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Comparative transcriptome reveals circadian and hormonal control of adventitious rooting in mulberry hardwood cuttings

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Abstract

Adventitious rooting derived from the parenchyma cells of vascular cambium is a highly efficient rooting type for cutting propagation of woody species. To unravel the molecular mechanisms underlying this distinct rooting process in mulberry stem hardwood cuttings, RNA-seq approach was adopted to perform wide transcriptional expression profiles of three stages characterized by initial excision (stage 1), root primordia induction (stage 2) and emergence of adventitious roots (stage 3). Compared to the former two stages, stage 3 had the most expressed genes (19,987) to establish functionally mature adventitious roots. In contrast, differentially expressed genes (DEGs) identified in stage 1 vs stage 2 comparison group were over threefold higher than stage 2 vs stage 3 comparison group (8930 vs 2739), suggesting a drastic transcriptional activation of genes involved in root primordia induction. GO and KEGG enrichment analysis of the DEGs showed that circadian rhythm-plant pathway was significantly enriched in response to environmental and endogenous changes in stage 2, whereas plant hormones including auxin, ethylene and cytokinin coordinately participated in the formation of adventitious roots in a stage-specific manner via an extensive and delicate regulation of their biosynthesis and signal transduction. Among which, several sets of genes relevant to circadian clock and hormone biosynthesis and signaling are speculated to potentially associated with the induction and differentiation of parenchyma cell initiated adventitious rooting. These findings will enrich our understandings to the mechanisms of adventitious rooting in mulberry, and provide theoretical support for the development of rooting techniques for other woody crops.

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References

  • Agullo-Anton MA, Ferrandez-Ayela A, Fernandez-Garcia N, Nicolas C, Albacete A, Perez-Alfocea F, Sanchez-Bravo J, Perez-Perez 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  CAS  Google Scholar 

  • Atamian HS, Harmer SL (2016) Circadian regulation of hormone signaling and plant physiology. Plant Mol Biol 91:691–702

    Article  CAS  Google Scholar 

  • Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7:986–995

    Article  CAS  Google Scholar 

  • Baranwal VK, Negi N, Khurana P (2017) Auxin response factor genes repertoire in mulberry: identification and structural functional and evolutionary analyses. Genes 8:E202

    Article  Google Scholar 

  • Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188

    Article  Google Scholar 

  • Bie B, Sun J, Pan J, He H, Cai R (2014) Ectopic expression of CsCTR1 a cucumber CTR-like gene attenuates constitutive ethylene signaling in an Arabidopsis ctr1-1 mutant and expression pattern analysis of CsCTR1 in cucumber (Cucumis sativus). Int J Mol Sci 15:16331–16350

    Article  Google Scholar 

  • Cheng J, Huang P, Du W, Zhang G, Fang R, Liu Y, Chai J (2015) A method of breeding seedlings using multilayer heating boxes. China Patent No. ZL2015100615960

  • De Klerk GJ, Guan HY, 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 

  • Della Rovere F, Fattorini L, D’Angeli S, Veloccia A, Falasca G, Altamura MM (2013) Auxin and cytokinin control formation of the quiescent centre in the adventitious root apex of arabidopsis. Ann Bot 112:1395–1407

    Article  CAS  Google Scholar 

  • Druege U, Franken P, Lischewski S, Ahkami AH, Zerche S, Hause B, Hajirezaei MR (2014) Transcriptomic analysis reveals ethylene as stimulator and auxin as regulator of adventitious root formation in petunia cuttings. Front Plant Sci 5:494. https://doi.org/10.3389/fpls.2014.00494

    Article  PubMed  PubMed Central  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. https://doi.org/10.3389/fpls.2016.00381

    Article  PubMed  PubMed Central  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  Google Scholar 

  • Ford B, Deng WW, Clausen J, Oliver S, Boden S, Hemming M, Trevaskis B (2016) Barley (Hordeum vulgare) circadian clock genes can respond rapidly to temperature in an EARLY FLOWERING 3-dependent manner. J Exp Bot 67:5517–5528

    Article  CAS  Google Scholar 

  • Guimaraes LL, Toledo MS, Ferreira FAS, Straus AH, Takahashi HK (2014) Structural diversity and biological significance of glycosphingolipids in pathogenic and opportunistic fungi. Front Cell Infect Microbiol 4:138. ​https://doi.org/10.3389/fcimb.2014.00138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gutierrez L, Mongelard G, Flokova K, Pacurar DI, Novak O, Staswick P, Kowalczyk M, Pacurar M, Demailly H, Geiss G, Bellini C (2012) Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell 24:2515–2527

    Article  CAS  Google Scholar 

  • He N, Zhang C, Qi X, Zhao S, Tao Y, Yang G, Lee TH, Wang X, Cai Q, Li D (2013) Draft genome sequence of the mulberry tree Morus notabilis. Nat Commun 4:2445–2445

    Article  Google Scholar 

  • Ito S, Nakamichi N, Matsushika A, Fujimori T, Yamashino T, Mizuno T (2005) Molecular dissection of the promoter of the light-induced and circadian-controlled APRR9 gene encoding a clock-associated component of Arabidopsis thaliana. Biosci Biotechnol Biochem 69:382–390

    Article  CAS  Google Scholar 

  • James AB, Monreal JA, Nimmo GA, Kelly CL, Herzyk P, Jenkins GI, Nimmo HG (2008) The circadian clock in Arabidopsis roots is a simplified slave version of the clock in shoots. Science 322:1832–1835

    Article  CAS  Google Scholar 

  • Kant S, Rothstein SJ (2009) SAUR39, a small auxin-up RNA gene, acts as a negative regulator of auxin synthesis and transport in rice. Plant Physiol 151:691–701

    Article  CAS  Google Scholar 

  • Kushwah S, Jones AM, Laxmi A (2011) Cytokinin interplay with ethylene auxin and glucose signaling controls Arabidopsis seedling root directional growth. Plant Physiol 156:1851–1866

    Article  CAS  Google Scholar 

  • Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:1–10

    Article  Google Scholar 

  • Lau S, Juergens G, De Smet I (2008) The evolving complexity of the auxin pathway. Plant Cell 20:1738–1746

    Article  CAS  Google Scholar 

  • Lee Y, Lee DE, Lee HS, Kim SK, Lee WS, Kim SH, Kim MW (2011) Influence of auxins cytokinins and nitrogen on production of rutin from callus and adventitious roots of the white mulberry tree (Morus alba L). Plant Cell Tissue Org Cult 105:9–19

    Article  CAS  Google Scholar 

  • Legris M, Nieto C, Sellaro R, Prat S, Casal JJ (2017) Perception and signalling of light and temperature cues in plants. Plant J 90:683–697

    Article  CAS  Google Scholar 

  • Lewis DR, Negi S, Sukumar P, Muday GK (2011) Ethylene inhibits lateral root development increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers. Development 138:3485–3495

    Article  CAS  Google Scholar 

  • Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25:1966–1967

    Article  CAS  Google Scholar 

  • Li T, Qi X, Zeng Q, Xiang Z, He N (2014) MorusDB: a resource for mulberry genomics and genome biology. In: Database, vol 2014. https://doi.org/10.1093/database/bau054

  • Li XW, Jiang J, Zhang LP, Yu Y, Ye ZW, Wang XM, Zhou JY, Chai ML, Zhang HQ, Arús P (2015a) Identification of volatile and softening-related genes using digital gene expression profiles in melting peach. Tree Genet Genomes 11:71

    Article  Google Scholar 

  • Li YH, Zhang W, Li Y (2015b) Transcriptomic analysis of flower blooming in Jasminum sambac through De Novo RNA sequencing. Molecules 20:10734–10747

    Article  CAS  Google Scholar 

  • Liu M, Sun L, Zhang X, Nie H, Cheng J (2011) Physiological and biochemical analysis of mulberry hardwood cuttings rooting process. China Seric 1:9–14

    CAS  Google Scholar 

  • Liu J, Ming Y, Cheng Y, Zhang Y, Xing J, Sun Y (2017) Comparative transcriptome analysis reveal candidate genes potentially involved in regulation of primocane apex rooting in raspberry (Rubus spp). Front Plant Sci 8:1036. https://doi.org/10.3389/fpls.2017.01036

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Markakis MN, Boron AK, Van Loock B, Saini K, Cirera S, Verbelen JP, Vissenberg K (2013) Characterization of a small auxin-up RNA (SAUR)-like gene involved in Arabidopsis thaliana development. PLoS One 8(11):e82596. https://doi.org/10.1371/journal.pone.0082596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minibayeva F, Kolesnikov O, Chasov A, Beckett RP, Luthje S, Vylegzhanina N, Buck F, Bottger M (2009) Wound-induced apoplastic peroxidase activities: their roles in the production and detoxification of reactive oxygen species. Plant Cell Environ 32:497–508

    Article  CAS  Google Scholar 

  • Mizoguchi T, Wheatley K, Hanzawa Y, Wright L, Mizoguchi M, Song H-R, Carré IA, Coupland G (2002) LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev Cell 2:629–641

    Article  CAS  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 11:1–11

    Article  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  CAS  Google Scholar 

  • Mortimer JC, Yu X, Albrecht S, Sicilia F, Huichalaf M, Ampuero D, Michaelson LV, Murphy AM, Matsunaga T, Kurz S, Stephens E, Baldwin TC, Ishii T, Napier JA, Weber APM, Handford MG, Dupree P (2013) Abnormal glycosphingolipid mannosylation triggers salicylic acid-mediated responses in Arabidopsis. Plant Cell 25:1881–1894

    Article  CAS  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  Google Scholar 

  • Press MO, Lanctot A, Queitsch C (2016) PIF4 and ELF3 act independently in Arabidopsis thaliana thermoresponsive flowering. PLoS One 11(8): e0161791. https://doi.org/10.1371/journal.pone.0161791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Randall RS, Miyashima S, Blomster T, Zhang J, Elo A, Karlberg A, Immanen J, Nieminen K, Lee JY, Kakimoto T, Blajecka K, Melnyk CW, Alcasabas A, Forzani C, Matsumoto-Kitano M, Maehoenen AP, Bhalerao R, Dewitte W, Helariutta Y, Murray JAH (2015) AINTEGUMENTA and the d-type cyclin CYCD3;1 regulate root secondary growth and respond to cytokinins. Biol Open 4:1229–1236

    Article  CAS  Google Scholar 

  • Rhee Y, Hwang K, Cho S, Lee M, Kil EJ, Choi S, Hahn BS, Kim D, Auh CK, Lee S (2016) Expression analysis of d-type cyclin in potato (Solanum tuberosum L) under different culture conditions. Acta Physiol Plant 38:36. https://doi.org/10.1007/s11738-016-2066-1

    Article  CAS  Google Scholar 

  • Ribeiro CL, Silva CM, Drost DR, Novaes E, Novaes C, 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. https://doi.org/10.1186/s12870-016-0753-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Street IH, Aman S, Yan Z, Ramzan A, Wang X, Shakeel SN, Kieber JJ, Schaller GE (2015) Ethylene inhibits cell proliferation of the Arabidopsis root meristem. Plant Physiol 169:338–350

    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  Google Scholar 

  • van Meer G, Holthuis JC (2000) Sphingolipid transport in eukaryotic cells. BBA Biomembr 1486:145–170

    Google Scholar 

  • Voss U, Wilson MH, Kenobi K, Gould PD, Robertson FC, Peer WA, Lucas M, Swarup K, Casimiro I, Holman TJ, Wells DM, Peret B, Goh T, Fukaki H, Hodgman TC, Laplaze L, Halliday KJ, Ljung K, Murphy AS, Hall AJ, Webb AAR, Bennett MJ (2015) The circadian clock rephases during lateral root organ initiation in Arabidopsis thaliana. Nat Commun 6:7641

    Article  Google Scholar 

  • Wang X, Wu L, Zhang S, Wu L, Ku L, Wei X, Xie L, Chen Y (2011) Robust expression and association of ZmCCA1 with circadian rhythms in maize. Plant Cell Rep 30:1261–1272

    Article  Google Scholar 

  • Wei C, Liu X, Long D, Guo Q, Fang Y, Bian C, Zhang D, Zeng Q, Xiang Z, Zhao A (2014) Molecular cloning and expression analysis of mulberry MAPK gene family. Plant Physiol Biochem 77:108–116

    Article  CAS  Google Scholar 

  • Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmuelling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15:2532–2550

    Article  CAS  Google Scholar 

  • Xu L (2017) De novo root regeneration from leaf explants: wounding auxin and cell fate transition. Curr Opin Plant Biol 41:39–45

    Article  Google Scholar 

  • Xu M, Liu S, Xuan L, Huang M, Wang Z (2016) Isolation and characterization of a poplar d-type cyclin gene associated with the SHORT-ROOT/SCARECROW network. Trees Struct Funct 30:255–263

    Article  CAS  Google Scholar 

  • Xu YX, Xiao MZ, Liu Y, Fu JL, He Y, Jiang DA (2017) The small auxin-up RNA OsSAUR45 affects auxin synthesis and transport in rice. Plant Mol Biol 94:97–107

    Article  CAS  Google Scholar 

  • Xue ZG, Zhang XM, Lei CF, Chen XJ, Fu YF (2012) Molecular cloning and functional analysis of one ZEITLUPE homolog GmZTL3 in soybean. Mol Biol Rep 39:1411–1418

    Article  CAS  Google Scholar 

  • Yamamoto Y, Sato E, Shimizu T, Nakamich N, Sato S, Kato T, Tabata S, Nagatani A, Yamashino T, Mizuno T (2003) Comparative genetic studies on the APRR5 and APRR7 genes belonging to the APRR1/TOC1 quintet implicated in circadian rhythm control of flowering time and early photomorphogenesis. Plant Cell Physiol 44:1119–1130

    Article  CAS  Google Scholar 

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Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (Grant no. 31670306), Applied Basic Research Projects in Yunnan Academy of Agricultural Sciences (Grant no. YJM201704) and China Agriculture Research System (Grant no. CARS-18).

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  1. Xu Cao and Wei Du contributed equally to this work.

Authors and Affiliations

  1. Jiangsu University of Science and Technology, Zhenjiang, Jiangsu, 212003, People’s Republic of China

    Xu Cao, Chunqiong Shang, Qiudi Shen, Li Liu & Jialing Cheng

  2. Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, Sericultural Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, Jiangsu, 212018, People’s Republic of China

    Xu Cao, Chunqiong Shang, Qiudi Shen, Li Liu & Jialing Cheng

  3. Sericulture and Apiculture Research Institute, Yunnan Academy of Agricultural Sciences, Mengzi, Yunnan, 661101, People’s Republic of China

    Wei Du

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  1. Xu Cao
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Correspondence to Jialing Cheng.

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Communicated by P. Wojtaszek.

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Cao, X., Du, W., Shang, C. et al. Comparative transcriptome reveals circadian and hormonal control of adventitious rooting in mulberry hardwood cuttings. Acta Physiol Plant 40, 197 (2018). https://doi.org/10.1007/s11738-018-2772-y

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