Journal of Plant Growth Regulation

, Volume 37, Issue 2, pp 438–451 | Cite as

Jasmonic Acid-Ethylene Crosstalk via ETHYLENE INSENSITIVE 2 Reprograms Arabidopsis Root System Architecture Through Nitric Oxide Accumulation

  • Salvador Barrera-Ortiz
  • Amira Garnica-Vergara
  • Saraí Esparza-Reynoso
  • Elizabeth García-Cárdenas
  • Javier Raya-González
  • León Francisco Ruiz-Herrera
  • José López-Bucio


Plant growth and development are tightly regulated by phytohormones, including jasmonic acid (JA) and ethylene (ET), two canonical players in plant defense and in the control of root system architecture. Here, we show that JA inhibits primary root growth and promotes lateral root development while inducing nitric oxide (NO) accumulation in the wild-type (WT) primary root, but not in jar1-1, coi1-1, myc2-1, and myc2-2 Arabidopsis mutants defective in JA biosynthesis or response. NO-related mutants nia1/nia2 and Atnoa1 were indistinguishable in root architectural responses to JA when compared to WT seedlings, and the developmental changes were apparently unrelated to reactive oxygen species (ROS) accumulation. Root growth inhibition by the NO donor, sodium nitroprusside (SNP), was reduced in coi1-1 mutants, and NO accumulation induced the expression of the downstream repressors JAZ1 and JAZ10 at the differentiation and/or meristematic root regions. Comparison of growth of WT, ein2-1, jar1-1, and ein2-1/jar1-1 mutants further revealed a critical role of ETHYLENE INSENSITIVE2 (EIN2) in mediating both JA and NO root sensing. Our results suggest that NO mediates JA signaling during the configuration of the Arabidopsis root system architecture and that EIN2 plays a role in this developmental program.


Arabidopsis Jasmonic acid Nitric oxide Root development Phytohormones 



This work was supported by grants from the Consejo Nacional de Ciencia y Tecnología (CONACYT, México, Grant No. 177775) and the Consejo de la Investigación Científica (UMSNH, México, Grant No. CIC 2.26). Salvador Barrera-Ortiz and Amira Garnica-Vergara are indebted to CONACYT for a doctoral fellowship, and Saraí Esparza-Reynoso and Elizabeth García-Cárdenas are indebted to CONACYT for masters scholarships. Kind donation of Arabidopsis lines by Drs. Keiko Torii, and Alain Goossens are appreciated.

Supplementary material

344_2017_9741_MOESM1_ESM.pdf (343 kb)
Supplementary material 1 (PDF 342 KB)


  1. Ahlfors R, Lang S, Overmyer K, Jaspers P, Brosché M, Tauriainen A, Kollist H, Tuominen H, Belles-Boix E, Piippo M, Inzé D, Palva ET, Kangasjärvi J (2004) Arabidopsis RADICAL-INDUCED CELL DEATH1 belongs to the WWE protein-protein interaction domain protein family and modulates abscisic acid, ethylene, and methyl jasmonate responses. Plant Cell 16:1925–1937CrossRefPubMedPubMedCentralGoogle Scholar
  2. Blancaflor EB, Kilaru A, Keereetaweep J, Khan BR, Faure L, Chapman KD (2014) N-acylethanolamines: lipid metabolites with functions in plant growth and development. Plant J 79:568–583CrossRefPubMedGoogle Scholar
  3. Campos-Cuevas JC, Pelagio-Flores R, Raya-González J, Méndez-Bravo A, Ortiz-Castro R, López-Bucio J (2008) Tissue culture of Arabidopsis thaliana explants reveals a stimulatory effect of alkamides on adventitious root formation and nitric oxide accumulation. Plant Sci 174:165–173CrossRefGoogle Scholar
  4. Chen Q, Sun J, Zhai Q, Zhou W, Qi L, Xu L, Wang B, Chen R, Jiang H, Qi J, Li X, Palme K, Li C (2011) The basic helix-loop-helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis. Plant Cell 23:3335–3352CrossRefPubMedPubMedCentralGoogle Scholar
  5. Chini A, Fonseca S, Fernández G, Adie B, Chico JM, Lorenzo O, García-Casado G, López-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671CrossRefPubMedGoogle Scholar
  6. Chung HS, Howe GA (2009) A critical role for the TIFY motif in repression of jasmonate signaling by a stabilized splice variant of the JASMONATE ZIM-domain protein JAZ10 in Arabidopsis. Plant Cell 21:131–145CrossRefPubMedPubMedCentralGoogle Scholar
  7. Fernández-Marcos M, Sanz L, Lewis D, Muday GK, Lorenzo O (2012) Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport. Proc Natl Acad Sci USA 108:18506–18511CrossRefGoogle Scholar
  8. Feys BJF, Benedetti CE, Penfold CN, Turner JG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male-sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6:751–759CrossRefPubMedPubMedCentralGoogle Scholar
  9. Fujibe T, Saji H, Arakawa K, Yabe N, Takeuchi Y, Yamamoto KT (2004) A methyl viologen-resistant mutant of Arabidopsis, which is allelic to ozone-sensitive rcd1, is tolerant to supplemental ultraviolet-B irradiation. Plant Physiol 134:275–285CrossRefPubMedPubMedCentralGoogle Scholar
  10. Gasperini D, Chételat A, Acosta IF, Goossens J, Pauwels L, Goossens A, Dreos R, Alfonso E, Farmer E (2015) Multilayered organization of jasmonate signalling in the regulation of root growth. PLoS Genet 11:e1005300CrossRefPubMedPubMedCentralGoogle Scholar
  11. Gibbs DL, Isa MD, Movahedi M, Lozano-Juste J, Mendiondo GM, Berckhan S, Marin-de la Rosa N, Conde JV, Sousa Correia C, Pearce SP, Bassel GW, Hamali B, Talloji P, Tome DFA, Coego A, Beynon J, Alabadí D, Bachmair A, León J, Gray JE, Theodoulou FL, Holdsworth MJ (2014) Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors. Mol Cell 53:369–379CrossRefPubMedPubMedCentralGoogle Scholar
  12. Greger H (2016) Alkamides: a critical reconsideration of a multifunctional class of unsaturated fatty acid amides. Phytochem Rev 15:729–770CrossRefGoogle Scholar
  13. Grunewald W, Vanholme B, Pauwels L, Plovie E, Inze D, Gheysen G, Goossens A (2009) Expression of the Arabidopsis jasmonate signaling repressor JAZ1/TIFY10A is stimulated by auxin. EMBO Rep 10:923–928CrossRefPubMedPubMedCentralGoogle Scholar
  14. Guo FQ, Okamoto M, Crawford NM (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signalling. Science 302:100–103CrossRefPubMedGoogle Scholar
  15. Guzmán P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2:513–523CrossRefPubMedPubMedCentralGoogle Scholar
  16. Huang X, Stettmaier K, Michel C, Hutzler P, Mueller MJ, Durner J (2004) Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana. Planta 218:938–946CrossRefPubMedGoogle Scholar
  17. Kasten D, Mithöfer A, Georgii E, Lang H, Durner J, Gaupels F (2016) Nitrite is the driver, phytohormones are modulators while NO and H2O2 act as promoters of NO2-induced cell death. J Exp Bot 67:6337–6349CrossRefPubMedGoogle Scholar
  18. Lorenzo O, Piqueras R, Sánchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15:165–178CrossRefPubMedPubMedCentralGoogle Scholar
  19. Méndez-Bravo A, Raya-González J, Herrera-Estrella L, López-Bucio J (2010) Nitric oxide is involved in alkamide-induced lateral root development in Arabidopsis. Plant Cell Physiol 51:1612–1626CrossRefPubMedGoogle Scholar
  20. Méndez-Bravo A, Calderón-Vázquez C, Ibarra-Laclette E, Raya-González J, Ramírez-Chávez E, Molina-Torres J, Guevara-García A, López-Bucio J, Herrera-Estrella L (2011) Alkamides activate jasmonic acid biosynthesis and signaling pathways and confer resistance to Botrytis cinerea in Arabidopsis thaliana. PLoS ONE 6:e27251CrossRefPubMedPubMedCentralGoogle Scholar
  21. Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309CrossRefPubMedGoogle Scholar
  22. Mur LAJ, Laarhoven L, Harren FJM, Hall MA, Smith AR (2008) Nitric oxide interacts with salicylate to regulate biphasic ethylene production during the hypersensitive response. Plant Physiol 148:1537–1546CrossRefPubMedPubMedCentralGoogle Scholar
  23. Ortiz-Castro R, Martínez-Trujillo M, López-Bucio J (2008) N-acyl-L-homoserine lactones: a class of bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana. Plant Cell Environ 31:1497–1509CrossRefPubMedGoogle Scholar
  24. Park BS, Song JT, Seo HS (2011) Arabidopsis nitrate reductase activity is stimulated by the E3 SUMO ligase AtSIZ1. Nat Commun 2:400CrossRefPubMedPubMedCentralGoogle Scholar
  25. Pauwels L, Barbero GF, Geerinck J, Tilleman S, Grunewald W, Cuéllar Pérez A, Chico JM, vanden Bossche R, Sewell J, Gil E, García-Casado G, Witters E, Inzé D, Long JA, De Jaeger G, Solano R, Goossens A (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464:788–791CrossRefPubMedPubMedCentralGoogle Scholar
  26. Pelagio-Flores R, Ruiz-Herrera LF, López-Bucio J (2016) Serotonin modulates Arabidopsis root growth via changes in reactive oxygen species and jasmonic acid-ethylene signaling. Physiol Plant 158:92–105CrossRefPubMedGoogle Scholar
  27. Penninckx IA, Thomma BP, Buchala A, Métraux 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 10:2103–2113CrossRefPubMedPubMedCentralGoogle Scholar
  28. Pillitteri LJ, Peterson KM, Horst RJ, Torii KU (2011) Molecular profiling of stomatal meristemoids reveals new component of asymmetric cell division and commonalities among stem cell populations in Arabidopsis. Plant Cell 23:3260–3275CrossRefPubMedPubMedCentralGoogle Scholar
  29. Plett JM, Khachane A, Ouassou M, Sundberg B, Kohler A, Martin F (2014) Ethylene and jasmonic acid act as negative modulators during mutualistic symbiosis between Laccaria bicolor and Populus roots. New Phytol 202:270–286CrossRefPubMedGoogle Scholar
  30. Ramírez-Chávez E, López-Bucio J, Herrera-Estrella L, Molina-Torres J (2004) Alkamides isolated from plants promote growth and alter root development in Arabidopsis. Plant Physiol 134:1058–1068CrossRefPubMedPubMedCentralGoogle Scholar
  31. Raya-González J, Pelagio-Flores R, López-Bucio J (2012) The jasmonate receptor COI1 plays a role in jasmonate-induced lateral root formation and lateral root positioning in Arabidopsis thaliana. J Plant Physiol 169:1348–1358CrossRefPubMedGoogle Scholar
  32. Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot 53:103–110CrossRefPubMedGoogle Scholar
  33. Santolini J, Andre F, Jeandroz S, Wendehenne D (2017) Nitric oxide synthase in plants: where do we stand? Nitric Oxide 63:30–38CrossRefPubMedGoogle Scholar
  34. Schlicht M, Ludwig-Muller J, Burbach C, Volkmann D, Baluska F (2013) Indole-3-butyric acid induces lateral root formation via peroxisome-derived indole-3-acetic acid and nitric oxide. New Phytol 200:473–482CrossRefPubMedGoogle Scholar
  35. Staswick PE, Su W, Howell SH (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci USA 89:6837–6840CrossRefPubMedPubMedCentralGoogle Scholar
  36. Street I, Aman S, Zubo Y, Ramzan A, Wang X, Shakeel S, Kieber J, Schaller G (2015) Ethylene inhibits cell proliferation of the Arabidopsis root meristem. Plant Physiol 169:338–350CrossRefPubMedPubMedCentralGoogle Scholar
  37. Sudhamsu J, Lee GI, Klessig DF, Crane BR (2008) The structure of YqeH. An AtNOS1/AtNOA1 ortholog that couples GTP hydrolysis to molecular recognition. J Biol Chem 283:32968–32976CrossRefPubMedPubMedCentralGoogle Scholar
  38. Terrile MC, París R, Calderón-Villalobos LI, Iglesias MJ, Lamattina L, Estelle M, Casalongué CA (2012) Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. Plant J 70:492–500CrossRefPubMedPubMedCentralGoogle Scholar
  39. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448:661–665CrossRefPubMedGoogle Scholar
  40. Thomann A, Lechner E, Hansen M, Dumbliauskas E, Parmentier Y, Kieber J, Scheres B, Genschik P (2009) Arabidopsis CULLIN3 genes regulate primary root growth and patterning by ethylene-dependent and independent mechanisms. PLoS Genet 5:e1000328CrossRefPubMedPubMedCentralGoogle Scholar
  41. Wendehenne D, Hancock JT (2011) New frontiers in nitric oxide biology in plant. Plant Sci 181:507–508CrossRefPubMedGoogle Scholar
  42. Wilkinson JQ, Crawford NM (1993) Identification and characterization of a chlorate-resistant mutant of Arabidopsis thaliana with mutations in both nitrate reductase structural genes NIA1 and NIA2. Mol Gen Genet 239:289–297PubMedGoogle Scholar
  43. Xu Y, Chang P, Liu D, Narasimhan ML, Raghothama KG, Hasegawa PM, Bressan RA (1994) Plant defense genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell 6:1077–1108CrossRefPubMedPubMedCentralGoogle Scholar
  44. Xu L, Liu F, Lechner E, Genschik P, Crosby WL, Ma H, Peng W, Huang D, Xie D (2002) The SCF(COI1) ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell 14:1919–1935CrossRefPubMedPubMedCentralGoogle Scholar
  45. Xu MJ, Dong JF, Zhu MY (2005) Nitric oxide mediates the fungal elicitor-induced hypericin production of Hypericum perforatum cell suspension cultures through a jasmonic-acid-dependent signal pathway. Plant Physiol 139:991–998CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Salvador Barrera-Ortiz
    • 1
  • Amira Garnica-Vergara
    • 1
  • Saraí Esparza-Reynoso
    • 1
  • Elizabeth García-Cárdenas
    • 1
  • Javier Raya-González
    • 1
  • León Francisco Ruiz-Herrera
    • 1
  • José López-Bucio
    • 1
  1. 1.Instituto de Investigaciones Químico-BiológicasUniversidad Michoacana de San Nicolás de HidalgoMoreliaMéxico

Personalised recommendations