pp 1–12 | Cite as

The bacterial volatile dimethyl-hexa-decylamine reveals an antagonistic interaction between jasmonic acid and cytokinin in controlling primary root growth of Arabidopsis seedlings

  • Ernesto Vázquez-Chimalhua
  • León Francisco Ruíz-Herrera
  • Salvador Barrera-Ortiz
  • Eduardo Valencia-Cantero
  • José López-Bucio
Original Article


Chemical communication underlies major adaptive traits in plants and shapes the root microbiome. An increasing number of diffusible and/or volatile organic compounds released by bacteria have been identified, which play phytostimulant or protective functions, including dimethyl-hexa-decylamine (DMHDA), a volatile biosynthesized by Arthrobacter agilis UMCV2 that induces jasmonic acid (JA) signaling in Arabidopsis. Here, he found that the growth repressing effects of both DMHDA and JA are antagonized by kinetin and correlated with an inhibition of cytokinin-related ARR5::GUS and TCS::GFP expression in Arabidopsis primary roots. Moreover, we demonstrate that shoot supplementation of JA triggers JAZ1 expression both locally and systemically and represses cytokinin-dependent promoter activity in roots. A similar effect was observed after cotyledon wounding, in which an increase of JA-inducible LOX2:GUS expression represses root growth, which correlates with the loss of TCS::GFP detection at the very root tip. Our data demonstrate that the bacterial volatile DMHDA crosstalks with cytokinin signaling and reveals the downstream antagonistic interaction between JA and cytokinin in controlling root growth.


N-N-dimethyl-hexadecylamine Arabidopsis thaliana Jasmonic acid Cytokinin Root growth 


Funding information

The Coordinación de la Investigación Científica UMSNH (México) funded this work via projects 2.22 (EVC) and 2.26 (JLB).

Supplementary material

709_2018_1327_Fig9_ESM.png (2.3 mb)
Supplementary figure 1

JA upregulates expression of JAZ1 in nuclei of epidermal cells in cotyledons. Representative confocal images of epidermal cells of cotyledons 12 h after contact with 0.2X MS medium drops without JA (a) or supplemented with 128 μM JA (b). (PNG 2320 kb)

709_2018_1327_MOESM1_ESM.tif (8.7 mb)
High Resolution Image (TIF 8917 kb)
709_2018_1327_Fig10_ESM.png (1.3 mb)
Supplementary figure 2

Expression of early JA-response JAZ1 gene shows JA signal translocation from shoot to stem. Representative confocal images of epidermal cells of stems 24 h after contact with 0.2X MS medium drops without JA (a and d) or supplemented with 64 μM (b and e) or 128 μM (c and f). (PNG 1324 kb)

709_2018_1327_MOESM2_ESM.tif (5.2 mb)
High Resolution Image (TIF 5338 kb)
709_2018_1327_Fig11_ESM.png (1.9 mb)
Supplementary figure 3

TCS::GFP expression is systemically downregulated by cotyledon wounding. Cotyledons of 4 dag seedlings were wounded and the root apex was photographed with a confocal microscope. Representative image are shown from at least 15 seedlings analyzed. The experiment was repeated twice with similar results. (PNG 1948 kb)

709_2018_1327_MOESM3_ESM.tif (9.4 mb)
High Resolution Image (TIF 9641 kb)


  1. Castulo-Rubio DY, Alejandre-Ramírez NA, Orozco-Mosqueda MC, Santoyo G, Macías-Rodríguez LI, Valencia-Cantero E (2015) Volatile organic compounds produced by the rhizobacterium Arthrobacter agilis UMCV2 modulate Sorghum bicolor (strategy II plant) morphogenesis and SbFRO1 transcription in vitro. J Plant Growth Regul 34:611–623CrossRefGoogle Scholar
  2. Chung HS, Koo AJK, Gao X, Jayanty S, Thines B, Jones AD, Howe GA (2008) Regulation and function of Arabidopsis JASMONATE ZIM-DOMAIN genes in response to wounding and herbivory. Plant Physiol 146:952–964CrossRefGoogle Scholar
  3. D’Agostino IB, Deruère J, Kieber JJ (2000) Characterization of the Arabiodopsis response regulator gene family to cytokinin. Plant Physiol 124:1706–1717CrossRefGoogle Scholar
  4. Etesami H, Hosseini HM, Alikhani HA, Mohammadi L (2014) Bacterial biosynthesis of 1-aminocyclopropane-1-carboxylate (ACC) deaminase and indole-3-acetic acid (IAA) as endophytic preferential selection traits by rice plant seedlings. J Plant Growth Regul 33:654–670CrossRefGoogle Scholar
  5. Fonouni-Farde C, Diet A, Frugier F (2016) Root development and endosymbiosis: DELLAs lead the orchestra. Trends Plant Sci 21:898–900CrossRefGoogle Scholar
  6. Henkes GJ, Thorpe MR, Minchin PEH, Schurr U, Röse USR (2008) Jasmonic acid treatment to part of the root system is consistent with simulated leaf herbivory, diverting recently assimilated carbon towards untreated roots within an hour. Plant Cell Environ 31:1229–1236CrossRefGoogle Scholar
  7. Hernández-León R, Rojas-Solís D, Contreras-Pérez M, Orozco-Mosqueda MC, Macías-Rodríguez LI, Reyes-de la Cruz H, Valencia-Cantero E, Santoyo G (2015) Characterization of the antifungal and plant growth-promoting effects of diffusible and volatile organic compounds produced by Pseudomonas fluorescens strains. Biol Control 81:83–92CrossRefGoogle Scholar
  8. Ishimaru Y, Oikawa T, Suzuki T, Takeishi S, Matsuura H, Takahashi K, Hamamoto S, Uozumi N, Shimizu T, Seo M, Ohta H, Ueda M (2017) GTR1 is a jasmonic acid and jasmonoyl-I-isoleucine transporter in Arabidopsis thaliana. Biosci Biotechnol Biochem 81:249–255CrossRefGoogle Scholar
  9. Jensen AB, Raventos D, Mundy J (2002) Fusion genetic analysis of jasmonate signalling mutants in Arabidopsis. Plant J 29:595–606CrossRefGoogle Scholar
  10. Kim HJ, Chiang YH, Kieber JJ, Schaller GE (2013) SCFKMD controls cytokinin signaling by regulating the degradation of type-B response regulators. Proc Natl Acad Sci U S A 110:10028–10033CrossRefGoogle Scholar
  11. Koo AJK, Gao X, Jones AD, Howe GA (2009) A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. Plant J 59:974–986CrossRefGoogle Scholar
  12. Kudoyarova GR, Melentiev AI, Martynenko EV, Timergalina LN, Arkhipova TN, Shendel GV, Kuz'mina LY, Dodd IC, Veselov SY (2014) Cytokinin producing bacteria stimulate amino acid deposition by wheat roots. Plant Physiol Biochem 83:285–291CrossRefGoogle Scholar
  13. Li Q, Zheng J, Li S, Huang G, Skilling SJ, Wang LL, Li M, Yuan L, Liu P (2017) Transporter-mediated nuclear entry of jasmonoyl-isoluecine is essential for jasmonate signaling. Mol Plant 10:695–708CrossRefGoogle Scholar
  14. Liu W, Mu W, Zhu B, Liu F (2008) Antifungal activities and component of VOCs produced by Bacillus subtilis G8. Current Res Bacteriol 1:28–34CrossRefGoogle Scholar
  15. Liu L, Li H, Zeng H, Cai Q, Zhou X, Yin C (2015) Exogenous jasmonic acid and cytokinin antagonistically regulate rice flag leaf senescence by mediating chlorophyll degradation, membrane deterioration, and senescence-associated genes expression. J Plant Growth Regul 35:366–376CrossRefGoogle Scholar
  16. Moubayidin L, Di Mambro R, Sabatini S (2009) Cytokinin-auxin crosstalk. Trends Plant Sci 14:557–562CrossRefGoogle Scholar
  17. Müller B, Sheen J (2008) Cytokinin and auxin interplay in root stem-cell specification during early embryogenesis. Nature 453:1094–1097CrossRefGoogle Scholar
  18. Naik GR, Mukherjee I, Reid DM (2002) Influence of cytokinins on the methyl jasmonate-promoted senescence in Helianthus annus cotyledons. Plant Growth Regul 38:61–68CrossRefGoogle Scholar
  19. Orozco-Mosqueda MC, Macías-Rodríguez LI, Santoyo G, Farías-Rodríguez R, Valencia-Cantero E (2013) Medicago truncatula increases its iron-uptake mechanism in response to volatile organic compounds produced by Sinorhizobium meliloti. Folia Microbiol 58:579–585CrossRefGoogle Scholar
  20. 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 31:1497–1509CrossRefGoogle Scholar
  21. Ortiz-Castro R, Díaz-Pérez C, Martínez-Trujillo M, del Río-Torres RE, Campos-García J, López-Bucio J (2011) Transkingdom signaling based on bacterial cyclopeptides with auxin activity in plants. Proc Natl Acad Sci U S A 108:7253–7258CrossRefGoogle Scholar
  22. Raya-González J, Velázquez-Becerra C, Barrera-Ortiz S, López-Bucio J, Valencia-Cantero E (2017) N,N-dimethyl hexadecylamine and related amines regulate root morphogenesis via jasmonic acid in Arabidopsis thaliana. Protoplasma 254:1399–1410CrossRefGoogle Scholar
  23. Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Paré PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci U S A 100:4927–4932CrossRefGoogle Scholar
  24. Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026CrossRefGoogle Scholar
  25. Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in Arabidopsis root. Cell 99:463–472CrossRefGoogle Scholar
  26. Sato C, Seto Y, Nabeta K, Matsuura H (2009) Kinetics of the accumulation of jasmonic acid and its derivatives in systemic leaves of tabacco (Nicotiana tabacum cv. Xanthi nc) and translocation of deuterium-labeled jasmonic acid from wounding site to the systemic site. Biosci Biotechnol Biochem 73:1962–1970CrossRefGoogle Scholar
  27. Stoynova-Bakalova E, Petrov PI, Gigova L, Baskin TI (2007) Differential effects of methyl jasmonate on growth and division of etiolated zucchini cotyledons. Plant Biol 10:476–484CrossRefGoogle Scholar
  28. Stratmann JW (2003) Long distance run in the wound response – jasmonic acid is pulling ahead. Trends Plant Sci 8:247–250CrossRefGoogle Scholar
  29. 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 448:661–665CrossRefGoogle Scholar
  30. Valencia-Cantero E, Flores-Cortez I, Ambriz-Parra J, López-Albarrán P, Velázquez-Becerra C (2015) Arthrobacter agilis UMCV2 accelerates growth of Pinus devoniana. Phyton Int J Exp Bot 84:64–69Google Scholar
  31. Velázquez-Becerra C, Macías-Rodríguez LI, López-Bucio J, Altamirano-Hernández J, Flores-Cortez I, Valencia-Cantero E (2011) A volatile organic compound analysis from Arthrobacter agilis identifies dimethylhexadecylamine, an amino-containing lipid modulating bacterial growth and Medicago sativa morphogenesis in vitro. Plant Soil 339:329–340CrossRefGoogle Scholar
  32. Velázquez-Becerra C, Macías-Rodríguez LI, López-Bucio J, Flores-Cortez I, Santoyo G, Hernández-Soberano C, Valencia-Cantero E (2013) The rhizobacterium Arthrobacter agilis produces dimethylhexadecylamine, a compound that inhibits growth of phytopathogenic fungi in vitro. Protoplasma 250:1251–1262CrossRefGoogle Scholar
  33. Zhang ZP, Baldwin IT (1997) Transport of [2-14C]jasmonic acid from leaves to roots mimics wound-induced changes in endogenous jasmonic acid pools in mi Nicotiana sylvestris. Planta 203:436–441CrossRefGoogle Scholar
  34. Zhang Y, Turner JG (2008) Wound-induced endogenous jasmonates stunt plant growth by inhibiting of mitosis. PLoS One 3:e3699CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Instituto de Investigaciones Químico-BiológicasUniversidad Michoacana de San Nicolás de HidalgoMoreliaMéxico

Personalised recommendations