Skip to main content
Log in

Plasma membrane H+-ATPase is involved in methyl jasmonate-induced root hair formation in lettuce (Lactuca sativa L.) seedlings

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Our results show that methyl jasmonate induces plasma membrane H + -ATPase activity and subsequently influences the apoplastic pH of trichoblasts to maintain a cell wall pH environment appropriate for root hair development.

Abstract

Root hairs, which arise from root epidermal cells, are tubular structures that increase the efficiency of water absorption and nutrient uptake. Plant hormones are critical regulators of root hair development. In this study, we investigated the regulatory role of the plasma membrane (PM) H+-ATPase in methyl jasmonate (MeJA)-induced root hair formation. We found that MeJA had a pronounced effect on the promotion of root hair formation in lettuce seedlings, but that this effect was blocked by the PM H+-ATPase inhibitor vanadate. Furthermore, MeJA treatment increased PM H+-ATPase activity in parallel with H+ efflux from the root tips of lettuce seedlings and rhizosphere acidification. Our results also showed that MeJA-induced root hair formation was accompanied by hydrogen peroxide accumulation. The apoplastic acidification acted in concert with reactive oxygen species to modulate root hair formation. Our results suggest that the effect of MeJA on root hair formation is mediated by modulation of PM H+-ATPase activity.

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

Similar content being viewed by others

References

  • An LJ, Zhou ZJ, Sun LL, Xi WY, Yu N, Cai WJ, Chen XJ, Yu H, Schiefelbein J, Gan YB (2012) Azinc finger protein gene ZFP5 integrates phytohormone signaling to control root hair development in Arabidopsis. Plant J 72:474–490

    Article  CAS  PubMed  Google Scholar 

  • Baluška F, Salaj J, Mathur J, Braun M, Jasper F, Sâmaj J, Chua N-H, Barlow PW, Volkmann D (2000) Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges. Dev Biol 227:618–632

    Article  PubMed  Google Scholar 

  • Bibikova T, Gilroy S (2008) Calcium in root hair growth. In: Emons AMC, Ketelaar T (eds) Root hairs: excellent tools for the study of plant molecular cell biology. Springer, Berlin. doi:10.1007/7089_2008_3

    Google Scholar 

  • Bibikova TN, Zhigilei A, Gilroy S (1997) Root hair growth in Arabidopsis thaliana is directed by calcium and an endogenous polarity. Planta 203:495–505

    Article  CAS  PubMed  Google Scholar 

  • Bibikova TN, Jacob T, Dahse I, Gilroy S (1998) Localized changes in apoplastic and cytoplasmic pH are associated with root hair development in Arabidopsis thaliana. Development 125:2925–2934

    CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Bloch D, Monshausen G, Singer M, Gilroy S, Yalovsky S (2011) Nitrogen source interacts with ROP signalling in root hair tip-growth. Plant Cell Environ 34:76–88

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  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 Central  CAS  PubMed  Google Scholar 

  • de Keijzer MN, Emons AMC, Mulder BM (2008) Modeling tip growth: pushing ahead. In: Emons AMC, Ketelaar T (eds) Root hairs: excellent tools for the study of plant molecular cell biology. Springer, Berlin. doi:10.1007/7089_2008_7

    Google Scholar 

  • De Michele R, Vurro E, Rigo C, Costa A, Elviri L, Di Valentin M, Careri M, Zottini M, Sanitadi Toppi L, Lo Schiavo F (2009) Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol 150:217–228

    Article  PubMed Central  PubMed  Google Scholar 

  • Devoto A, Turner JG (2003) Regulation of jasmonate-mediated plant responses in Arabidopsis. Ann Bot 92:329–337

    Article  PubMed Central  CAS  PubMed  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 

  • Dreher K, Callis J (2007) Ubiquitin, hormones and biotic stress in plants. Ann Bot 99:787–822

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dunlop J, Gardiner S (1993) Phosphate uptake, proton extrusion and membrane electropotentials of phosphorus deficient Trifolium repens L. J Exp Bot 44:1801–1808

    Article  CAS  Google Scholar 

  • Ewens M, Leigh RA (1985) The effect of nutrient solution composition on the length of root hair of wheat (Triticum aestivum L.). J Exp Bot 36:713–724

    Article  CAS  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JH (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    Article  CAS  PubMed  Google Scholar 

  • Frías I, Caldeira MT, Pérez-Castiiieira JR, Navarro-Aviñó Juan P, Culiaiiez-Maciá FA, Kuppinger O, Stransky H, Pagés M, Hager A, Serrano R (1996) A major isoform of the maize plasma membrane H+-ATPase: characterization and induction by auxin in coleoptiles. Plant Cell 8:1533–1544

    PubMed Central  PubMed  Google Scholar 

  • Gutjahr C, Riemann M, Müller A, Düchting P, Weiler EW, Nick P (2005) Cholodny-Went revisited: a role for jasmonate in gravitropism of rice coleoptiles. Planta 222:575–585

    Article  CAS  PubMed  Google Scholar 

  • Hager A (2003) Role of the plasma membrane H+-ATPase in auxin induced elongation growth: historical and new aspects. J Plant Res 116:483–505

    Article  CAS  PubMed  Google Scholar 

  • Haruta M, Sabat G, Stecker K, Minkoff BB, Sussman MR (2014) A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343:408–411

    Article  CAS  PubMed  Google Scholar 

  • Hayashi Y, Takahashi K, Inoue S, Kinoshita T (2014) Abscisic acid suppresses hypocotyl elongation by dephosphorylating plasma membrane H+-ATPase in Arabidopsis thaliana. Plant Cell Physiol 55:845–853

    Article  CAS  PubMed  Google Scholar 

  • Hentrich M, Böttcher C, Düchting P, Cheng Y, Zhao Y, Berkowitz O, Masle J, Medina J, Pollmann S (2013) The jasmonic acid signaling pathway is linked to auxin homeostasis through the modulation of YUCCA8 and YUCCA9 gene expression. Plant J l74:626–637

    Article  Google Scholar 

  • Hildmann T, Ebneth M, Pena-Cortes H, Sanchez-Serrano JJ, Willmitzer L, Prat S (1992) General roles of abscisic and jasmonic acids in gene activation as a result of mechanical wounding. Plant Cell 4:1157–1170

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hoffmann M, Hentrich M, Pollmann S (2011) Auxin-oxylipin crosstalk: relationship of antagonists. J Integr Plant Biol 53:429–445

    Article  CAS  PubMed  Google Scholar 

  • Hohm T, Demarsy E, Quan C, Allenbach PL, Preuten T, Vernoux T, Bergmann S, Fankhauser C (2014) Plasma membrane H+-ATPase regulation is required for auxin gradient formation preceding phototropic growth. Mol Syst Biol 10:751

    Article  PubMed Central  PubMed  Google Scholar 

  • Howe GA (2004) Jasmonates as signals in the wound response. J Plant Growth Regul 23:223–237

    Article  CAS  Google Scholar 

  • Huang GQ, Li E, Ge FR, Li S, Wang Q, Zhang CQ, Zhang Y (2013) Arabidopsis RopGEF4 and RopGEF10 are important for FERONIA-mediated developmental but not environmental regulation of root hair growth. New Phytol 200:1089–1101

    Article  CAS  PubMed  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 

  • Islam MM, Hossain MA, Jannat R, Munemasa S, Nakamura Y, Mori IC, Murata Y (2010) Cytosolic alkalization and cytosolic calcium oscillation in Arabidopsis guard cells response to ABA and MeJA. Plant Cell Physiol 51:1721–1730

    Article  CAS  PubMed  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. Plant Cell 14:763–776

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jones AR, Kramer EM, Swarup R, Bennett M, Lazarus CM (2009) Auxin transport through non-hair cells sustains root-hair development. Nat Cell Biol 11:78–84

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ketelaar T, Emons AM (2008) The actin cytoskeleton in root hairs: a cell elongation device. In: Emons AMC, Ketelaar T (eds) Root hairs: excellent tools for the study of plant molecular cell biology. Springer, Berlin. doi:10.1007/7089_2008_8

    Google Scholar 

  • Kwasniewski M, Chwialkowska K, Kwasniewska J, Kusak J, Siwinski K, Szarejko I (2013) Accumulation of peroxidase-related reactive oxygen species in trichoblasts correlates with root hair initiation in barley. J Plant Physiol 170:185–195

    Article  CAS  PubMed  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 Central  CAS  PubMed  Google Scholar 

  • Li L, Li C, Lee GI, Howe GA (2002) Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc Natl Acad Sci USA 99:6416–6421

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lin CY, Huanga LY, Chia WC, Huanga TL, Kakimotob T, Tsaia CR, Huanga HJ (2014) Pathways involved in vanadate-induced root hair formation in Arabidopsis. Physiol Plant. doi:10.1111/ppl.12229

    Google Scholar 

  • Miller DD, de Ruijter NCA, Bisseling T, Emons AMC (1999) The role of actin in root hair morphogenesis: studies with lipochito-oligosaccharide as a growth stimulator and cytochalasin as an actin perturbing drug. Plant J 17:141–154

    Article  CAS  Google Scholar 

  • Monshausen GB, Bibikova TN, Messerli MA, Shi C, Gilroy S (2007) Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc Natl Acad Sci USA 104:20996–21001

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE, Ecker JR, Reed JW (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132:4107–4118

    Article  CAS  PubMed  Google Scholar 

  • Nechay BR (1984) Mechanisms of action of vanadium. Annu Rev Pharmacol Toxicol 24:501–524

    Article  CAS  PubMed  Google Scholar 

  • Nielsen E (2008) Plant cell wall biogenesis during tip growth in root hair cells. In: Emons AMC, Ketelaar T (eds) Root hairs : excellent tools for the study of plant molecular cell biology. Springer, Berlin. doi:10.1007/7089_2008_11

    Google Scholar 

  • Overmyer K, Tuominen H, Kettunen R, Betz C, Langebartels C, Sandermann H, Kangasjarvi J (2000) Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. Plant Cell 12:1849–1862

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Paciorek T, Zazímalová E, Ruthardt N, Petrásek J, Stierhof YD, Kleine-Vehn J, Morris DA, Emans N, Jürgens G, Geldner N, Friml J (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435:1251–1256

    Article  CAS  PubMed  Google Scholar 

  • Palmgren MG (2001) Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52:817–845

    Article  CAS  PubMed  Google Scholar 

  • Payne RJH, Grierson CS (2009) A theoretical model for ROP localization by auxin in Arabidopsis root hair cells. PLoS ONE 4(12):e8337. doi:10.1371/journal.pone.0008337

    Article  PubMed Central  PubMed  Google Scholar 

  • Pemberton LM, Tsai SL, Lovell PH, Harris PJ (2001) Epidermal patterning in seedlings roots of eudicotyledons. Ann Bot 87:649–654

    Article  Google Scholar 

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

    Article  CAS  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 

  • Rayle DL, Cleland R (1970) Enhancement of wall loosening and elongation by acid solutions. Plant Physiol 46:250–253

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rayle DL, Cleland RE (1980) Evidence that auxin-induced growth of soybean hypocotyls involves proton excretion. Plant Physiol 66:433–437

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rayle DL, Cleland RE (1992) The acid growth theory of auxin-induced cell elongation is alive and well. Plant Physiol 99:1271–1274

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ridge RW (1995) Micro-vesicles, pyriform vesicles and macro-vesicles associated with the plasma membrane in the root hairs of Vicia hirsute after freeze-substitution. J Plant Res 108:363–368

    Article  Google Scholar 

  • Rigas S, Ditengou FA, Ljung K, Daras G, Tieta O, Palme K, Hatzopoulos P (2013) Root gravitropism and root hair development constitute coupled developmental responses regulated by auxin homeostasis in the Arabidopsis root apex. New Phytol 197:1130–1141

    Article  CAS  PubMed  Google Scholar 

  • Rober-Kleber N, Albrechtová JTP, Fleig S, Huck N, Michalke W, Wagner E, Speth V, Neuhaus G, Fischer-Iglesias C (2003) Plasma membrane H+-ATPase is involved in auxin-mediated cell elongation during wheat embryo development. Plant Physiol 131:1302–1312

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Robert S, Kleine-Vehn J, Barbez E, Sauer M, Paciorek T, Baster P, Vanneste S, Zhang J, Simon S, Covanova M, Hayashi K, Dhonukshe P, Yang Z, Bednarek SY, Jones AM, Luschnig C, Aniento F, Zazimalova E, Friml J (2010) ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 143:111–121

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Römheld V, Müller Ch, Marschner H (1984) Localization and capacity of proton pumps in roots of intact sunflower plants. Plant Physiol 76:603–606

    Article  PubMed Central  PubMed  Google Scholar 

  • Seo JS, Joo J, Kim MJ, Kim YK, Nahm BH, Song SI, Cheong JJ, Lee JS, Kim JK, Choi YD (2011) OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J 65:907–921

    Article  CAS  PubMed  Google Scholar 

  • Spartz AK, Ren H, Park MY, Grandt KN, Lee SH, Murphy AS, Sussman MR, Overvoorde PJ, Gray WM (2014) SAUR inhibition of PP2C-D phosphatases activates plasma membrane H+-ATPases to promote cell expansion in Arabidopsis. Plant Cell 26:2129–2142

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sun J, Xu Y, Ye S, Jiang H, Chen Q, Liu F, Zhou W, Chen R, Li X, Tietz O, Wu X, Cohen JD, Palme K, Li C (2009) Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation. Plant Cell 21:1495–1511

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sun J, Chen Q, Qi L, Jiang H, Li S, Xu Y, Liu F, Zhou W, Pan J, Li X, Palme K, Li C (2011) Jasmonate modulates endocytosis and plasma membrane accumulation of the Arabidopsis PIN2 protein. New Phytol 191:360–375

    Article  CAS  PubMed  Google Scholar 

  • Sundaravelpandian K, Chandrika NNP, Schmidt W (2013) PFT1, a transcriptional mediator complex subunit, controls root hair differentiation through reactive oxygen species (ROS) distribution in Arabidopsis. New Phytol 197:151–161

    Article  CAS  PubMed  Google Scholar 

  • Takahashi K, Hayashi K, Kinoshita T (2012) Auxin activates the plasma membrane H+-ATPase by phosphorylation during hypocotyl elongation in Arabidopsis. Plant Physiol 159:632–641

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tanaka N, Kato M, Tomioka R, Kurata R, Fukao Y, Aoyama T, Maeshima M (2014) Characteristics of a root hair-less line of Arabidopsis thaliana under physiological stresses. J Exp Bot 65:1497–1512

    Article  PubMed Central  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Wang Y, Noguchi K, Ono N, Inoue S, Terashima I, Kinoshita T (2014) Overexpression of plasma membrane H+-ATPase in guard cells promotes light-induced stomatal opening and enhances plant growth. Proc Natl Acad Sci USA 111:533–538

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot 111:1021–1058

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wu J, Kurten EL, Monshausen G, Hummel GM, Gilroy S, Baldwin IT (2007) NaRALF, a peptide signal essential for the regulation of root air tip apoplastic pH in Nicotiana attenuata, is required for root hair development and plant growth in native soils. Plant J 52:877–890

    Article  CAS  PubMed  Google Scholar 

  • Wu MZ, HuangJJ XuS, Ling TF, Xie YJ, Shen WB (2011) Haem oxygenase delays programmed cell death in wheat aleurone layers by modulation of hydrogen peroxide metabolism. J Exp Bot 62:235–248

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wymer CL, Bibikova TN, Gilroy S (1997) Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant J 12:427–439

    Article  CAS  PubMed  Google Scholar 

  • Xu WF, Jia LG, BaluŠka F, Ding GC, Shi WM, Ye NH, Zhang JH (2012) PIN2 is required for the adaptation of Arabidopsis roots to alkaline stress by modulating proton secretion. J Exp Bot 63:6105–6114

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xu WF, Jia LG, Shi WM, Liang JS, Zhou F, Li QF, Zhang JH (2013) Abscisic acid accumulation modulates auxin transport in the root tip to enhance proton secretion for maintaining root growth under moderate water stress. New Phytol 197:139–150

    Article  CAS  PubMed  Google Scholar 

  • Yan SL, Dong SS, Zhang RX, Shen YB (2014) Relationship of H2O2 accumulation and plasma membrane H+-ATPase in Arabidopsis thaliana guard cells response to MeJA. Acta Botanica Boreali Occidentalia Sinica 34:298–303

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zhu YY, Di TJ, Xu GH, Chen X, Zeng HQ, Yan F, Shen QR (2009) Adaptation of plasma membrane H+-ATPase of rice roots to low pH as related to ammonium nutrition. Plant Cell Environ 32:1428–1440

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was funded by the National Natural Science Foundation of China (grant No. J1210056). We are grateful to Prof. Y. Y. Zhu of Nanjing agricultural university for technical support and to anonymous reviewers for valuable comments and suggestions for revising the manuscript.

Conflict of interest

All authors read and agreed with the final manuscript and have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Kai Xia or Lijun Gan.

Additional information

Communicated by E. Guiderdoni.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 598 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhu, C., Yang, N., Ma, X. et al. Plasma membrane H+-ATPase is involved in methyl jasmonate-induced root hair formation in lettuce (Lactuca sativa L.) seedlings. Plant Cell Rep 34, 1025–1036 (2015). https://doi.org/10.1007/s00299-015-1762-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-015-1762-4

Keywords

Navigation