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Mycorrhiza

, Volume 27, Issue 6, pp 525–535 | Cite as

Indirect interactions between arbuscular mycorrhizal fungi and Spodoptera exigua alter photosynthesis and plant endogenous hormones

  • Lei He
  • Changyou Li
  • Runjin LiuEmail author
Original Article

Abstract

Peanut (Arachis hypogaea Linn. cv: Luhua 11) and tomato (Lycopersicon esculentum Mill. cv: Zhongshu 4) were inoculated with arbuscular mycorrhizal fungi (AMF) Funneliformis mosseae BEG167 (Fm), Rhizophagus intraradices BEG141 (Ri), and Glomus versiforme Berch (Gv), and/or Spodoptera exigua (S. exigua) under greenhouse conditions. Results indicated that feeding by S. exigua had little influence on colonization of peanut plants by AMF, but improved colonization of tomato by Fm and Gv. Feeding by S. exigua had little influence on leaf net photosynthetic rate, transpiration rate, and stomatal conductance of nonmycorrhizal peanut plants but significantly improved net photosynthetic rate and transpiration rate of mycorrhizal plants of both hosts. AMF with or without S. exigua inoculation improved host plant photosynthetic characteristics, growth, and hormone status. Fm showed maximum beneficial effects, followed by Gv. The concentrations and ratios of phytohormones abscisic acid (ABA), indole-3-acetic acid (IAA), gibberellin (GA), zeatin riboside (ZR), and jasmonic acid (JA) in the leaves of the host plants were changed due to the interaction between AMF and S. exigua. Generally, AMF with or without S. exigua inoculation increased the concentrations of GA, ZR, and JA and the ratios of IAA/ABA, GA/ABA, ZR/ABA, and IAA + GA + ZR/ABA, while feeding by S. exigua on nonmycorrhizal plants showed the opposite effect. The concentration of JA in the leaves of peanut and tomato inoculated with Fm or Fm + S. exigua was 1.9 and 1.9 times and 2.5 and 2.7 times, respectively, greater than that of the controls inoculated with neither. There was a negative correlation between the JA concentration and the survival percentage of S. exigua larva. We conclude that indirect interactions between AMF and insect herbivores changed the photosynthetic and hormone characteristics, and ratios of phytohormones, thereby revealing mechanisms of belowground-aboveground interactions.

Keywords

AMF Spodoptera exigua Peanut Tomato Hormone Photosynthesis 

Notes

Acknowledgements

This study was financially supported by the National Natural Science Foundation of China (31272210 and 31470101) and the Key Research Program of Shandong Government (2016GNC110021).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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References

  1. Ansari A, Razmjoo J, Karimmojeni H (2016) Mycorrhizal colonization and seed treatment with salicylic acid to improve physiological traits and tolerance of flaxseed (Linum usitatissimum L.) plants grown under drought stress. Acta Physiol Plant 38:34 . doi: 10.1007/s11738-015-2054-x Published online: 11 January 2016CrossRefGoogle Scholar
  2. Barber NA (2013) Arbuscular mycorrhizal fungi are necessary for the induced response to herbivores by Cucumis sativus. J Plant Ecol 6(2):171–176CrossRefGoogle Scholar
  3. Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69(4):473–488CrossRefPubMedGoogle Scholar
  4. Bennett AE, Bever JD, Bowers MD (2009) Arbuscular mycorrhizal fungal species suppress inducible plant responses and alter defensive strategies following herbivory. Oecologia 160(1):771–779. doi: 10.1007/s00442-009-1338-5 CrossRefPubMedGoogle Scholar
  5. Biermann B, Linderman RG (1981) Quantifying vercular-arbuscular mycorrhizas: a proposed method towards standardization. New Phytol 87:63–67CrossRefGoogle Scholar
  6. Ding XH, Cao YL, Huang LL, Zhao J, Xu CG, Li XH, Wang SP (2008) Activation of the indole-3-acetic acid-amido synthetase GH3-8 suppresses expansin expression and promotes salicylate- and jasmonate-independent basal immunity in rice. Plant Cell 20(1):228–240CrossRefPubMedPubMedCentralGoogle Scholar
  7. Durán Prieto J, Castañé C, Calvet C, Camprubi A, Battaglia D, Trotta V, Fanti P (2016) Tomato belowground–aboveground interactions: Rhizophagus irregularis affects foraging behavior and life history traits of the predator Macrolophus pygmaeus (Hemiptera: Miridae). Arthropod Plant Interact . doi: 10.1007/s11829-016-9465-5 Published online: 13 October 2016Google Scholar
  8. Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends in Plant Sci 17(5):250–259CrossRefGoogle Scholar
  9. Gao L (2002) Control of arbuscular mycorrhizal colonisation: studies of a mycorrhiza-defective tomato mutant. PhD thesis. University of Adelaide, South Australia, AustraliaGoogle Scholar
  10. Gao CM, Wang MY, Mi Y, Wan FH, Liu RJ (2014) Interactions between arbuscular mycorrhizal fungi and herbivorous insects. Acta Ecol Sin 13:3481–3489 (in Chinese)Google Scholar
  11. Gao CM, Li M, Liu RJ (2016) Combination effects of arbuscular mycorrhizal fungi and dark septate endophytes on promoting growth of cucumber plants and resistance to nematode disease. Mycosystema 35(10):1208–1217 (in Chinese)Google Scholar
  12. Giron D, Frago E, Glevarec G, Pieterse CMJ, Dicke M (2013) Plant-microbe-insect interactions: cytokinins as key regulators in plant–microbe–insect interactions: connecting plant growth and defence. Funct Ecol 27:599–609CrossRefGoogle Scholar
  13. Hoffmann D, Vierheilig H, Peneder S, Schausberger P (2011) Mycorrhiza modulates aboveground tri-trophic interactions to the fitness benefit of its host plant. Ecol Entomol 36:574–581CrossRefGoogle Scholar
  14. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66CrossRefPubMedGoogle Scholar
  15. Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38(6):651–664CrossRefPubMedGoogle Scholar
  16. Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62(14):4731–4748CrossRefPubMedGoogle Scholar
  17. Leitner M, Kaiser R, Hause B, Boland W, Mithöfer A (2010) Does mycorrhization influence herbivore volatile emission in Medicago truncatula? Mycorrhiza 20:89–101CrossRefPubMedGoogle Scholar
  18. Li JX, Li H, Wang WH, Zhu XC, Liu RJ (2010) Effects of arbuscular mycorrhizal fungal arbuscule development on soybean cyst nematode diseases. J Qingdao Agri Univ (Natural Sci) 27(2):95–99 (in Chinese)Google Scholar
  19. Li LL, Shao TY, Yang H, Chen MX, Gao XM, Long XH, Shao HB, Liu ZP, Rengel Z (2016) The endogenous plant hormones and ratios regulate sugar and dry matter accumulation in Jerusalem artichoke in salt-soil. Sci Total Environ. doi: 10.1016/j.scitotenv.2016. 06. 075 Google Scholar
  20. Liu RJ, Chen YL (2007) Mycorrhizology. Science Press, Beijing, pp 381–387 (in Chinese)Google Scholar
  21. Liu RJ, Luo XS (1994) A new method to quantify the inoculum potential of arbuscular mycorrhizal fungi. New Phytol 128:89–92CrossRefGoogle Scholar
  22. Moraes MC, Birkett MA, Gordon-Weeks R, Smart LE, Martin JL, Pye BJ, Bromilow R, Pickett JA (2011) Cis-jasmone induces accumulation of defence compounds in wheat, Triticum aestivum. Phytochemistry 69(1):9–17CrossRefGoogle Scholar
  23. Nakashima K, Yamaguchi-Shinozaki K (2013) ABA signaling in stress-response and seed development. Plant Cell Rep 32(7):959–970CrossRefPubMedGoogle Scholar
  24. Naser HM, Hanan EH, Elsheery NI, Kalaji HM (2016) AMF show different effects on endogenous hormones in various plants. Trees 30:1149–1161. doi: 10.1007/s00468-016-1353-1 CrossRefGoogle Scholar
  25. Nishida T, Katayama N, Izumi N, Ohgushi T (2010) Arbuscular mycorrhizal fungi species-specifically affect induced plant responses to a spider mite. Population Ecol 52(4):507–515CrossRefGoogle Scholar
  26. Nogales A, Aguirreolea J, Santa Maria E, Camprubí A, Calvet C (2009) Response of mycorrhizal grapevine to Armillaria mellea inoculation: disease development and polyamines. Plant Soil 317:177–187CrossRefGoogle Scholar
  27. Onkokesung N, Gális I, von Dahl CC, Matsuoka K, Saluz HP, Baldwin IT (2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated herbivory in Nicotiana attenuata leaves. Physiol Plantarum 153(2):785–798CrossRefGoogle Scholar
  28. Pozo MJ, López-Ráez JA, Azcón-Aguilar C, García-Garrido JM (2015) Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytol 205:1431–1436CrossRefPubMedGoogle Scholar
  29. Schädler M, Ballhorn DJ (2016) Beneficial soil microbiota as mediators of the plant defensive phenotype and aboveground plant-herbivore interactions. Progress of Bot 78:305–343Google Scholar
  30. Selig P, Keough S, Nalam VJ, Nachappa P (2016) Jasmonate-dependent plant defenses mediate soybean thrips and soybean aphid performance on soybean. Arthropod Plant Interact 10:273–282CrossRefGoogle Scholar
  31. Shrivastava G, Ownley BH, Augé RM, Toler H, Dee M, Vu A, Köllner TG, Chen F (2015) Colonisation by arbuscular mycorrhizal and endophytic fungi enhanced terpene production in tomato plants and their defense against a herbivorous insect. Symbiosis 65:65–74CrossRefGoogle Scholar
  32. Song YY, Zeng RS, Xu JF, Li J, Shen X, Yihdego WG (2010) Interplant communication of tomato plants through underground common mycorrhizal network. PLoS One 5(10):e13324CrossRefPubMedPubMedCentralGoogle Scholar
  33. Spoel SH, Koornneef A, Claessens SM, Korzelius JP, van Pelt JA, Mueller MJ, Buchala AJM, Métraux JP, Brown R, Kazan K (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15(3):760–770CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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(5):1495–1511CrossRefPubMedPubMedCentralGoogle Scholar
  35. Tomczak VV, Schweiger R, Müller C (2016) Effects of arbuscular mycorrhiza on plant chemistry and the development and behavior of a generalist herbivore. J Chem Ecol 42:1247–1258CrossRefPubMedGoogle Scholar
  36. Tooker JF, De Moraes CM (2011) Feeding by a gall-inducing caterpillar species alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems. Arthropod Plant Interact 5:115–124CrossRefGoogle Scholar
  37. Wang Y, Li B, Du MW, Eneji AE, Wang BM, Duan LS, Li ZH, Tian XL (2012) Mechanism of phytohormone involvement in feedback regulation of cotton leaf senescence induced by potassium deficiency. J Exp Bot. doi: 10.1093/jxb/ers238 Journal of Experimental Botany Advance Access published September 7, 2012Google Scholar
  38. Wang M, Bezemer M, van der Putten WH, Biere A (2015) Effects of the timing of herbivory on plant defense induction and insect performance in ribwort plantain (Plantago lanceolata L.) depend on plant mycorrhizal status. J Chem Ecol 41:1006–1017CrossRefPubMedPubMedCentralGoogle Scholar
  39. Wright DP, Scholes JD, Read DJ (1998) Effects of VA mycorrhizal colonization on photosynthesis and biomass production of Trifolium repens L. Plant Cell Environ 21:209–216CrossRefGoogle Scholar
  40. Yang YM, Xu CN, Wang BM, Jia JZ (2001) Effects of plant growth regulators on secondary wall thickening of cotton fibres. Plant Growth Regul 35:233–237CrossRefGoogle Scholar
  41. Yang HX, Liu RJ, Guo SX (2014) Effects of arbuscular mycorrhizal fungus Glomus mosseae on the growth characteristics of Festu caarundinacea under salt stress conditions. Acta Pratacul Sin 4:195–203 (in Chinese)Google Scholar
  42. Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Res 97(1):111–119CrossRefGoogle Scholar
  43. Zhu XQ, Tang M, Zhang HQ (2016) Arbuscular mycorrhizal fungi enhanced the growth, photosynthesis, and calorific value of black locust under salt stress Photosynthetica. pp 1–8 First online 4 October 2016. doi: 10.1007/s11099-017-0662-y

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Institute of Mycorrhizal BiotechnologyQingdao Agricultural UniversityQingdaoChina
  2. 2.Center for Advanced Invertebrate Cell Culture and Cell Engineering, College of Agronomy and Plant ProtectionQingdao Agricultural UniversityQingdaoChina

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