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Elevated α-Linolenic Acid Content in Extra-plastidial Membranes of Tomato Accelerates Wound-Induced Jasmonate Generation and Improves Tolerance to the Herbivorous Insects Heliothis peltigera and Spodoptera littoralis

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Abstract

In tomato, desaturation of linoleic acid (18:2) to α-linolenic acid (18:3) is mediated in the plastidial membranes by the ω-3 fatty acid desaturases 7 (FAD7), and in the ER membrane by its paralog FAD3. According to the prevalent model, the hormone jasmonic acid isoleucine (JA-Ile), which plays a key role in the plant response to various stresses, including wounding and herbivores attack, is derived from 18:3 which is released from the plastidial membrane glycerolipids. The current work aimed at assessing in tomato the effects of ectopic FAD3 over-expression or SlFAD7 silencing on herbivore tolerance and on wound response. The tomato SlFAD7 gene encoding for the plastidial-residing FAD7 was silenced by RNA interference, and enhanced expression of the extra-plastidial ER-residing FAD3 was induced by ectopic expression of BnFAD3. Over-expression of BnFAD3 led to increase, whereas SlFAD7 silencing led to decrease in 18:3 content in the extra-plastidial and plastidial membrane, respectively. As anticipated, silencing SlFAD7 attenuated the accumulation of JA-Ile following wounding, and enhanced susceptibility to two important pest insects: the chewing herbivores Spodoptera littoralis and Heliothis peltigera. Unexpected was the finding that ectopic over-expression of the extra-plastidial ER-residing FAD3 accelerated both wound-induced JA-Ile accumulation and expression of wound-response marker genes. Furthermore, BnFAD3 over-expression significantly improved the tomato tolerance to these two chewing herbivores. The presented information supports the notion that 18:3 derived from extra-plastidial membranes may serve as a substrate for, or as a source for a cue triggering, JA-Ile biosynthesis in response to wounding and insect chewing.

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Acknowledgements

We thank Dr. Yehiam Salts, ARO, Israel, for assistance in primers design, and Prof. Yuval Eshed, Weizmann Institute of Science, Rehovot, Israel, for the pRNA69 and pART27 plasmids. The technical assistance of Sabine Freitag, (Georg-August-University, Göttingen, Germany), Chen Klap, and Sara Shabtai (ARO, Israel) is greatly appreciated.

Funding

This work was supported by the United States-Israel Binational Agricultural Research and Development BARD fund (Grant No. TB-8050-08), and by the Chief Scientist Fund, Ministry of Agriculture, Israel (Grant No. 204-442-01).

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  1. Meng Zhang

    Present address: College of Agronomy, Northwest A&F University, Yangling, 712100, Shaanxi, China

  2. Meng Zhang and Yonatan Demeshko contributed equally to this work.

Authors and Affiliations

  1. The Institute of Plant Sciences, The Volcani Center, Agricultural Research Organization, HaMaccabim Road 68, P.O.B 15159, 7528809, Rishon LeZion, Israel

    Meng Zhang, Yonatan Demeshko, Rita Dumbur, Rivka Barg & Gozal Ben-Hayyim

  2. Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences, Georg-August-University, Justus-von-Liebig-Weg 11, 37077, Göttingen, Germany

    Tim Iven & Ivo Feussner

  3. Department of Plant Biochemistry, Goettingen Center for Molecular Biosciences (GZMB), Georg-August-University, Justus-von-Liebig-Weg 11, 37077, Göttingen, Germany

    Ivo Feussner

  4. Institute of Plant Protection, The Volcani Center, Agricultural Research Organization, HaMaccabim Road 68, P.O.B 15159, 7528809, Rishon LeZion, Israel

    Galina Lebedov & Murad Ganim

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Zhang, M., Demeshko, Y., Dumbur, R. et al. Elevated α-Linolenic Acid Content in Extra-plastidial Membranes of Tomato Accelerates Wound-Induced Jasmonate Generation and Improves Tolerance to the Herbivorous Insects Heliothis peltigera and Spodoptera littoralis. J Plant Growth Regul 38, 723–738 (2019). https://doi.org/10.1007/s00344-018-9885-9

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