Skip to main content

Hairy Roots as a Tool for the Functional Analysis of Plant Genes

  • Chapter
  • First Online:
Hairy Roots

Abstract

With its root-inducing (Ri) plasmid, Agrobacterium rhizogenes is a valuable alternative to transfer gene constructs into the genome of plant species which are difficult to stably transform with disarmed strains of Agrobacterium tumefaciens. Composite plants consisting of transformed hairy roots induced on a non-transgenic shoot have been reported in an increasing number of legume and nonlegume plant species. They were first used in the model legumes Medicago truncatula and Lotus japonicus to study the symbiotic interaction with rhizobia. Since then, composite plants have been shown to be effective to investigate the function of genes involved in mycorrhizal symbiosis, root-nematode and root-pathogen interactions, resistance response of plant roots to parasitic weeds, root development and branching, and the formation of wood. The different methodologies developed to generate composite plants and the applications of co-transformed hairy roots for studying gene function are discussed in this chapter, together with recent opportunities offered by genome editing technologies in hairy roots.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abdel-Lateif K, Vaissayre V, Gherbi H et al (2013) Silencing of the chalcone synthase gene in Casuarina glauca highlights the important role of flavonoids during nodulation. New Phytol 199:1012–1021

    Article  CAS  PubMed  Google Scholar 

  • Alagarsamy K, Shamala LF, Wei S (2018) Protocol: high-efficiency in-planta Agrobacterium-mediated transgenic hairy root induction of Camellia sinensis var. sinensis. Plant Methods 14:17

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Alpizar E, Dechamp E, Espeout S et al (2006) Efficient production of Agrobacterium rhizogenes-transformed roots and composite plants for studying gene expression in coffee roots. Plant Cell Rep 25:959–967

    Article  CAS  PubMed  Google Scholar 

  • An J, Hu Z, Che B, Chen H et al (2017) Heterologous expression of Panax ginseng PgTIP1 confers enhanced salt tolerance of soybean cotyledon hairy roots, composite, and whole plants. Front Plant Sci 8:1232

    Article  PubMed  PubMed Central  Google Scholar 

  • Anami S, Njuguna E, Coussens G et al (2013) Higher plant transformation: principles and molecular tools. Int J Dev Biol 57:483–494

    Article  CAS  PubMed  Google Scholar 

  • Balasubramanian A, Venkatachalam R, Selvakesavan R et al (2011) Optimisation of methods for Agrobacterium rhizogenes mediated generation of composite plants in Eucalyptus camaldulensis. BMC Proc 5(suppl. 7):45–46

    Article  Google Scholar 

  • Banasiak J, Biala W, Staszków A et al (2013) A Medicago truncatula ABC transporter belonging to subfamily G modulates the level of isoflavonoids. J Exp Bot 64(4):1005–1015

    Article  CAS  PubMed  Google Scholar 

  • Beach KH, Gresshoff PM (1988) Characterization and culture of Agrobacterium rhizogenes transformed roots of forage Legumes. Plant Sci 57:73–81

    Article  CAS  Google Scholar 

  • Belhaj K, Chaparro-Garcia A, Kamoun S et al (2015) Editing plant genomes with CRISPR/Cas9. Curr Opin Biotechnol 32:76–84

    Article  CAS  PubMed  Google Scholar 

  • Belmondo S, Calcagno C, Genre A (2016) The Medicago truncatula MtRbohE gene is activated in arbusculated cells and is involved in root cortex colonization. Planta 243:251–262

    Article  CAS  PubMed  Google Scholar 

  • Boisson-Dernier A, Chabaud M, Garcia F et al (2001) Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Mol Plant Microbe Interact 14:695–700

    Article  CAS  PubMed  Google Scholar 

  • Boisson-Dernier A, Andriankaja A, Chabaud M et al (2005) MtENOD11 gene activation during rhizobial infection and mycorrhizal arbuscule development requires a common AT-rich-containing regulatory sequence. Mol Plant Microbe Interact 18:1269–1276

    Article  CAS  PubMed  Google Scholar 

  • Bonaldi K, Gherbi H, Franche C et al (2010) The Nod factor-independent symbiotic signalling pathway: development of Agrobacterium rhizogenes-mediated transformation for the legume Aeschynomene indica. Mol Plant Microbe Interact 12:1537–1544

    Article  CAS  PubMed  Google Scholar 

  • Bosselut N, Van Ghelder C, Claverie M et al (2011) Agrobacterium rhizogenes-mediated transformation of Prunus as an alternative for gene functional analysis in hairy-roots and composite plants. Plant Cell Rep 30:1313–1326

    Article  CAS  PubMed  Google Scholar 

  • Britton MT, Escobar MA, Dandekar M (2008) The oncogenes of Agrobacterium tumefaciens and Agrobacterium rhizogenes. In: Tzfira T, Citovsky V (eds) Agrobacterium: from biology to biotechnology. Springer, Heidelberg, pp 525–563

    Google Scholar 

  • Cai Y, Chen L, Liu X et al (2015) CRISPR/Cas9-mediated genome editing in soybean hairy roots. PLoS One 10(8):e0136064

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cao D, Hou W, Song S et al (2009) Assessment of conditions affecting Agrobacterium rhizogenes-mediated transformation of soybean. Plant Cell Tissue Organ Cult 96:45–52

    Article  Google Scholar 

  • Claverie M, Dirlewanger E, Bosselut N et al (2011) The Ma gene for complete-spectrum resistance to Meloidogyne species in Prunus is a TNL with a huge repeated C-terminal post-LRR region. Plant Physiol 156:779–792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Collier R, Fuchs B, Walter N et al (2005) Ex vitro composite plants: an inexpensive, rapid method for root biology. Plant J 43:449–457

    Article  CAS  PubMed  Google Scholar 

  • Colpaert N, Tilleman S, van Montagu M et al (2008) Composite Phaseolus vulgaris plants with transgenic roots as research tool. African J Biotechnol 7:404–408

    CAS  Google Scholar 

  • Coque L, Neogi P, Pislariu C et al (2008) Transcription of ENOD8 in Medicago truncatula nodules directs ENOD8 esterase to developing and mature symbiosomes. Mol Plant Microbe Interact 21:404–410

    Article  CAS  PubMed  Google Scholar 

  • Díaz CL, Melchers LS, Hooykaas PJJ et al (1989) Root lectin as a determinant of host-plant specificity in the Rhizobium-legume symbiosis. Nature 338:579–581

    Article  Google Scholar 

  • Diaz CL, Spaink JD, Kijne JW (2000) Heterologous rhizobial lipochitin oligosaccharides and chitin oligomers induce cortical cell divisions in red clover roots, transformed with the pea lectin gene. Mol Plant-Microbe Interact 13:268–276

    Article  CAS  PubMed  Google Scholar 

  • Diouf D, Gherbi H, Prin Y et al (1995) Hairy root nodulation of Casuarina glauca: a system for the study of symbiotic gene expression in an actinorhizal tree. Mol Plant Microbe Interact 8(4):532–537

    Article  CAS  PubMed  Google Scholar 

  • Dolatabadian A, Modarres Sanavy SA et al (2013) Agrobacterium rhizogenes transformed soybean roots differ in their nodulation and nitrogen fixation response to genistein and salt stress. World J Microbiol Biotechnol 29:1327–1339

    Article  CAS  PubMed  Google Scholar 

  • Du H, Zeng X, Zhao M et al (2016) Efficient targeted mutagenesis in soybean by TALENs and CRISPR/Cas9. J Biotechnol 217:90–97

    Article  CAS  PubMed  Google Scholar 

  • Estrada-Navarrete G, Alvarado-Affantranger X, Olivares JE et al (2006) Agrobacterium rhizogenes transformation of the Phaseolus spp.: a tool for functional genomics. Mol Plant Microbe Interact 19:1385–1393

    Article  CAS  PubMed  Google Scholar 

  • Fan Y, Liu J, Lyu S et al (2017) The Soybean Rfg1 gene restricts nodulation by Sinorhizobium fredii USDA193. Front Plant Sci 8:1548

    Article  PubMed  PubMed Central  Google Scholar 

  • Fosu-Nyarko J, Jones MG (2016) Advances in understanding the molecular mechanisms of root lesion nematode host interactions. Annu Rev Phytopathol 54:253–278

    Article  CAS  PubMed  Google Scholar 

  • Geng L, Chi J, Shu C, Gresshoff PM et al (2013) A chimeric cry8Ea1 gene flanked by MARs efficiently controls Holotrichia parallela. Plant Cell Rep 32:1211–1218

    Article  CAS  PubMed  Google Scholar 

  • Geurts R, Xiao TT, Reinhold-Hurek B (2016) What does it take to evolve a nitrogen-fixing endosymbiosis? Trends Plant Sci 21:199–208

    Article  CAS  PubMed  Google Scholar 

  • Gherbi H, Svistoonoff S, Estevan J et al (2008a) SymRK defines a common genetic basis for plant root endosymbioses with AM fungi, rhizobia and Frankia bacteria. Proc National Acad Sci USA 105:4928–4932

    Article  CAS  Google Scholar 

  • Gherbi H, Nambiar-Veetil M, Zhong C et al (2008b) Post-transcriptional gene silencing in the root system of the actinorhizal tree Allocasuarina verticillata. Mol Plant Microbe Interact 21:518–524

    Article  CAS  PubMed  Google Scholar 

  • Guillon S, Trémouillaux-Guiller J, Kumar Pati P et al (2006) Hairy root research: recent scenario and exciting prospects. Cur Opin Plant Biol 9:341–346

    Article  CAS  Google Scholar 

  • Guimaraes LA, Pereira BM, Araujo ACG et al (2017a) Ex vitro hairy root induction in detached peanut leaves for plant-nematode interaction studies. Plant Methods 13:25

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guimaraes LA, Mota APZ, Araujo ACG et al (2017b) Genome-wide analysis of expansin superfamily in wild Arachis discloses a stress-responsive expansin-like B gene. Plant Mol Biol 94:79–96

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo W, Zhao J, Li X, Qin L et al (2011) A soybean β-expansin gene GmEXPB2 intrinsically involved in root system architecture responses to abiotic stresses. Plant J 66:541–552

    Article  CAS  PubMed  Google Scholar 

  • Hansen J, Jorgensen JE, Stougaard J, Marcker K (1989) Hairy roots – a short cut to transgenic root nodules. Plant Cell Rep 8:12–15

    Article  CAS  PubMed  Google Scholar 

  • Haselhoff J, Siemering KR (2006) The use of green fluorescent protein in plants. Methods Biochem Anal 47:259–284

    Google Scholar 

  • Horn P, Santala J, Nielsen SL et al (2014) Composite potato plants with transgenic roots on non-transgenic shoots: a model system for studying gene silencing in roots. Plant Cell Rep 33:1977–1992

    Article  CAS  PubMed  Google Scholar 

  • Iaffaldano B, Zhang Y, Cornish K (2016) CRISPR/Cas9 genome editing of rubber producing dandelion Taraxacum kok-saghyz using Agrobacterium rhizogenes without selection. Ind Crop Prod 89:356–362

    Google Scholar 

  • Ilina EL, Logachov AA, Laplaze L et al (2012) Composite Cucurbita pepo plants with transgenic roots as a tool to study root development. Ann Bot 110:479–489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Imanishi L, Vayssières A, Franche C et al (2011) Transformed hairy roots of Discaria trinervis: a valuable tool for studying actinorhizal symbiosis in the context of intercellular infection. Mol Plant Microbe Interact 24:1317–1324

    Article  CAS  PubMed  Google Scholar 

  • Jacobs TB, LaFayette PR, Schmitz RJ, Parrott WA (2015) Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnol 15:16

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusion: ß-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jensen JS, Marcker KA, Otten L, Schell J (1986) Nodule-specific expression of a chimeric soybean leghemoglobin gene in transgenic Lotus corniculatus. Nature 321:669–674

    Article  CAS  Google Scholar 

  • Karami O (2008) Factors affecting Agrobacterium-mediated transformation of plants. Transgenic Plant J 2:127–137

    Google Scholar 

  • Kassaw T, Nowak S, Schnabel E, Frugoli J (2017) ROOT DETERMINED NODULATION1 is required for M. truncatula CLE12, but not CLE13, peptide signaling through the SUNN receptor kinase. Plant Physiol 174:2445–2456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kereszt A, Li D, Indrasumunar A et al (2007) Agrobacterium rhizogenes-mediated transformation of soybean to study root biology. Nature Protoc 2:948–952

    Article  CAS  Google Scholar 

  • Kiirika LM, Bergmann HF, Schikowsky C et al (2012) Silencing of the Rac1 GTPase MtROP9 in Medicago truncatula stimulates early mycorrhizal and oomycete root colonizations but negatively affects rhizobial infection. Plant Physiol 159:501–516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirchner TW, Niehaus M, Debener T et al (2017) Efficient generation of mutations mediated by CRISPR/Cas9 in the hairy root transformation system of Brassica carinata. PLoS One 12:e0185429

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Koplow J, Byrne MC, Jen G et al (1984) Physical map of the Agrobacterium rhizogenes strain 8196 virulence plasmid. Plasmid 11:130–140

    Article  Google Scholar 

  • Lacroix B, Citovsky V (2013) The roles of bacterial and host plant factors in Agrobacterium-mediated genetic transformation. Int J Dev Biol 57:46481

    Article  CAS  Google Scholar 

  • Lanfranco L, Bonfante P, Genre A (2016) The mutualistic interaction between plants and arbuscular mycorrhizal fungi. Microbiol Spectr 4(6)

    Google Scholar 

  • Lee NG, Stein B, Suzuki H, Verma DPS (1993) Expression of antisense nodulin-35 RNA in Vigna aconitifolia transgenic root nodules retards peroxisome development and affects nitrogen availability to the plant. Plant J 3:599–606

    Article  CAS  PubMed  Google Scholar 

  • Leppyanen IV, Shakhnazarova VY, Shtark OY et al (2017) Receptor-like kinase LYK9 in Pisum sativum L. is the CERK1-Like Receptor that controls both plant immunity and AM symbiosis development. Int J Mol Sci 19(1):E8

    Article  PubMed  CAS  Google Scholar 

  • Li J, Todd TC, Trick HN (2010) Rapid in planta evaluation of root expressed transgenes in chimeric soybean plants. Plant Cell Rep 29:113–123

    Article  CAS  PubMed  Google Scholar 

  • Li J-F, Zhang D, Sheen J (2014) Cas9-based genome editing in Arabidopsis and tobacco. Methods Enzymol 546:459–472

    Article  CAS  PubMed  Google Scholar 

  • Li X, Zhao J, Tan Z et al (2015) GmEXPB2, a cell wall β-expansin, affects soybean nodulation through modifying root architecture and promoting nodule formation and development. Plant Physiol 169:2640–2653

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li B, Cui G, Shen G, Zhan Z et al (2017) Targeted mutagenesis in the medicinal plant Salvia miltiorrhiza. Sci Rep 7:43320

    Article  PubMed  PubMed Central  Google Scholar 

  • Liang Z, Zhang K, Chen K, Gao C (2014) Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. J Genet Genom 41:63–68

    Article  CAS  Google Scholar 

  • Limpens E, Ramos J, Franken C et al (2004) RNA interference in Agrobacterium rhizogenes-transformed roots of Arabidopsis and Medicago truncatula. J Exp Bot 55:983–992

    Article  CAS  PubMed  Google Scholar 

  • Liu D, Hu R, Palla KJ et al (2016) Advances and perspectives on the use of CRISPR/Cas9 systems in plant genomics research. Curr Opin Plant Biol 30:70–77

    Article  CAS  PubMed  Google Scholar 

  • Markmann K, Giczey C, Parniske M (2008) Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria. PLoS Biol 6:e68

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mehrotra S, Srivastava V, Ur Rahman L, Kukreja AK (2015) Hairy root biotechnology – indicative timeline to understand missing links and future outlook. Protoplasma 252:1189–1201

    Article  CAS  PubMed  Google Scholar 

  • Mellor KE, Hoffman AM, Timko MP (2012) Use of ex vitro composite plants to study the interaction of cowpea (Vigna unguiculata L.) with the root parasitic angiosperm Striga gesnerioides. Plant Methods 8(1):22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miao J, Guo D, Zhang J et al (2013) Targeted mutagenesis in rice using CRISPR-Cas system. Cell Res 23:1233–1236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michno JM, Wang X, Liu J et al (2015) CRISPR/Cas mutagenesis of soybean and Medicago truncatula using a new web-tool and a modified Cas9 enzyme. GM Crops Food 6:243–252

    Article  PubMed  PubMed Central  Google Scholar 

  • Mrosk C, Forner S, Hause G et al (2009) Composite Medicago truncatula plants harbouring Agrobacterium rhizogenes-transformed roots reveal normal mycorrhization by Glomus intraradices. J Exp Bot 60:3797–3807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nanjareddy K, Arthikala MK, Aguirre AL et al (2017) Plant promoter analysis: identification and characterization of root nodule specific promoter in the common bean. J Vis Exp 130

    Google Scholar 

  • Neb D, Das A, Hintelmann A, Nehls U (2017) Composite poplars: a novel tool for ectomycorrhizal research. Plant Cell Rep 36:1959–1970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nogué F, Mara K, Collonnier C, Casacuberta JM (2016) Genome engineering and plant breeding: impact on trait discovery and development. Plant Cell Rep 35:1475–1486

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Plasencia A, Soler M, Dupas A et al (2016) Eucalyptus hairy roots, a fast, efficient and versatile tool to explore function and expression of genes involved in wood formation. Plant Biotechnol J 14:1381–1393

    Article  CAS  PubMed  Google Scholar 

  • Prabhu SA, Ndlovu B, Engelbrecht J, van den Berg N (2017) Generation of composite Persea americana (Mill.) (avocado) plants: a proof-of-concept-study. PLoS One 12:e0185896

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Quandt H-J, Pühler A, Broer I (1993) Transgenic root nodules of Vicia hirsuta: a fast and efficient system for the study of gene expression in indeterminate-type nodules. Mol Plant-Microbe Interact 6:699–706

    Article  Google Scholar 

  • Ree SY, Mutwill M (2014) Towards revealing the functions of all genes in plants. Trends Plant Sci 19:212–221

    Article  CAS  Google Scholar 

  • Ron M, Kajala K, Pauluzzi G et al (2014) Hairy root transformation using Agrobacterium rhizogenes as a tool for exploring cell type-specific gene expression and function using tomato as a model. Plant Physiol 166:455–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Runo S, Macharia S, Alakonya A et al (2012) Striga parasitizes transgenic hairy roots of Zea mays and provides a tool for studying plant-plant interactions. Plant Methods 8:20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sinharoy S, Saha S, Chaudhury SR, Dasgupta M (2009) Transformed hairy roots of Arachis hypogea: a tool for studying root nodule symbiosis in a non-infection thread legume of the Aeschynomene tribe. Mol Plant Microbe Interact 22:132–142

    Article  CAS  PubMed  Google Scholar 

  • Smouni A, Laplaze L, Bogusz D et al (2002) The 35S promoter is not constitutively expressed in the transgenic tropical actinorhizal tree, Casuarina glauca. Funct Plant Biol 29:649–656

    Article  CAS  PubMed  Google Scholar 

  • Stiller J, Martirani L, Tuppale S et al (1997) High frequency transformation and regeneration of transgenic plants in the model Lotus japonicus. J Exp Bot 48:1357–1365

    Article  CAS  Google Scholar 

  • Subramanian S, Hu X, Lu G et al (2004) The promoters of two isoflavone synthase genes respond differentially to nodulation and defense signals in transgenic soybean roots. Plant Mol Biol 54:623–639

    Article  CAS  PubMed  Google Scholar 

  • Subramanian S, Stacey G, Yu O (2006) Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. Plant J 48:261–273

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Hu Z, Chen R et al (2015) Targeted mutagenesis in soybean using the CRISPR-Cas9 system. Sci Rep 5:10342

    Article  PubMed  PubMed Central  Google Scholar 

  • Svistoonoff S, Gherbi H, Nambiar-Veetil M et al (2010) Contribution of transgenic Casuarinaceae to our knowledge of the actinorhizal symbiosis. Symbiosis 50:3–11

    Article  CAS  Google Scholar 

  • Svistoonoff S, Benabdoun FM, Nambiar-Veetil M et al (2013) The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis. PLoS One 8(5):e64515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Talano MA, Oller AL, Gonzalez P, Agostini E (2012) Hairy roots, their multiple applications and recent patents. Recent Pt Biotechnol 6:115–133

    Article  CAS  Google Scholar 

  • Tepfer D (1990) Genetic transformation using Agrobacterium rhizogenes. Physiol Plant 79:140–146

    Article  CAS  Google Scholar 

  • Uhde-Stone C, Liu J, Allan DL, Vance C (2005) Transgenic proteoid roots of white lupin: a vehicle for characterizing and silencing root genes involved in adaptation to P stress. Plant J 44:840–853

    Article  CAS  PubMed  Google Scholar 

  • Van de Velde W, Mergeay J, Hoslsters M, Goormachtig S (2003) Agrobacterium rhizogenes-mediated transformation of Sesbania rostrata. Plant Sci 165:1281–1288

    Article  CAS  Google Scholar 

  • Wang Y, Cheng X, Shan Q et al (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nature Biotechnol 32:947–951

    Article  CAS  Google Scholar 

  • Wang L, Wang L, Tan Q et al (2016) Efficient inactivation of symbiotic nitrogen fixation related genes in Lotus japonicus using CRISPR-Cas9. Front Plant Sci 7:1333

    PubMed  PubMed Central  Google Scholar 

  • Wang L, Wang L, Zhou Y, Duanmu D (2017) Use of CRISPR/Cas9 for symbiotic nitrogen fixation research in Legumes. Prog Mol Biol Transl Sci 149:187–213

    Article  PubMed  Google Scholar 

  • White LJ, Jothibasu K, Reese RN et al (2015) Spatio temporal influence of isoflavonoids on bacterial diversity in the soybean rhizosphere. Mol Plant Microbe Interact 28:22–29

    Article  PubMed  Google Scholar 

  • Yao Z, Tian J, Liao H (2014) Comparative characterization of GmSPX members reveals that GmSPX3 is involved in phosphate homeostasis in soybean. Ann Bot 114:477–488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida S, Cui S, Ichihashi Y, Shirasu K (2016) The Haustorium, a specialized invasive organ in parasitic plants. Annu Rev Plant Biol 67:643–667

    Article  CAS  PubMed  Google Scholar 

  • Zhou Z, Tan H, Li Q et al (2018) CRISPR/Cas9-mediated efficient targeted mutagenesis of RAS in Salvia miltiorrhiza. Phytochem 148:63–70

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Dr. Chonglu Zhong acknowledges the supports of the Specific Program for National Non-profit Scientific Institutions (CAFYBB2018ZB003) and CAF International Cooperation Innovation Project “Tropical Tree Genetic Resources and Genetic Diversity.” Research conducted at the Institute of Forest Genetics and Tree Breeding was supported by the Indian Council of Forestry Research and Education, Dehradun, India. Research conducted in UMR DIADE was supported by the Research Institute for sustainable Development and the University of Montpellier, France.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Claudine Franche .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Zhong, C., Nambiar-Veetil, M., Bogusz, D., Franche, C. (2018). Hairy Roots as a Tool for the Functional Analysis of Plant Genes. In: Srivastava, V., Mehrotra, S., Mishra, S. (eds) Hairy Roots. Springer, Singapore. https://doi.org/10.1007/978-981-13-2562-5_12

Download citation

Publish with us

Policies and ethics