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

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Abstract

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.

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References

  • 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 34:611–623

    Article  CAS  Google Scholar 

  • 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 146:952–964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • D’Agostino IB, Deruère J, Kieber JJ (2000) Characterization of the Arabiodopsis response regulator gene family to cytokinin. Plant Physiol 124:1706–1717

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 33:654–670

    Article  CAS  Google Scholar 

  • Fonouni-Farde C, Diet A, Frugier F (2016) Root development and endosymbiosis: DELLAs lead the orchestra. Trends Plant Sci 21:898–900

    Article  CAS  PubMed  Google Scholar 

  • 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 31:1229–1236

    Article  CAS  PubMed  Google Scholar 

  • 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 81:83–92

    Article  CAS  Google Scholar 

  • 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 81:249–255

    Article  CAS  PubMed  Google Scholar 

  • Jensen AB, Raventos D, Mundy J (2002) Fusion genetic analysis of jasmonate signalling mutants in Arabidopsis. Plant J 29:595–606

    Article  CAS  PubMed  Google Scholar 

  • 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 110:10028–10033

    Article  PubMed  PubMed Central  Google Scholar 

  • Koo AJK, Gao X, Jones AD, Howe GA (2009) A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. Plant J 59:974–986

    Article  CAS  PubMed  Google Scholar 

  • 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 83:285–291

    Article  CAS  PubMed  Google Scholar 

  • 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 10:695–708

    Article  CAS  PubMed  Google Scholar 

  • Liu W, Mu W, Zhu B, Liu F (2008) Antifungal activities and component of VOCs produced by Bacillus subtilis G8. Current Res Bacteriol 1:28–34

    Article  CAS  Google Scholar 

  • 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 35:366–376

    Article  CAS  Google Scholar 

  • Moubayidin L, Di Mambro R, Sabatini S (2009) Cytokinin-auxin crosstalk. Trends Plant Sci 14:557–562

    Article  CAS  PubMed  Google Scholar 

  • Müller B, Sheen J (2008) Cytokinin and auxin interplay in root stem-cell specification during early embryogenesis. Nature 453:1094–1097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naik GR, Mukherjee I, Reid DM (2002) Influence of cytokinins on the methyl jasmonate-promoted senescence in Helianthus annus cotyledons. Plant Growth Regul 38:61–68

    Article  CAS  Google Scholar 

  • 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 58:579–585

    Article  CAS  Google Scholar 

  • 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 31:1497–1509

    Article  CAS  PubMed  Google Scholar 

  • 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 108:7253–7258

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 254:1399–1410

    Article  CAS  PubMed  Google Scholar 

  • 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 100:4927–4932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 99:463–472

    Article  CAS  PubMed  Google Scholar 

  • 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 73:1962–1970

    Article  CAS  PubMed  Google Scholar 

  • 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 10:476–484

    Article  CAS  Google Scholar 

  • Stratmann JW (2003) Long distance run in the wound response – jasmonic acid is pulling ahead. Trends Plant Sci 8:247–250

    Article  CAS  PubMed  Google Scholar 

  • 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 448:661–665

    Article  CAS  PubMed  Google Scholar 

  • 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 84:64–69

    Google Scholar 

  • 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 339:329–340

    Article  CAS  Google Scholar 

  • 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 250:1251–1262

    Article  CAS  PubMed  Google Scholar 

  • 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 203:436–441

    Article  CAS  Google Scholar 

  • Zhang Y, Turner JG (2008) Wound-induced endogenous jasmonates stunt plant growth by inhibiting of mitosis. PLoS One 3:e3699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

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

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Authors and Affiliations

  1. Instituto de Investigaciones Químico-Biológicas, Universidad Michoacana de San Nicolás de Hidalgo, Edificio A1’, Ciudad Universitaria, C. P, 58030, Morelia, Michoacán, México

    Ernesto Vázquez-Chimalhua, León Francisco Ruíz-Herrera, Salvador Barrera-Ortiz, Eduardo Valencia-Cantero & José López-Bucio

Authors
  1. Ernesto Vázquez-Chimalhua
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  2. León Francisco Ruíz-Herrera
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  3. Salvador Barrera-Ortiz
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  4. Eduardo Valencia-Cantero
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  5. José López-Bucio
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Corresponding authors

Correspondence to Eduardo Valencia-Cantero or José López-Bucio.

Additional information

Handling Editor: Peter Nick

Electronic supplementary material

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)

High Resolution Image (TIF 8917 kb)

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)

High Resolution Image (TIF 5338 kb)

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)

High Resolution Image (TIF 9641 kb)

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Vázquez-Chimalhua, E., Ruíz-Herrera, L.F., Barrera-Ortiz, S. et al. The bacterial volatile dimethyl-hexa-decylamine reveals an antagonistic interaction between jasmonic acid and cytokinin in controlling primary root growth of Arabidopsis seedlings. Protoplasma 256, 643–654 (2019). https://doi.org/10.1007/s00709-018-1327-9

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  • DOI: https://doi.org/10.1007/s00709-018-1327-9

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