Skip to main content
Log in

Transcriptional sequencing and analysis of major genes involved in the adventitious root formation of mango cotyledon segments

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

A total of 74,745 unigenes were generated and 1975 DEGs were identified. Candidate genes that may be involved in the adventitious root formation of mango cotyledon segment were revealed.

Adventitious root formation is a crucial step in plant vegetative propagation, but the molecular mechanism of adventitious root formation remains unclear. Adventitious roots formed only at the proximal cut surface (PCS) of mango cotyledon segments, whereas no roots were formed on the opposite, distal cut surface (DCS). To identify the transcript abundance changes linked to adventitious root development, RNA was isolated from PCS and DCS at 0, 4 and 7 days after culture, respectively. Illumina sequencing of libraries generated from these samples yielded 62.36 Gb high-quality reads that were assembled into 74,745 unigenes with an average sequence length of 807 base pairs, and 33,252 of the assembled unigenes at least had homologs in one of the public databases. Comparative analysis of these transcriptome databases revealed that between the different time points at PCS there were 1966 differentially expressed genes (DEGs), while there were only 51 DEGs for the PCS vs. DCS when time-matched samples were compared. Of these DEGs, 1636 were assigned to gene ontology (GO) classes, the majority of that was involved in cellular processes, metabolic processes and single-organism processes. Candidate genes that may be involved in the adventitious root formation of mango cotyledon segment are predicted to encode polar auxin transport carriers, auxin-regulated proteins, cell wall remodeling enzymes and ethylene-related proteins. In order to validate RNA-sequencing results, we further analyzed the expression profiles of 20 genes by quantitative real-time PCR. This study expands the transcriptome information for Mangifera indica and identifies candidate genes involved in adventitious root formation in cotyledon segments of mango.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

Aux/IAA:

Auxin/indole-3-acetic acid

DCS:

Distal cut surface

DEGs:

Differentially expressed genes

ERF:

Ethylene-responsive transcription factor

GH3:

Gretchen Hagen 3

GO:

Gene ontology

KEGG:

Kyoto Encyclopedia of Genes and Genomes

KOG:

euKaryotic Ortholog Groups

Nr:

NCBI non-redundant protein sequences

Nt:

NCBI non-redundant nucleotide sequences

PAT:

Polar auxin transport

PCS:

Proximal cut surface

PIN:

PIN-FORMED

References

  • Ahkami AH, Melzer M, Ghaffari MR, Pollmann S, Ghorbani Javid M, Shahinnia F, Hajirezaei MR, Druege U (2013) Distribution of indole-3-acetic acid in Petunia hybrida shoot tip cuttings and relationship between auxin transport, carbohydrate metabolism and adventitious root formation. Planta 238:499–517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Annadurai RS, Jayakumar V, Mugasimangalam RC, Katta MA, Anand S, Gopinathan S, Sarma SP, Fernandes SJ, Mullapudi N, Murugesan S, Rao SN (2012) Next generation sequencing and de novo transcriptome analysis of Costus pictus D. Don, a non-model plant with potent anti-diabetic properties. BMC Genomics 13:663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azim MK, Khan IA, Zhang Y (2014) Characterization of mango (Mangifera indica L.) transcriptome and chloroplast genome. Plant Mol Biol 85:193–208

    Article  CAS  PubMed  Google Scholar 

  • Bai XG, Todd CD, Desikan R, Yang YP, Hu XY (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 158:725–736

    Article  CAS  PubMed  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 

  • Busov VB, Johannes E, Whetten RW, Sederoff RR, Spiker SL, Lanz-Garcia C, Goldfarb B (2004) An auxin-inducible gene from loblolly pine (Pinus taeda L.) is differentially expressed in mature and juvenile-phase shoots and encodes a putative transmembrane protein. Planta 218:916–927

    Article  CAS  PubMed  Google Scholar 

  • Clark DG, Gubrim EK, Barrett JE, Nell TA, Klee HJ (1999) Root formation in ethylene-insensitive plants. Plant Physiol 121:53–59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • da Costa CT, deAlmeida MR, Ruedell CM, Schwambach J, Maraschin FS, Fett-Neto AG (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 

  • Dautt-Castro M, Ochoa-Leyva A, Contreras-Vergara CA, Pacheco-Sanchez MA, Casas-Flores S, Sanchez-Flores A, Kuhn DN, Islas-Osuna MA (2015) Mango (Mangifera indica L.) cv. Kent fruit mesocarp de novo transcriptome assembly identifies gene families important for ripening. Front. Plant Sci 6:62

    Google Scholar 

  • Davies F, Davis T, Kester D (1994) Commercial importance of adventitious rooting to horticulture. In: Davis T, Haissig B (eds) Biology of adventitious root formation. Plenum Press, New York, pp 53–59

    Chapter  Google Scholar 

  • De Klerk GJ, Van der Krieken W, De Jong JC (1999) Review the formation of adventitious roots: new concepts, new possibilities. In Vitro Cell Dev Plant 35:189–199

    Article  Google Scholar 

  • De Klerk GJ, Hanecakova J, Jasik J (2001) The role of cytokinins in rooting of stem slices cut from apple microcuttings. Plant Biosyst 135:79–84

    Article  Google Scholar 

  • De Veylder L, Beeckman T, Inze D (2007) The ins and outs of the plant cell cycle. Nat Rev Mol Cell Biol 8:655–665

    Article  PubMed  Google Scholar 

  • Diaz-Sala C, Hutchison KW, Goldfarb B, Greenwood MS (1996) Maturation-related loss in rooting competence by loblolly pine stem cuttings: the role of auxin transport, metabolism and tissue sensitivity. Physiol Plant 97:481–490

    Article  CAS  Google Scholar 

  • Dong CJ, Cao N, Wang LL, Zhang HX, Wang HF, Tai LL, Shang QM (2016) Regulatory roles of cotyledon-generated auxin in adventitious root formation on the hypocotyls of cucumber seedlings. Acta Hortic Sin 43:1929–1940

    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 5:1–19

    Article  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 X, Zhang X, Nie H, Liu M, Cheng JL (2016) Transcript profiling analysis reveals crucial genes regulating main metabolism during adventitious root formation in cuttings of Morus alba L. Plant Growth Regul 79:251–262

    Article  CAS  Google Scholar 

  • FAO (2012) FAOSTAT database. http://faostat.fao.org/site/567/default.aspx. Accessed 28 Feb 2016

  • Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–W37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Friml J (2010) Subcellular trafficking of PIN auxin efflux carriers in auxin transport. Eur J Cell Biol 89:231–235

    Article  CAS  PubMed  Google Scholar 

  • Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talón M, Dopazo J, Conesa A (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36:3420–3435

    Article  PubMed  PubMed Central  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gutierrez L, Mongelard G, Floková K, Pacurar DI, Novák 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  PubMed  PubMed Central  Google Scholar 

  • Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385

    Article  CAS  PubMed  Google Scholar 

  • Harbage JF, Stimart DP (1996) Ethylene does not promote adventitious root initiation on apple microcuttings. J Am Soc Hortic Sci 121:880–885

    CAS  Google Scholar 

  • Hošek P, Kubeš M, Laňková M, Dobrev PI, Klíma P, Kohoutová M, Petrásek J, Hoyerová K, Jirina M, Zazímalová E (2012) Auxin transport at cellular level: new insights supported by mathematical modelling. J Exp Bot 63:3815–3828

    Article  PubMed  PubMed Central  Google Scholar 

  • Hutchison KW, Singer PB, McInnis S, Diaz-Sala C, Greenwood MS (1999) Expansins are conserved in conifers and expressed in hypocotyls in response to exogenous auxin. Plant Physiol 120:827–832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480–D484

    Article  CAS  PubMed  Google Scholar 

  • Kevers C, Hausman JF, Faivre-Rampant O, Evers D, Gaspar T (1997) Hormonal control of adventitious rooting: progress and questions. Angew Bot 71:71–79

    CAS  Google Scholar 

  • Kim HJ, Lynch JP, Brown KM (2008) Ethylene insensitivity impedes a subset of responses to phosphorus deficiency in tomato and petunia. Plant Cell Environ 31:1744–1755

    Article  CAS  PubMed  Google Scholar 

  • León J, Rojo E, Sánchez Serrano JJ (2001) Wound signalling in plants. J Exp Bot 52:1–9

    Article  PubMed  Google Scholar 

  • Lewis DR, Olex AL, Lundy SR, Turkett WH, Fetrow JS, Muday GK (2013) A kinetic analysis of the auxin transcriptome reveals cell wall remodeling proteins that modulate lateral root development in Arabidopsis. Plant Cell 25:3329–3346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li B, Dewey C (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323

    Article  CAS  Google Scholar 

  • Li YH, Chen QZ, Xiao JN, Chen YF, Li XJ, Staehelin C, Huang XL (2008) Characteristics of adventitious root formation in cotyledon segments of mango (Mangifera indica L. cv. Zihua): two induction patterns, histological origins and the relationship with polar auxin transport. Plant Growth Regul 54:165–177

    Article  CAS  Google Scholar 

  • Li YH, Ma J, Wu YJ, Sun GM (2011) The factors of influencing adventitious root formation of cotyledon segments in mango (Mangifera indica L.). Acta Bot Boreali Occident Sin 31:842–847

    Google Scholar 

  • Li YH, Zou MH, Feng BH, Huang X, Zhang Z, Sun GM (2012) Molecular cloning and characterization of the genes encoding an auxin efflux carrier and the auxin influx carriers associated with the adventitious root formation in mango (Mangifera indica L.) cotyledon segments. Plant Physiol Biochem 55:33–42

    Article  CAS  PubMed  Google Scholar 

  • Li SW, Shi RF, Leng Y (2015) De novo characterization of the mung bean transcriptome and transcriptomic analysis of adventitious rooting in seedlings using RNA-Seq. PLoS One 10:e0132969

    Article  PubMed  PubMed Central  Google Scholar 

  • Li SW, Shi RF, Leng Y, Zhou Y (2016a) Transcriptomic analysis reveals the gene expression profile that specifically responds to IBA during adventitious rooting in mung bean seedlings. BMC Genomics 17:43

    Article  PubMed  PubMed Central  Google Scholar 

  • Li YH, Zhang Z, Wu QS (2016b) Isolation and expression analysis of the ethylene receptor gene MiETR1b in mango (Mangifera indica). Hortic Plant J 2:1–7

    Article  Google Scholar 

  • Luo C, He XH, Chen H, Hu Y, Ou SJ (2013) Molecular cloning and expression analysis of four actin genes (MiACT) from mango. Biol Plant 57:238–244

    Article  CAS  Google Scholar 

  • Luria N, Sela N, Yaari M, Feygenberg O, Kobiler I, Lers A, Prusky D (2014) De-novo assembly of mango fruit peel transcriptome reveals mechanisms of mango response to hot water treatment. BMC Genomics 15:1

    Article  Google Scholar 

  • Marín-Rodríguez MC, Orchard J, Seymour GB (2002) Pectate lyases, cell wall degradation and fruit softening. J Exp Bot 53:2115–2119

    Article  PubMed  Google Scholar 

  • Metaxas D, Syros T, Yupsanis T, Economou A (2004) Peroxidases during adventitious rooting in cuttings of Arbutus unedo and Taxus baccata as affected by plant genotype and growth regulator treatment. Plant Growth Regul 44:257–266

    Article  CAS  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  PubMed  Google Scholar 

  • Muday GK, Maloney GS, Lewis DR (2015) Integration of ethylene and auxin signaling and the developmental consequences of their crosstalk. In: Wen CK (ed) The ethylene in plants. Springer, Netherlands, pp 175–204

    Google Scholar 

  • Negi S, Sukumar P, Liu X, Cohen JD, Muday GK (2010) Genetic dissection of the role of ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato. Plant J 61:3–15

    Article  CAS  PubMed  Google Scholar 

  • Pacurar DI, Pacurar ML, Bussell JD, Schwambach J, Pop TI, Kowalczyk M, Gutierrez L, Cavel E, Chaabouni S, Ljung K, Fett-Neto AG, Pamfil D, Bellini C (2014a) Identification of new adventitious rooting mutants amongst suppressors of the Arabidopsis thaliana superroot2 mutation. J Exp Bot 65:1605–1618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pijut PM, Woeste KE, Michler CH (2011) Promotion of adventitious root formation of difficult-to-root hardwood tree species. Hortic Rev 38:213–253

    CAS  Google Scholar 

  • Ramírez-Carvajal GA, Morse AM, Dervinis C, Davis M (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 

  • Rout GR, Mohapatra A, Jain SM (2006) Tissue culture of ornamental pot plant: a critical review on present scenario and future prospects. Biotechnol Adv 24:531–560

    Article  CAS  PubMed  Google Scholar 

  • Schopfer P, Liszkay A, Bechtold M, Frahry G, Wagner A (2002) Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta 214:821–828

    Article  CAS  PubMed  Google Scholar 

  • Sorin C, Negroni L, Balliau T, Corti H, Jacquemot MP, Davanture M, Sandberg G, Zivy M, Bellini C (2006) Proteomic analysis of different mutant genotypes of Arabidopsis led to the identification of 11 proteins correlating with adventitious root development. Plant Physiol 140:349–364

    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 

  • Sukumar P (2010) Role of auxin and ethylene in adventitious root formation in Arabidopsis and tomato. Dissertation, Wake Forest University

  • Sukumar P, Maloney GS, Muday GK (2013) Localized induction of the ATP-binding cassette B19 auxin transporter enhances adventitious root formation in Arabidopsis. Plant Physiol 162:1392–1405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takáč T, Obert B, Rolčík J, Šamaj J (2016) Improvement of adventitious root formation in flax using hydrogen peroxide. New Biotechnol 33:728–734

    Article  Google Scholar 

  • Tchoundjeu Z, Avana ML, Leakey RRB, Simons AJ, Asaah E, Duguma B, Bell JM (2002) Vegetative propagation of Prunus africana: effects of rooting medium, auxin concentrations and leaf area. Agroforestry Syst 54:183–192

    Article  Google Scholar 

  • Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Sandt VST, Suslov D, Verbelen JP, Vissenberg K (2007) Xyloglucan endotransglucosylase activity loosens a plant cell wall. Ann Bot 100:1467–1473

    Article  PubMed  PubMed Central  Google Scholar 

  • Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136:1005–1016

    Article  CAS  PubMed  Google Scholar 

  • Veloccia A, Fattorini L, Della Rovere F, Sofo A, D’Angeli S, Betti C, Falasca G, Altamura MM (2016) Ethylene and auxin interaction in the control of adventitious rooting in Arabidopsis thaliana. J Exp Bot 67:6445–6458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verstraeten I, Beeckman T, Geelen D (2013) Adventitious root induction in Arabidopsis thaliana as a model for in vitro root organogenesis. In: De Smet I (ed) Plant organogenesis: methods and protocols. Humana Press, New York, pp 159–175

    Chapter  Google Scholar 

  • Verstraeten I, Schotte S, Geelen D (2014) Hypocotyl adventitious root organogenesis differs from lateral root development. Front Plant Sci 5:495

    Article  PubMed  PubMed Central  Google Scholar 

  • Vidal N, Arellano G, San-Jose MC, Vieitez AM, Ballester A (2003) Developmental stages during the rooting of in vitro-cultured Quercus robur shoots from material of juvenile and mature origin. Tree Physiol 23:1247–1254

    Article  CAS  PubMed  Google Scholar 

  • Villacorta-Martín C, Sánchez-García AB, Villanova J, Cano A, van de Rhee M, de Haan J, Acosta M, Passarinho P, Pérez-Pérez JM (2015) Gene expression profiling during adventitious root formation in carnation stem cuttings. BMC Genomics 16:1

    Article  Google Scholar 

  • Wendling I, Trueman SJ, Xavier A (2014) Maturation and related aspects in clonal forestry—part I: concepts, regulation and consequences of phase change. New For 45:449–471

    Article  Google Scholar 

  • Wu HX, Jia HM, Ma XW, Wang SB, Yao QS, Xu WT, Zhou YG, Gao ZS, Zhan RL (2014) Transcriptome and proteomic analysis of mango (Mangifera indica Linn) fruits. J Proteomics 105:19–30

    Article  CAS  PubMed  Google Scholar 

  • Xiao JN, Huang XL, Li Y, Huang X, Li XJ (2003) RNA extraction from cotyledon of mango with high levels of secondary substances and carbohydrates. China Biotech 23:83–86

    CAS  Google Scholar 

  • Xuan W, Zhu FY, Xu S, Huang BK, Ling TF, Qi JY, Ye MB, Shen WB (2008) The heme oxygenase/carbon monoxide system is involved in the auxin-induced cucumber adventitious rooting process. Plant Physiol 148:881–893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou DX, Yin K, Xu ZH, Xue HW (2003) Effect of polar auxin transport on rice root development. Acta Bot Sin 45:1421–1427

    CAS  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (31372053), the Agriculture and Food Research Initiative competitive Grant (# 2015-06811 to GKM) of the United States Department of Agriculture National Institute of Food and Agriculture, China Scholarship Council (201503260005).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yun-He Li.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, YH., Zhang, HN., Wu, QS. et al. Transcriptional sequencing and analysis of major genes involved in the adventitious root formation of mango cotyledon segments. Planta 245, 1193–1213 (2017). https://doi.org/10.1007/s00425-017-2677-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-017-2677-9

Keywords

Navigation