Trade-offs between the accumulation of cuticular wax and jasmonic acid-mediated herbivory resistance in maize

doi:10.1111/jipb.13586

J Integr Plant Biol. ›› 2024, Vol. 66 ›› Issue (1): 143-159.DOI: 10.1111/jipb.13586

• Plant Biotic Interactions • Previous Articles

Trade-offs between the accumulation of cuticular wax and jasmonic acid-mediated herbivory resistance in maize

Jiong Liu^1,2†, Lu Li^1,3†, Zhilong Xiong^1,3,4†, Christelle A.M. Robert⁵, Baozhu Li^1,2,4, Shan He^1,3, Wenjie Chen^1,3, Jiasheng Bi^1,3, Guanqing Zhai^1,3,4, Siyi Guo^1,2,4, Hui Zhang^1,2, Jieping Li^1,2, Shutang Zhou^1,3,4*, Xi Zhang^1,3,4* and Chun‐Peng Song^1,2,4*

1. School of Life Sciences, Henan University, Kaifeng 475004, China;
2. State Key Laboratory of Crop Stress Adaptation and Improvement, Henan University, Kaifeng 475004, China;
3. State Key Laboratory of Cotton Bio‐Breeding and Integrated Utilization, Henan University, Kaifeng 475004, China;
4. Sanya Institute of Henan University, Sanya 572025, China;
5. Institute of Plant Sciences, University of Bern, Bern 3013, Switzerland
^†These authors contributed equally to this work.
^*Correspondence: Xi Zhang (xizhang@henu.edu.cn); Shutang Zhou (szhou@henu.edu.cn); Chun‐Peng Song (songcp@henu.edu.cn, Dr. Song is fully responsible for distributions of all materials associated with this article)

Received:2023-07-19 Accepted:2023-11-14 Online:2023-11-17 Published:2024-01-01

Abstract

Abstract: Plants have evolved complex physical and chemical defense systems that allow them to withstand herbivory infestation. Composed of a complex mixture of very-long-chain fatty acids (VLCFAs) and their derivatives, cuticular wax constitutes the first physical line of defense against herbivores. Here, we report the function of Glossy 8 (ZmGL8), which encodes a 3-ketoacyl reductase belonging to the fatty acid elongase complex, in orchestrating wax production and jasmonic acid (JA)-mediated defenses against herbivores in maize (Zea mays). The mutation of GL8 enhanced chemical defenses by activating the JA-dependent pathway. We observed a trade-off between wax accumulation and JA levels across maize glossy mutants and 24 globally collected maize inbred lines. In addition, we demonstrated that mutants defective in cuticular wax biosynthesis in Arabidopsis thaliana and maize exhibit enhanced chemical defenses. Comprehensive transcriptomic and lipidomic analyses indicated that the gl8 mutant confers chemical resistance to herbivores by remodeling VLCFA-related lipid metabolism and subsequent JA biosynthesis and signaling. These results suggest that VLCFA-related lipid metabolism has a critical role in regulating the trade-offs between cuticular wax and JA-mediated chemical defenses.

Key words: cuticular wax, fall armyworm, herbivore resistance, jasmonic acid, maize, plant–herbivore interactions

Jiong Liu, Lu Li, Zhilong Xiong, Christelle A.M. Robert, Baozhu Li, Shan He, Wenjie Chen, Jiasheng Bi, Guanqing Zhai, Siyi Guo, Hui Zhang, Jieping Li, Shutang Zhou, Xi Zhang and Chun‐Peng Song. Trade-offs between the accumulation of cuticular wax and jasmonic acid-mediated herbivory resistance in maize[J]. J Integr Plant Biol., 2024, 66(1): 143-159.

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Trade-offs between the accumulation of cuticular wax and jasmonic acid-mediated herbivory resistance in maize

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