):1789–1801. https://doi.org/10.1104/pp.106.093971
Devi J, Kaur E, Swarnkar MK, Acharya V, Bhushan S (2021) De novo transcriptome analysis provides insights into formation of in vitro adventitious root from leaf explants of Arnebia euchroma. BMC Plant Biol 21(1):1–16. https://doi.org/10.1186/s12870-021-03172-6
Ding Y, Kalo P, Yendrek C, Sun J, Liang Y, Marsh JF, Harris JM, Oldroyd GE (2008) Abscisic acid coordinates nod factor and cytokinin signaling during the regulation of nodulation in Medicago truncatula. Plant C 20(10):2681–2695. https://doi.org/10.1105/tpc.108.061739
Druege U, Franken P, Hajirezaei MR (2016) Plant hormone homeostasis, signaling, and function during adventitious root formation in cuttings. Front Plant Sci 7:381. https://doi.org/10.3389/fpls.2016.00381
Druege U, Hilo A, Pérez-Pérez JM, Klopotek Y, Acosta M, Shahinnia F, Zerche S, Franken P, Hajirezaei MR (2019) Molecular and physiological control of adventitious rooting in cuttings: phytohormone action meets resource allocation. Ann Bot 123(6):929–949. https://doi.org/10.1093/aob/mcy234
Duclercq J, Sangwan-Norreel B, Catterou M, Sangwan RS (2011) De novo shoot organogenesis: from art to science. Trends Plant Sci 16(11):597–606. https://doi.org/10.1016/j.tplants.2011.08.004
Efroni I, Mello A, Nawy T, Ip P-L, Rahni R, DelRose N, Powers A, Satija R, Birnbaum KD (2016) Root regeneration triggers an embryo-like sequence guided by hormonal interactions. Cell 165(7):1721–1733
Fujii H, Verslues PE, Zhu J-K (2007) Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant C 19(2):485–494. https://doi.org/10.1105/tpc.106.048538
Geiss G, Gutierrez L, Bellini C (2009) Adventitious root formation: new insights and perspectives. Annu Plant Rev 37(1):127–156
Guan L, Tayengwa R, Cheng ZM, Peer WA, Murphy AS, Zhao M (2019) Auxin regulates adventitious root formation in tomato cuttings. BMC Plant Biol 19(1):1–16. https://doi.org/10.1186/s12870-019-2002-9
Günes T (2000) Peroxidase and IAA-oxidase activities during rooting in cuttings of threepoplar species. Turkish J Bot 24(2):97–102
Gutierrez L, Mongelard G, Floková K, Păcurar DI, Novák O, Staswick P, Kowalczyk M, Păcurar M, Demailly H, Geiss G (2012) Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant C 24(6):2515–2527. https://doi.org/10.1105/tpc.112.099119
Han H, Sun X, Xie Y, Feng J, Zhang S (2014) Transcriptome and proteome profiling of adventitious root development in hybrid larch (Larix kaempferi × Larix olgensis). BMC Plant Biol 14(1):1–13. https://doi.org/10.1186/s12870-014-0305-4
Heloir M-C, Kevers C, Hausman J-F, Gaspar T (1996) Changes in the concentrations of auxins and polyamines during rooting of in-vitro-propagated walnut shoots. Tree Physiol 16(5):515–519. https://doi.org/10.1093/treephys/16.5.515
Hernandez M, Fernandez-Garcia N, Diaz-Vivancos P, Olmos E (2010) A different role for hydrogen peroxide and the antioxidative system under short and long salt stress in Brassica oleracea roots. J Exp Bot 61(2):521–535. https://doi.org/10.1093/jxb/erp321
Jia K-P, Dickinson AJ, Mi J, Cui G, Xiao TT, Kharbatia NM, Guo X, Sugiono E, Aranda M, Blilou I (2019) Anchorene is a carotenoid-derived regulatory metabolite required for anchor root formation in Arabidopsis. Sci Adv 5(11):6787. https://doi.org/10.1126/sciadv.aaw6787
Jia-Hui LU, Wang CX, Rao SQ, Qin QP (2018) Effect of hormone treatments on rooting of Hydrangea macrophylla under water culture. J Zhe Sci Tech 38:77–80
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357–360. https://doi.org/10.1038/nmeth.3317
Kohanová J, Martinka M, Vaculík M, White PJ, Hauser M-T, Lux A (2018) Root hair abundance impacts cadmium accumulation in Arabidopsis thaliana shoots. Ann Bot 122(5):903–914. https://doi.org/10.1093/aob/mcx220
Kong Q, Ma W, Yang H, Ma G, Mantyla JJ, Christoph B (2017) The Arabidopsis WRINKLED1 transcription factor affects auxin homeostasis in roots. J Exp Bot 16:4627–4634. https://doi.org/10.1093/jxb/erx275
Koyuncu F, Balta F (2004) Adventitious root formation in leaf-bud cuttings of tea (Camellia sinensis L.). Pak J Bot 36(4):763–768
Kromer K, Gamian A (2000) Analysis of soluble carbohydrates, proteins and lipids in shoots of M 7 apple rootstock cultured in vitro during regeneration of adventitious roots. J Plant Physiol 156(5–6):775–782. https://doi.org/10.1016/S0176-1617(00)80247-3
Kuang X, Sun S, Wei J, Li Y, Sun C (2019) Iso-Seq analysis of the Taxus cuspidata transcriptome reveals the complexity of Taxol biosynthesis. BMC Plant Biol 19(1):1–16. https://doi.org/10.1186/s12870-019-1809-8
Kubiasová K, Montesinos JC, Šamajová O, Nisler J, Mik V, Semerádová H, Plíhalová L, Novák O, Marhavý P, Cavallari N (2020) Cytokinin fluoroprobe reveals multiple sites of cytokinin perception at plasma membrane and endoplasmic reticulum. Nat Commu 11(1):1–11. https://doi.org/10.1038/s41467-020-17949-0
Kumari S, Yadav S, Patra D, Singh S, Sarkar AK, Panigrahi KC (2019) Uncovering the molecular signature underlying the light intensity-dependent root development in Arabidopsis thaliana. BMC Genomics 20(1):1–23. https://doi.org/10.1186/s12864-019-5933-5
Kurepin L, Haslam T, Lopez-Villalobos A, Oinam G, Yeung E (2011) Adventitious root formation in ornamental plants: II. The role of plant growth regulators. Prop Orna Plants 11(4):161–171
Laplaze L, Benkova E, Casimiro I, Maes L, Vanneste S, Swarup R, Weijers D, Calvo V, Parizot B, Herrera-Rodriguez MB (2007) Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant C 19(12):3889–3900. https://doi.org/10.1105/tpc.107.055863
Lau S, Jürgens G, De Smet I (2008) The evolving complexity of the auxin pathway. Plant C 20(7):1738–1746. https://doi.org/10.1105/tpc.108.060418
Lei M, Liu Y, Zhang B, Zhao Y, Wang X, Zhou Y, Raghothama KG, Liu D (2011) Genetic and genomic evidence that sucrose is a global regulator of plant responses to phosphate starvation in Arabidopsis. Plant Physiol 156(3):1116–1130. https://doi.org/10.1104/pp.110.171736
Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12(1):1–16. https://doi.org/10.1186/1471-2105-12-323
Li G, Ma J, Tan M, Mao J, An N, Sha G, Zhang D, Zhao C, Han M (2016) Transcriptome analysis reveals the effects of sugar metabolism and auxin and cytokinin signaling pathways on root growth and development of grafted apple. BMC Genomics 17(1):1–17. https://doi.org/10.1186/s12864-016-2484-x
Li K, Liang Y, Xing L, Mao J, Liu Z, Dong F, Meng Y, Han M, Zhao C, Bao L (2018) Transcriptome analysis reveals multiple hormones, wounding and sugar signaling pathways mediate adventitious root formation in apple rootstock. Int J Mol Sci 19(8):2201. https://doi.org/10.3390/ijms19082201
Li Z, Liu C, Zhang Y, Wang B, Ran Q, Zhang J (2019) The bHLH family member ZmPTF1 regulates drought tolerance in maize by promoting root development and abscisic acid synthesis. J Exp Bot 70(19):5471–5486. https://doi.org/10.1093/jxb/erz307
Li A, Lakshmanan P, He W, Tan H, Liu L, Liu H, Liu J, Huang D, Chen Z (2020) Transcriptome profiling provides molecular insights into auxin-induced adventitious root formation in sugarcane (Saccharum spp. interspecific hybrids) Microshoots. Plants 9(8):931. https://doi.org/10.3390/plants9080931
Li X, Mao X, Xu Y, Li Y, Zhao N, Yao J, Dong Y, Tigabu M, Zhao X, Li S (2021) Comparative transcriptomic analysis reveals the coordinated mechanisms of Populus × Canadensis ‘Neva’ leaves in response to cadmium stress. Ecotoxicol Environ Saf 216:112179. https://doi.org/10.1016/j.ecoenv.2021.112179
Liu R, Chen S, Jiang J, Zhu L, Zheng C, Han S, Gu J, Sun J, Li H, Wang H (2013) Proteomic changes in the base of chrysanthemum cuttings during adventitious root formation. BMC Genomics 14(1):1–14. https://doi.org/10.1186/1471-2164-14-919
Liu S, Xuan L, Xu L-A, Huang M, Xu M (2016) Molecular cloning, expression analysis and subcellular localization of four DELLA genes from hybrid poplar. Springerplus 5(1):1–8. https://doi.org/10.1186/s40064-016-2728-x
Liu S, Murtaza A, Liu Y, Hu W, Xu X, Pan S (2018) Catalytic and structural characterization of a browning-related protein in oriental sweet melon (Cucumis melo var. Makuwa Makino). Front Chem 6:354. https://doi.org/10.3389/fchem.2018.00354
Liu Y, Qu J, Zhang L, Xu X, Wei G, Zhao Z, Ren M, Cao M (2019) Identification and characterization of the TCA cycle genes in maize. BMC Plant Biol 19(1):1–16. https://doi.org/10.1186/s12870-019-2213-0
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):1–21. https://doi.org/10.1186/s13059-014-0550-8
Luo J, Nvsvrot T, Wang N (2021) Comparative transcriptomic analysis uncovers conserved pathways involved in adventitious root formation in poplar. Physiol Mol Biol Plants 27(9):1903–1918. https://doi.org/10.1007/s12298-021-01054-7
Ma C, Liang B, Chang B, Yan J, Liu L, Wang Y, Yang Y, Zhao Z (2019) Transcriptome profiling of anthocyanin biosynthesis in the peel of ‘Granny Smith’ apples (Malus domestica) after bag removal. BMC Genomics 20(1):1–18. https://doi.org/10.1186/s12864-019-5730-1
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(3):372–384. https://doi.org/10.1111/tpj.12478
Muñoz-Gutiérrez L, Vargas-Hernández JJ, López-Upton J, Soto-Hernández M (2009) Effect of cutting age and substrate temperature on rooting of Taxus globosa. New Fore 38(2):187–196. https://doi.org/10.1007/s11056-009-9139-6
Muzammil S, Shrestha A, Dadshani S, Pillen K, Siddique S, Léon J, Naz AA (2018) An ancestral allele of pyrroline-5-carboxylate synthase1 promotes proline accumulation and drought adaptation in cultivated barley. Plant Physiol 178(2):771–782. https://doi.org/10.1104/pp.18.00169
Nickel KS, Cunningham B (1969) Improved peroxidase assay method using leuco 2,3′,6-trichloroindophenol and application to comparative measurements of peroxidatic catalysis. Anal Biochem 27(2):292–299. https://doi.org/10.1016/0003-2697(69)90035-9
Okuma N, Soyano T, Suzaki T, Kawaguchi M (2020) MIR2111-5 locus and shoot-accumulated mature miR2111 systemically enhance nodulation depending on HAR1 in Lotus japonicus. Nat Commu 11(1):1–13. https://doi.org/10.1038/s41467-020-19037-9
Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant C 19(1):118–130. https://doi.org/10.1105/tpc.106.047761
OuYang F, Wang J, Li Y (2015) Effects of cutting size and exogenous hormone treatment on rooting of shoot cuttings in Norway spruce [Picea abies (L.) Karst.]. New Fore 46(1):91–105. https://doi.org/10.1007/s11056-014-9449-1
Pacurar DI, Pacurar ML, Bussell JD, Schwambach J, Pop TI, Kowalczyk M, Gutierrez L, Cavel E, Chaabouni S, Ljung K (2014) Identification of new adventitious rooting mutants amongst suppressors of the Arabidopsis thaliana superroot2 mutation. J Exp Bot 65(6):1605–1618. https://doi.org/10.1093/jxb/eru026
Poupart J, Rashotte AM, Muday GK, Waddell CS (2005) The rib1 mutant of Arabidopsis has alterations in indole-3-butyric acid transport, hypocotyl elongation, and root architecture. Plant Physiol 139(3):1460–1471. https://doi.org/10.1104/pp.105.067967
Qu B, He X, Wang J, Zhao Y, Teng W, Shao A, Zhao X, Ma W, Wang J, Li B (2015) A wheat CCAAT box-binding transcription factor increases the grain yield of wheat with less fertilizer input. Plant Physiol 167(2):411–423. https://doi.org/10.1104/pp.114.246959
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(1):1–14. https://doi.org/10.1186/s12864-017-3554-4
Ragonezi C, Klimaszewska K, Castro MR, Lima M, de Oliveira P, Zavattieri MA (2010) Adventitious rooting of conifers: influence of physical and chemical factors. Trees 24(6):975–992. https://doi.org/10.1007/s00468-010-0488-8
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(2):759–771. https://doi.org/10.1104/pp.109.137505
Ranjan A, Perrone I, Alallaq S, Singh R, Rigal A, Brunoni F, Chitarra W, Guinet F, Kohler A, Martin F (2022) Molecular basis of differential adventitious rooting competence in poplar genotypes. J Exp Bot 73(12):4046–4064. https://doi.org/10.1093/jxb/erac126
Raya-González J, Oropeza-Aburto A, López-Bucio JS, Guevara-García ÁA, De Veylder L, López-Bucio J, Herrera-Estrella L (2018) MEDIATOR18 influences Arabidopsis root architecture, represses auxin signaling and is a critical factor for cell viability in root meristems. Plant J 96(5):895–909. https://doi.org/10.1111/tpj.14114
Ribeiro CL, Silva CM, Drost DR, Novaes E, Novaes CR, 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(1):1–11. https://doi.org/10.1186/s12870-016-0753-0
Ricci A, Rolli E, Dramis L, Diaz-Sala C (2008) N, N′-bis-(2,3-Methylenedioxyphenyl) urea and N, N′-bis-(3,4-methylenedioxyphenyl) urea enhance adventitious rooting in Pinus radiata and affect expression of genes induced during adventitious rooting in the presence of exogenous auxin. Plant Sci 175(3):356–363. https://doi.org/10.1016/j.plantsci.2008.05.009
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(4):1996–2006. https://doi.org/10.1104/pp.112.204453
Sandhu M, Wani SH, Jiménez VM (2018) In vitro propagation of bamboo species through axillary shoot proliferation: a review. Plant Cell Tissue Organ Culture 132(1):27–53. https://doi.org/10.1007/s11240-017-1325-1
Sarli S, Kalani MR, Moradi A (2020) A potent and safer anticancer and antibacterial taxus-based green synthesized silver nanoparticle. Int J Nano 15:3791. https://doi.org/10.2147/IJN.S251174
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat pro 3(6):1101–1108. https://doi.org/10.1038/nprot.2008.73
Sedira M, Butler E, Gallagher T, Welander M (2005) Verification of auxin-induced gene expression during adventitious rooting in rolB-transformed and untransformed apple Jork 9. Plant Sci 168(5):1193–1198. https://doi.org/10.1016/j.plantsci.2004.12.017
Shang C, Yang H, Ma S, Shen Q, Liu L, Hou C, Cao X, Cheng J (2019) Physiological and transcriptomic changes during the early phases of adventitious root formation in mulberry stem hardwood cuttings. Int J Mol Sci 20(15):3707. https://doi.org/10.3390/ijms20153707
Sharma U, Kataria V, Shekhawat N (2018) Aeroponics for adventitious rhizogenesis in evergreen haloxeric tree Tamarix aphylla (L.) Karst.: Influence of exogenous auxins and cutting type. Physiol Mol Plant Pathol 24(1):167–174. https://doi.org/10.1007/s12298-017-0493-0
Shi W, Li H, Liu T, Polle A, PENG CH, LUO ZB, (2015) Exogenous abscisic acid alleviates zinc uptake and accumulation in Populus × Canescens exposed to excess zinc. Plant Cell Environ 38(1):207–223. https://doi.org/10.1111/pce.12434
Singh D, Debnath P, Roohi APS, Sane VA (2020) Expression of the tomato WRKY gene, SlWRKY23, alters root sensitivity to ethylene, auxin and JA and affects aerial architecture in transgenic Arabidopsis. Physiol Mol Plant Pathol 26(6):1187. https://doi.org/10.1007/s12298-020-00820-3
Smeekens S, Ma J, Hanson J, Rolland F (2010) Sugar signals and molecular networks controlling plant growth. Curr Opin Plant Biol 13(3):273–278. https://doi.org/10.1016/j.pbi.2009.12.002
Takahashi H, Xiaohua Q, Shimamura S, Yanagawa A, Hiraga S, Nakazono M (2018) Sucrose supply from leaves is required for aerenchymatous phellem formation in hypocotyl of soybean under waterlogged conditions. Ann Bot 121(4):723–732. https://doi.org/10.1093/aob/mcx205
Tata SK, Jung J, Kim YH, Choi JY, Jung JY, Lee IJ, Shin JS, Ryu SB (2016) Heterologous expression of chloroplast-localized geranylgeranyl pyrophosphate synthase confers fast plant growth, early flowering and increased seed yield. Plant Biotechnol J 14(1):29–39. https://doi.org/10.1111/pbi.12333
Trujillo-Hernandez JA, Bariat L, Enders TA, Strader LC, Reichheld J-P, Belin C (2020) A glutathione-dependent control of the indole butyric acid pathway supports Arabidopsis root system adaptation to phosphate deprivation. J Exp Bot 71(16):4843–4857. https://doi.org/10.1093/jxb/eraa195
Tsukagoshi H, Saijo T, Shibata D, Morikami A, Nakamura K (2005) Analysis of a sugar response mutant of Arabidopsis identified a novel B3 domain protein that functions as an active transcriptional repressor. Plant Physiol 138(2):675–685. https://doi.org/10.1104/pp.104.057752
Tucker ML, Xue P, Yang R (2010) 1-Aminocyclopropane-1-carboxylic acid (ACC) concentration and ACC synthase expression in soybean roots, root tips, and soybean cyst nematode (Heterodera glycines)-infected roots. J Exp Bot 61(2):463–472. https://doi.org/10.1093/jxb/erp317
Verma VK, Pandey A, Jha AK, Ngachan S (2017) Genetic characterization of chayote [Sechium edule (Jacq.) Swartz.] landraces of North Eastern Hills of India and conservation measure. Physiol Mol Biol Plants 23(4):911–924. https://doi.org/10.1007/s12298-017-0478-z
Wang S-J, Yuan L-N, Liu L-L, Niu H-W, Zhang J-X, Wang Z-Y (2012) Study on rooting agents used in micro-cutting of Taxus cuspidata World Auto Cong 2012. IEEE, Piscataway, pp 1–4
Wang P, Ma L, Li Y, Sa W, Li L, Yang R, Ma Y, Wang Q (2016) Transcriptome profiling of indole-3-butyric acid-induced adventitious root formation in softwood cuttings of the Catalpa bungei variety ‘YU-1’at different developmental stages. Genes Gen 38(2):145–162. https://doi.org/10.1007/s13258-015-0352-8
Wang Z, Hua J, Yin Y, Gu C, Yu C, Shi Q, Guo J, Xuan L, Yu F (2019) An integrated transcriptome and proteome analysis reveals putative regulators of adventitious root formation in Taxodium ‘Zhongshanshan.’ Int J Mol Sci 20(5):1225. https://doi.org/10.3390/ijms20051225
Waszczak C, Kerchev PI, Mühlenbock P, Hoeberichts FA, Van Der Kelen K, Mhamdi A, Willems P, Denecker J, Kumpf RP, Noctor G (2016) SHORT-ROOT deficiency alleviates the cell death phenotype of the Arabidopsis catalase2 mutant under photorespiration-promoting conditions. Plant C 28(8):1844–1859. https://doi.org/10.1105/tpc.16.00038
Wei K, Ruan L, Wang L, Cheng H (2019) Auxin-induced adventitious root formation in nodal cuttings of Camellia sinensis. Int J Mol Sci 20(19):4817. https://doi.org/10.3390/ijms20194817
Xuan W, Zhu F-Y, Xu S, Huang B-K, Ling T-F, Qi J-Y, Ye M-B, Shen W-B (2008) The heme oxygenase/carbon monoxide system is involved in the auxin-induced cucumber adventitious rooting process. Plant Physiol 148(2):881–893. https://doi.org/10.1104/pp.108.125567
Yang J, Zhang J, Wang Z, Zhu Q, Wang W (2001) Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiol 127(1):315–323. https://doi.org/10.1104/pp.127.1.315
Yang G, Chen S, Wang S, Liu G, Li H, Huang H, Jiang J (2015) BpGH3.5, an early auxin-response gene, regulates root elongation in Betula platyphylla × Betula pendula. Plant Cell Tiss Org Cult 120(1):239–250. https://doi.org/10.1007/s11240-014-0599-9
Yang H, Klopotek Y, Hajirezaei MR, Zerche S, Franken P, Druege U (2019) Role of auxin homeostasis and response in nitrogen limitation and dark stimulation of adventitious root formation in petunia cuttings. Ann Bot 124(6):1053–1066. https://doi.org/10.1093/aob/mcz095
Yilmaz H, Taşkin T, Otludil B (2003) Polyphenol oxidase activity during rooting in cuttings of grape (Vitis vinifera L.) varieties. Turkish J Bot 27(6):495–498
Zeng Y-h, Zhang Y-p, Xiang J, Hui W, Chen H-z, Zhang Y-k, Zhu D-f (2016) Effects of chilling tolerance induced by spermidine pretreatment on antioxidative activity, endogenous hormones and ultrastructure of indica-japonica hybrid rice seedlings. J Integ Agr 15(2):295–308. https://doi.org/10.1016/S2095-3119(15)61051-6
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(2):367–384. https://doi.org/10.1007/s00468-014-1116-9
Zhang Y, Nasser V, Pisanty O, Omary M, Wulff N, Di Donato M, Tal I, Hauser F, Hao P, Roth O (2018) A transportome-scale amiRNA-based screen identifies redundant roles of Arabidopsis ABCB6 and ABCB20 in auxin transport. Nat Commu 9(1):1–12. https://doi.org/10.1038/s41467-018-06410-y
Zhang K, Zhao L, Yang X, Li M, Sun J, Wang K, Li Y, Zheng Y, Yao Y, Li W (2019) GmRAV1 regulates regeneration of roots and adventitious buds by the cytokinin signaling pathway in Arabidopsis and soybean. Physiol Plant 165(4):814–829. https://doi.org/10.1111/ppl.12788
Zhang S, Lu X, Zheng T, Guo X, Chen Q, Tang Z (2021) Investigation of bioactivities of Taxus chinensis, Taxus cuspidata, and Taxus × media by gas chromatography-mass spectrometry. Open Life Sci 16(1):287–296. https://doi.org/10.1515/biol-2021-0032
Zhao Y, Hu Y, Dai M, Huang L, Zhou D-X (2009) The WUSCHEL-related homeobox gene WOX11 is required to activate shoot-borne crown root development in rice. Plant C 21(3):736–748. https://doi.org/10.1105/tpc.108.061655
Zhou X, Li Q, Chen X, Liu J, Zhang Q, Liu Y, Liu K, Xu J (2011) The Arabidopsis RETARDED ROOT GROWTH gene encodes a mitochondria-localized protein that is required for cell division in the root meristem. Plant Physiol 157(4):1793–1804. https://doi.org/10.1104/pp.111.185827
Acknowledgements
Thanks to the members of the State Key Laboratory of Tree Genetics and Breeding for their assistance during laboratory work and for fruitful discussions, and we thank Bullet Edits Limited for the linguistic editing and proofreading of the manuscript.
Funding
This work was supported by the Scientific Research Start-up Funds of Jilin Agricultural University (No. 2021002) and the Demonstration and Promotion Project of Selection Breeding and Efficient Cultivation Technology for Taxus cuspidata (GA19B201-4).
Author information
Authors and Affiliations
Contributions
KWC was a major contributor in writing the manuscript. DDZ and XL drafted the manuscript and substantially revised it. QHZ, LPJ, YXL, RXS and SQS analyzed the data and made the figures. RXG, RH and XQH participated in RNA extraction and performed qRT-PCR assay. XDZ participated in the revision of the manuscript. XNP and XYZ conceived of the study, participated in its design and data interpretation, and revised the manuscript critically. The authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Competing interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Additional information
Communicated by Zsófia Bánfalvi.
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.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Cai, K., Zhang, D., Li, X. et al. Exogenous phytohormone application and transcriptome analysis provides insights for adventitious root formation in Taxus cuspidata S. et Z. Plant Growth Regul 100, 33–53 (2023). https://doi.org/10.1007/s10725-022-00934-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-022-00934-6