Skip to main content
SpringerLink
Log in

Ammonium-Stimulated Root Hair Branching is Enhanced by Methyl Jasmonate and Suppressed by Ethylene in Arabidopsis thaliana

  • Original Research
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Root hair development is orchestrated by nutritional factors and plant hormones. We investigated the action of ammonium (NH +4 ) and its interactions with methyl jasmonate (MeJA) and ethylene in Arabidopsis root hair growth. The formation of root hair branches was dramatically stimulated in media containing 1.25 to 20 mM NH +4 at pH values of 4.0 to 6.5. The NH +4 -treated root hairs showed a very short tip growth stage and swells on the sides that indicated the emergence of branches. MeJA (0.08 to 10 μM) worked in synergism with NH +4 to enhance hair branching. In contrast, ethylene had an antagonistic effect; the stimulation of hair branching by NH +4 was suppressed by the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) and was diminished in ethylene-overproducing mutant eto1-1 seedlings. Moreover, the application of Ag+, an ethylene inhibitor, reduced the ACC-induced inhibition of NH +4 -stimulated hair branching and restored NH +4 -stimulated hair branching in eto1-1 seedlings. Thus, the actions of jasmonate and ethylene appear to be dependent on nutritional conditions such as available nitrogen.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ACC 1:

Aminocyclopropane-1-carboxylic acid

AVG:

Aminoethoxyvinylglycine

AOA:

Aminooxyacetic acid

IAA:

Indole-3 acetic acid

JA:

Jasmonic acid

MeJA:

Methyl jasmonate

ROS:

Reactive oxygen species

References

  • Adams E, Turner J (2010) COI1, a jasmonate receptor, is involved in ethylene-induced inhibition of Arabidopsis root growth in the light. J Exp Bot. doi:10.1093/jxb/erq240

    Google Scholar 

  • Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19:529–538

    Article  CAS  Google Scholar 

  • Bibikova TN, Blancaflor EB, Gilroy S (1999) Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. Plant J 17:657–665

    Article  PubMed  CAS  Google Scholar 

  • Bijlsma RJ, Lambers H, Kooijman SALM (2000) A dynamic whole plant model of integrated metabolism of nitrogen and carbon. 1. Comparative ecological implications of ammonium–nitrate interactions. Plant Soil 220:49–69

    Article  CAS  Google Scholar 

  • Bloch D, Monshausen G, Singer M, Gilroy S, Yalovsky S (2010) Nitrogen source interacts with ROP signalling in root hair tip-growth. Plant Cell Environ. doi:10.1111/j.1365-3040.2010.02227.x

    PubMed  Google Scholar 

  • Britto DT, Kronzucker HJ (2001) Constancy of nitrogen turnover kinetics in the plant cell: insights into the integration of subcellular N fluxes. Planta 213:175–181

    Article  PubMed  CAS  Google Scholar 

  • Britto DT, Kronzucker HJ (2002) NH +4 toxicity in higher plants: a critical review. J Plant Physiol 159:567–584

    Article  CAS  Google Scholar 

  • Carol RJ, Dolan L (2002) Building a hair: tip growth in Arabidopsis thaliana root hairs. Phil Trans R Soc Lond 357:815–821

    Article  CAS  Google Scholar 

  • Carol RJ, Dolan L (2006) The role of reactive oxygen species in cell growth: lessons from root hairs. J Exp Bot 57:1829–1834

    Article  PubMed  CAS  Google Scholar 

  • Carol RJ, Takeda S, Linstead P, Durrant MC, Kakesova H, Derbyshire P, Drea S, Zarsky V, Dolan L (2005) A RhoGDP dissociation inhibitor spatially regulates growth in root hair cell. Nature 438:1013–1016

    Article  PubMed  CAS  Google Scholar 

  • Cho M, Lee SH, Cho HT (2007) P-glycoprotein4 displays auxin efflux transporter like action in Arabidopsis root hair cells and tobacco cells. Plant Cell 19:3930–3943

    Article  PubMed  CAS  Google Scholar 

  • Dolan L, Duckett CM, Grierson C, Linstead P, Schneider K, Lawson E, Dean C, Poethig S, Roberts K (1994) Clonal relationships and cell patterning in the root epidermis of Arabidopsis. Development 120:2465–2474

    CAS  Google Scholar 

  • Ellis C, Turner JG (2001) The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell 13:1025–1033

    Article  PubMed  CAS  Google Scholar 

  • Ellis C, Turner JG (2002) A conditionally fertile coi1 allele indicates cross-talk between plant hormone signalling pathways in Arabidopsis thaliana seeds and young seedlings. Planta 215:549–556

    Article  PubMed  CAS  Google Scholar 

  • Forde BG (2002) Local and long-range signaling pathways regulation plant responses to nitrate. Annu Rev Plant Biol 53:203–224

    Article  PubMed  CAS  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    Article  PubMed  CAS  Google Scholar 

  • Galway ME, Heckman JW, Schiefelbein JW (1997) Growth and ultrastructure of Arabidopsis root hairs: the rhd3 mutation alters vacuole enlargement and tip growth. Planta 201:209–218

    Article  PubMed  CAS  Google Scholar 

  • Gilroy S, Jones DL (2000) Through form to function: root hair development and nutrient uptake. Trends Plant Sci 5:56–60

    Article  PubMed  CAS  Google Scholar 

  • Grierson CS, Roberts K, Feldmann KA, Dolan L (1997) The COW1 locus of Arabidopsis acts after RHD2, and in parallel with RHD3 and TIP1, to determine the shape, rate of elongation, and number of root hairs produced from each site of hair formation. Plant Physiol 115:981–990

    Article  PubMed  CAS  Google Scholar 

  • Grierson CS, Parker JS, Kemp AC (2001) Arabidopsis genes with roles in root hair development. J Plant Nutr Soil Sci 164:131–140

    Article  CAS  Google Scholar 

  • Guo H, Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7:40–49

    Article  PubMed  CAS  Google Scholar 

  • Inoue Y, Yamaoka K, Kimura K, Sawai K, Arai T (2000) Effects of low pH on the induction of root hair formation in young lettuce (Lactuca sativa L. cv. Grand Rapids) seedlings. J Plant Res 113:39–44

    Article  Google Scholar 

  • Jones MA, Shen JJ, Fu Y, Li H, Yang Z, Grierson CS (2002) The Arabidopsis Rop2 GTPase is a positive regulator of both root hair initiation and tip growth. J Plant Res 14:763–776

    CAS  Google Scholar 

  • Kandasamy MK, McKinney EC, Meagher RB (2009) A single vegetative actin isovariant overexpressed under the control of multiple regulatory sequences is sufficient for normal Arabidopsis development. Plant Cell 21:701–718

    Article  PubMed  CAS  Google Scholar 

  • Kusano H, Testerink C, VermeerJEM TsugeT, Shimada H, Oka A, Munnik T, Aoyama T (2008) The Arabidopsis phosphatidylinositol phosphate 5-kinase PIP5K3 is a key regulator of root hair tip growth. Plant Cell 20:367–380

    Article  PubMed  CAS  Google Scholar 

  • Lee SH, Cho HT (2006) PINOID positively regulates auxin efflux in Arabidopsis root hair cell and tobacco cells. Plant Cell 18:1604–1616

    Article  PubMed  CAS  Google Scholar 

  • Libault M, Brechenmacher L, Cheng J, Xu D, Stacey G (2010) Root hair systems biology. Trends Plant Sci. doi:10.1016/j.tplants.2010.08.010

    PubMed  Google Scholar 

  • Lorenzo O, Piqueras R, Sanchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15:165–178

    Article  PubMed  CAS  Google Scholar 

  • Lynch JP (1998) Root architecture and phosphorus acquisition efficiency in common bean. In: Flores HE, Lynch JP, Eisenstat D (eds) Radical biology: advances and perspectives on the function of plant roots. American Society of Plant Physiologists, Rockville, pp 81–91

    Google Scholar 

  • Ma Z, Bielenberg DG, Brown KM, Lynch JP (2001) Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant Cell Environ 29:459–467

    Article  Google Scholar 

  • Masucci JD, Schiefellbein JW (1994) The rhd6 mutation of Arabidopsis thaliana alters root hair initiation through an auxin- and ethylene-associated process. Plant Physiol 106:1335–1346

    PubMed  CAS  Google Scholar 

  • Masucci JD, Schiefelbein JW (1996) Hormones act downstream of TTG and GL2 to promote root hair outgrowth during epidermis development in the Arabidopsis root. Plant Cell 8:1505–1517

    Article  PubMed  CAS  Google Scholar 

  • Müller M, Schmidt W (2004) Environmentally induced plasticity of root hair development in Arabidopsis. Plant Physiol 134:409–419

    Article  PubMed  Google Scholar 

  • Norman-Setterblad C, Vidal S, Palva ET (2000) Interacting signal pathways control defense gene expression in Arabidopsis in response to cell wall-degrading enzymes from Erwinia carotovora. Mol Plant Microbe Interact 4:430–438

    Article  Google Scholar 

  • Ovecka M, Nadubinska M, Volkmann D, Baluska F (2000) Actomyosin and exocytosis inhibitors alter root hair morphology in Poa annua. Biologia 55:105–114

    CAS  Google Scholar 

  • Ovecka M, Lang I, Baluska F, Ismail A, Illes P, Lichtscheidl IK (2005) Endocytosis and vesicle trafficking during tip growth of root hairs. Protoplasma 226:39–54

    Article  PubMed  CAS  Google Scholar 

  • Penninckx IAMA, Thomma BPHJ, Buchala A, Metraux JP, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10:2103–2113

    Article  PubMed  CAS  Google Scholar 

  • Parker JS, Cavell AC, Dolan L, Roberts K, Gierson CS (2000) Genetic interactions during root hair morphogenesis in Arabidopsis. Plant Cell 124:1961–1974

    Article  Google Scholar 

  • Pauwels L, Inzé D, Goossens A (2009) Jasmonate-inducible gene: what does it mean? Trends Plant Sci 14:87–91

    Article  PubMed  CAS  Google Scholar 

  • Person RL, Stevens LJ (2000) Evidence for the uptake of nonessential ions and essential nutrient ions by root hairs and their effect on root hair development. In: Ridge RW, Emons AMC (eds) Root hairs: cell and molecular biology. Springer, Tokyo, pp 179–195

    Google Scholar 

  • Pitts RJ, Cernac A, Estelle M (1998) Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J 16:553–560

    Article  PubMed  CAS  Google Scholar 

  • Pré M, Atallah M, Champion A, De Vos M, Pieterse CMJ, Memelink J (2008) The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol 147:1347–1357

    Article  PubMed  Google Scholar 

  • Rahman A, Hosokawa S, Oono Y, Amakawa T, Goto N, Tsurumi S (2002) Auxin and ethylene response interactions during Arabidopsis root hair development dissected by auxin influx modulators. Plant Physiol 130:1909–1917

    Article  Google Scholar 

  • Robinson D, Rorison IH (1987) Root hairs and plant growth at low nitrogen availabilities. New Phytol 107:681–693

    Article  Google Scholar 

  • Rojo E, Leon J, Sanchez-Serrano JJ (1999) Cross-talk between wound signalling pathways determines local versus systemic gene expression in Arabidopsis thaliana. Plant J 20:135–142

    Article  PubMed  CAS  Google Scholar 

  • Romera FJ, Alcántara E, De la Guardia MD (1999) Ethylene production by Fe-deficient roots and its involvement in the regulation of Fe-deficiency stress responses by strategy I plants. Ann Bot 83:51–55

    Article  CAS  Google Scholar 

  • Ryan E, Grierson CS, Cavell A, Steer M, Dolan L (1998) TIP1 is required for both tip growth and non-tip growth in Arabidopsis. New Phytol 138:49–58

    Article  Google Scholar 

  • Ryan E, Steer M, Dolan L (2001) Cell biology and genetics of root hair formation in Arabidopsis thaliana. Protoplasma 215:140–149

    Article  PubMed  CAS  Google Scholar 

  • Schiefelbein J, Galway M, Masucci J, Ford S (1993) Pollen-tube and root-hair tip growth is disrupted in a mutant of Arabidopsis thaliana. Plant Physiol 103:979–985

    Article  PubMed  CAS  Google Scholar 

  • Schmidt W, Tittel J, Schilora A (2000) Role of hormones in the induction of iron deficiency responses in Arabidopsis root. Plant Physiol 122:1109–1118

    Article  PubMed  CAS  Google Scholar 

  • Tanimoto M, Roberts K, Dolan L (1995) Ethylene is a positive regulator of root hair development in Arabidopsis thaliana. Plant J 8:943–948

    Article  PubMed  CAS  Google Scholar 

  • Thole JM, Vermeer JEM, Zhang Y, Gadella TWJ Jr, Nielsen E (2008) Root hair defective 4 encodes a phosphatidylinositol-4-phosphate phosphatase required for proper root hair development in Arabidopsis thaliana. Plant Cell 20:381–395

    Article  PubMed  CAS  Google Scholar 

  • Vitousek PM, Gosz JR, Grier CC, Melillo JM, Reiners WA (1982) A comparative analysis of potential nitrification and nitrate mobility in forest ecosystems. Ecol Monogr 52:155–177

    Article  CAS  Google Scholar 

  • Xu Y, Chang L, Liu D, Narasimhan ML, Raghothama KG, Hasewaga PM, Bressan RA (1994) Plant defence genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell 6:1077–1085

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–409

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Forde BG (2000) Regulation of Arabidopsis root development by nitrate availability. J Exp Bot 51:51–59

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Jennings A, Barlow PW, Forde BG (1999) Dual pathways for regulation of root branching by nitrate. Proc Natl Acad Sci USA 96:6529–6534

    Article  PubMed  CAS  Google Scholar 

  • Zhu CH, Gan LJ, Shen ZG, Xia K (2006) Interaction between jasmonates and ethylene in regulation of root hair development in Arabidopsis. J Exp Bot 57:1299–1308

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This work was supported by a grant from the National Natural Science Foundation of China (30871460).

Author information

Authors and Affiliations

  1. College of Life Sciences, Nanjing Agricultural University, Nanjing, 210095, China

    Na Yang, Changhua Zhu, Lijun Gan & Kai Xia

  2. NCA Biotech, Inc., 3406 Pomona Blvd., Pomona, CA, 91768, USA

    Denny Ng

Authors
  1. Na Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Changhua Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lijun Gan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Denny Ng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kai Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kai Xia.

Additional information

Na Yang and Changhua Zhu equally contributed to this article.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yang, N., Zhu, C., Gan, L. et al. Ammonium-Stimulated Root Hair Branching is Enhanced by Methyl Jasmonate and Suppressed by Ethylene in Arabidopsis thaliana . J. Plant Biol. 54, 92–100 (2011). https://doi.org/10.1007/s12374-011-9147-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-011-9147-x

Keywords

Search

Navigation