Journal of Plant Growth Regulation

, Volume 36, Issue 4, pp 846–854 | Cite as

Insect Herbivory of Leaves Affects the Auxin Flux Along Root Apices in Arabidopsis thaliana

Article

Abstract

Plants reduce their growth rate when confronted by insect attack, and in turn resources are redirected from growth to enhance resistance against herbivory. In this study, one possible signaling cascade was investigated for establishing the underlying mechanism for the slow growth rate that has been observed following insect herbivory. Our results showed that free jasmonate (JA) and auxin levels were elevated in both leaves and roots after Plutella xylostella L. attack which was accompanied by the transcriptional increase of the auxin biosynthetic YUCCA3 and YUCCA8 genes. Further examination of endogenous auxin flux using physiological micro-sensor profiling showed that near the surface of the root transition zone, the net auxin flux decreased after insect attack. Conversely, insect herbivory caused an increase in the net H+ flux along the root surface with the most pronounced response occurring in the transition zone. Transcript levels of auxin transporter genes PIN1, PIN2, PIN3, PIN7, and AUX1 were also reduced after insect attack. Together, the auxin and H+ flux results indicate that the reduced growth after insect attack was likely associated with a decrease of auxin flux and proton secretion along the root tip.

Keywords

Insect herbivory Jasmonic acid Auxin flux Root growth Arabidopsis thaliana 

Notes

Acknowledgements

We would like to thank Yue Xu from Xuyue (Beijing) Science and Technology Company for their technical support. This work was financially supported by the National Natural Science Foundation of China (31270655) and the National ‘863’ Plan Project (No. 2011AA10020102).

Authors’ Contributions

Yingbai Shen and Suli Yan designed the project. Suli Yan and Chunyang Jiao performed the auxin flux measurement. Ningning Wang and Hongjun Yao performed the H+ flux measurement. Suli Yan and Chunyang Jiao analyzed the data and wrote the manuscript. Eric S. McLamore assisted with data analysis, NMT experiments, and manuscript preparation.

Supplementary material

344_2017_9688_MOESM1_ESM.docx (26 kb)
Supplementary material 1 (DOCX 25 KB)

References

  1. Baluška F, Volkmann D, Barlow PW (2001) A polarity crossroad in the transition growth zone of maize root apices: cytoskeletal and developmental implications. J Plant Growth Regul 20:170–181CrossRefGoogle Scholar
  2. Baluška F, Mancuso S, Volkmann D, Barlow P (2004) Root apices as plant command centres: the ‘brain-like’ status of the root apex transition zone. Biologia 59:1–13Google Scholar
  3. Baluška F, Mancuso S, Volkmann D, Barlow PW (2010) Root apex transition zone: a signalling-response nexus in the root. Trends Plant Sci 15:402–408CrossRefPubMedGoogle Scholar
  4. Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602CrossRefPubMedGoogle Scholar
  5. Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44CrossRefPubMedGoogle Scholar
  6. Bosch M, Berger S, Schaller A, Stintzi A (2014) Jasmonate-dependent induction of polyphenol oxidase activity in tomato foliage is important for defense against Spodoptera exigua but not against Manduca sexta. BMC Plant Biol 14:257–272CrossRefPubMedPubMedCentralGoogle Scholar
  7. Chen CW, Yang YW, Lur HS, Tsai YG, Chang MC (2005) A novel function of abscisic acid in the regulation of rice (Oryza. Sativa L.) root growth and development. Plant Cell Physiol 47(1):1–13CrossRefPubMedGoogle Scholar
  8. Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant anti herbivore defense. Science 23:895–900CrossRefGoogle Scholar
  9. Duffey SS, Stout MJ (1996) Antinutritive and toxic components of plant defense against insects. Arch insect biochem 32:3–37CrossRefGoogle Scholar
  10. Farmer EE, Ryan CA (1990) Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci 87:7713–7716CrossRefPubMedPubMedCentralGoogle Scholar
  11. Friml J (2003) Auxin transport-shaping the plant. Curr opin plant biol 6:7–12CrossRefPubMedGoogle Scholar
  12. Fürstenberg-Hägg J, Zagrobelny M, Bak S (2013) Plant defense against insect herbivores. Int J Mol Sci 14:10242–10297CrossRefPubMedPubMedCentralGoogle Scholar
  13. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227CrossRefPubMedGoogle Scholar
  14. Grieneisen VA, Xu J, Marée AF, Hogeweg P, Scheres B (2007) Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449:1008–1013CrossRefPubMedGoogle Scholar
  15. Haruta M, Sussman MR (2012) The effect of a genetically reduced plasma membrane protonmotive force on vegetative growth of Arabidopsis. Plant physiol 158:1158–1171CrossRefPubMedPubMedCentralGoogle Scholar
  16. 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 74:626–637CrossRefPubMedPubMedCentralGoogle Scholar
  17. 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 99:6416–6421CrossRefPubMedPubMedCentralGoogle Scholar
  18. McLamore ES, Porterfield DM (2011) Non-invasive tools for measuring metabolism and biophysical analyte transport: self-referencing physiological sensing. Chem Soc Rev 40:5308–5320CrossRefPubMedGoogle Scholar
  19. McLamore ES, Diggs A, Calvo Marzal P, Shi J, Blakeslee JJ, Peer WA, Murphy AS, Porterfield DM (2010) Non-invasive quantification of endogenous root auxin transport using an integrated flux microsensor technique. Plant J 63:1004–1016CrossRefPubMedGoogle Scholar
  20. Morisawa M, Steinhardt RA (1982) Changes in intracellular pH of Physarum plasmodium during the cell cycle and in response to starvation. Exp Cell Res 140:341–351CrossRefPubMedGoogle Scholar
  21. Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439CrossRefPubMedGoogle Scholar
  22. Pan X, Welti R, Wang X (2010) Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nature Protoc 5:986–992CrossRefGoogle Scholar
  23. Pitts RJ, Cernac A, Estelle M (1998) Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J 16:553–560CrossRefPubMedGoogle Scholar
  24. Porterfield DM, McLamore ES, Banks MK (2009) Microsensor technology for measuring H+ flux in buffered media. Sensor Actuat B 136:383–387CrossRefGoogle Scholar
  25. Qi L, Yan J, Li Y, Jiang H, Sun J, Chen Q, Li H, Chu J, Yan C, Sun X, Yu Y, Li C, Li C (2012) Arabidopsis thaliana plants differentially modulate auxin biosynthesis and transport during defense responses to the necrotrophic pathogen Alternaria brassicicola. New Phytol 195:872–882CrossRefPubMedGoogle Scholar
  26. Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62(10):3321–3338CrossRefPubMedGoogle Scholar
  27. Rober-Kleber N, Albrechtová JT, 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 131:1302–1312CrossRefPubMedPubMedCentralGoogle Scholar
  28. Schmidt L, Hummel GM, Thiele B, Schurr U, Thorpe MR (2015) Leaf wounding or simulated herbivory in young N. attenuata plants reduces carbon delivery to roots and root tips. Planta 241:917–928CrossRefPubMedGoogle Scholar
  29. Shabala S, Newman I, Whittington J, Juswono U (1998) Protoplast ion fluxes: their measurement and variation with time, position and osmoticum. Planta 204:146–152CrossRefGoogle Scholar
  30. Shabala S, Shabala L, Gradmann D, Chen Z, Newman I, Mancuso S (2006) Oscillations in plant membrane transport: model predictions, experimental validation, and physiological implications. J Exp Bot 57:171–184CrossRefPubMedGoogle Scholar
  31. Staal M, De Cnodder T, Simon D, Vandenbussche F, Van der Straeten D, Verbelen JP, Elzenga T, Vissenberg K (2011) Apoplastic alkalinization is instrumental for the inhibition of cell elongation in the Arabidopsis root by the ethylene precursor 1-aminocyclopropane – 1-carboxylic acid. Plant Physiol 155:2049–2055CrossRefPubMedPubMedCentralGoogle Scholar
  32. Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Dolezal K, Schlereth A, Jürgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191CrossRefPubMedGoogle Scholar
  33. 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 21:1495–1511CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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 191:360–375CrossRefPubMedGoogle Scholar
  35. Sussman MR, Goldsmith MH (1981) The action of specific inhibitors of auxin transport on uptake of auxin and binding of N-1-naphthylphthalamic acid to a membrane site in maize coleoptiles. Planta 152:13–18CrossRefPubMedGoogle Scholar
  36. Taiz L, Zeiger E (2006) Plant Physiology, 4th Revised edn. Sinauer Associates, USAGoogle Scholar
  37. Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859CrossRefPubMedGoogle Scholar
  38. Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14:S153–S164PubMedPubMedCentralGoogle Scholar
  39. Wang D, Pajerowska-Mukhtar K, Culler AH, Dong X (2007) Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr Biol 17:1784–1790CrossRefPubMedGoogle Scholar
  40. Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697CrossRefPubMedPubMedCentralGoogle Scholar
  41. Xu Y, Sun T, Yin L (2006) Application of non-invasive microsensing system to simultaneously measure both H+ and O2 fluxes around the pollen tube. J Integr Plant Biol 48:823–831CrossRefGoogle Scholar
  42. Xu W, Jia L, Shi W, Liang J, Zhou F, Li Q, Zhang J (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 197:139–150CrossRefPubMedGoogle Scholar
  43. Xue R, Zhang B (2007) Increased endogenous methyl jasmonate altered leaf and root development in transgenic soybean plants. J Genet and Genomics 34:339–346CrossRefGoogle Scholar
  44. Yan S, Luo S, Dong S, Zhang T, Sun J, Wang N, Yao H, Shen YB (2015a) Heterotrimeric G-proteins involved in the MeJA regulated ion flux and stomatal closure in Arabidopsis thaliana. Funct Plant Biol 42:126–135CrossRefGoogle Scholar
  45. Yan S, McLamore ES, Dong S, Gao H, Taguchi M, Wang N, Zhang T, Su X, Shen Y (2015b) The role of plasma membrane H+ -ATPase in jasmonate-induced ion fluxes and stomatal closure in Arabidopsis thaliana. Plant J 83:638–649CrossRefPubMedGoogle Scholar
  46. Yan S, Zhang T, Dong S, McLamore Eric, Wang N, Shan X, Shen Y, Wan Y (2016) MeJA affects root growth by modulation of transmembrane auxin flux in the transition zone. J Plant Growth Regul 35:256–265CrossRefGoogle Scholar
  47. Yang Y, Hammes UZ, Taylor CG, Schachtman DP, Nielsen E (2006) High-affinity auxin transport by the AUX1 influx carrier protein. Curr Biol 16:1123–1127CrossRefPubMedGoogle Scholar
  48. Yang ZB, Geng X, He C, Zhang F, Wang R, Horst WJ, Ding Z (2014) TAA1-regulated local auxin biosynthesis in the root-apex transition zone mediates the aluminum-induced inhibition of root growth in Arabidopsis. Plant Cell 26:2889–2904CrossRefPubMedPubMedCentralGoogle Scholar
  49. Zebelo S, Piorkowski J, Disi J, Fadamiro H (2014) Secretions from the ventral eversible gland of Spodoptera exigua caterpillars activate defense-related genes and induce emission of volatile organic compounds in tomato, Solanum lycopersicum. BMC Plant Biol 14:140–151CrossRefPubMedPubMedCentralGoogle Scholar
  50. Zhang Y, Turner JG (2008) Wound-induced endogenous jasmonates stunt plant growth by inhibiting mitosis. PLoS ONE 3:e3699CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.College of Biological Sciences and TechnologyBeijing Forestry UniversityBeijingChina
  2. 2.National Engineering Laboratory for Tree BreedingBeijing Forestry UniversityBeijingChina
  3. 3.Agricultural and Biological Engineering Department, Institute of Food and Agricultural SciencesUniversity of FloridaGainesvilleUSA

Personalised recommendations