Plant Diversity ›› 2020, Vol. 42 ›› Issue (02): 111-119.DOI: 10.1016/j.pld.2019.11.005

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Silencing JA hydroxylases in Nicotiana attenuata enhances jasmonic acid-isoleucine-mediated defenses against Spodoptera litura

Jinxiang Tanga,c, Dahai Yangb, Jianqiang Wua, Suiyun Chenc, Lei Wanga   

  1. a Department of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China;
    b Tobacco Breeding and Biotechnology Research Center, Yunnan Academy of Tobacco Agricultural Sciences, Key Laboratory of Tobacco Biotechnological Breeding, National Tobacco Genetic Engineering Research Center, Kunming, 650021, China;
    c School of Life Science, Yunnan University, Kunming, 650091, China
  • Received:2019-08-02 Revised:2019-10-23 Online:2020-04-25 Published:2020-04-30
  • Supported by:
    This work was supported by the Key Project of Applied Basic Research Program of Yunnan (2017FA015), the Young Academic and Technical Leader Raising Foundation of Yunnan Province (no. 2017HB063), and the Yunnan Academy of Tobacco Agricultural Sciences (2018530000241002 and 2019530000241003). We also thank the Biotechnology Experimental Center at the Kunming Institute of Botany, CAS, for supporting plant cultivation.

Abstract: Jasmonic acid (JA) plays important roles in plant resistance to insect herbivores. One important derivative of JA is 12-OH-JA, which is produced by two independent pathways: direct hydroxylation of JA by jasmonate-induced oxygenases (JOXs) or hydrolyzation of 12-OH-JA-Ile.Yet the function of 12-OH-JA in planteherbivore interactions remains largely unknown. In this study, we silenced four JOX homologs independently in the wild tobacco Nicotiana attenuata by virus-induced gene silencing (VIGS), and found that all four JOX homologs are involved in JA hydroxylation. Simultaneously silencing the four JA hydroxylases in VIGS-NaJOXs plants decreased herbivory-induced 12-OH-JA by 33%, but JA and JA-Ile levels increased by 45% and 30%, respectively, compared to those in control plants. Compared to direct hydroxylation from JA, hydrolyzation from 12-OH-JA-Ile is equally important for herbivory-induced 12-OHJA accumulation: in the 12-OH-JA-Ile deficient irJAR4/6 plants, 12-OH-JA decreased 34%. Moreover, VIGSNaJOXs plants exhibited enhanced resistance to the generalist herbivore Spodoptera litura. The poor larval performance was strongly correlated with high levels of several JA-Ile-dependent direct defense metabolites in the VIGS-NaJOXs plants. When we simultaneously silenced all four JA hydroxylases in the JAIle-deficient irJAR4/6 background, the enhanced herbivore resistance diminished, demonstrating that enhanced herbivore resistance resulted from elevated JA-Ile levels. Given that silencing these NaJOX-like genes did not detectably alter plant growth but highly increased plant defense levels, we propose that JOX genes are potential targets for genetic improvement of herbivore-resistant crops.

Key words: JA metabolism, 12-OH-JA, Spodoptera litura, 2-Oxoglutarate oxygenase, Herbivore defense, Nicotiana attenuata