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