Abscisic acid is essential for rewiring of jasmonic acid-dependent defenses during herbivory

Abstract

19Jasmonic acid (JA) is an important plant hormone in the regulation of defenses 20 against chewing herbivores and necrotrophic pathogens. In Arabidopsis thaliana, the 21 JA response pathway consists of two antagonistic branches that are regulated by 22 MYC-and ERF-type transcription factors, respectively. The role of abscisic acid 23 (ABA) and ethylene (ET) in the molecular regulation of the MYC/ERF antagonism 24 during plant-insect interactions is still unclear. Here, we show that production of ABA 25 induced in response to leaf-chewing Pieris rapae caterpillars is required for both the 26 activation of the MYC-branch and the suppression of the ERF-branch during 27 herbivory. Exogenous application of ABA suppressed ectopic ERF-mediated PDF1.2 28 expression in 35S::ORA59 plants. Moreover, the GCC-box promoter motif, which is 29 required for JA/ET-induced activation of the ERF-branch genes ORA59 and PDF1.2, 30 was targeted by ABA. Application of gaseous ET counteracted activation of the 31 MYC-branch and repression of the ERF-branch by P. rapae, but infection with the 32 ET-inducing necrotrophic pathogen Botrytis cinerea did not. Accordingly, P. rapae 33 performed equally well on B. cinerea-infected and control plants, whereas activation 34 of the MYC-branch resulted in reduced caterpillar performance. Together, these data 35 indicate that upon feeding by P. rapae, ABA is essential for activating the MYC-36 branch and suppressing the ERF-branch of the JA pathway, which maximizes 37 defense against caterpillars.38 65 proteins are degraded thereby releasing transcription factors that can activate JA-66 regulated genes.67 Within the JA pathway, two distinct, antagonistic branches of transcriptional 68 regulation are recognized; the MYC-branch and the ERF-branch. Feeding by 69 chewing herbivores activates the MYC-branch (Verhage et al., 2011; Vos et al., 70 2013b). This branch is controlled by the basic helix-loop-helix leucine zipper 71 transcription factors MYC2, MYC3 and MYC4 leading to transcription of hundreds of 72 4 JA-responsive MYC-branch regulated genes, including VSP1 and VSP2 (Anderson 73 et al. , 2004; Lorenzo et al., 2004; Fernández-Calvo et al., 2011; Niu et al., 2011). 74 Furthermore, previous studies have indicated that ABA plays a co-regulating role in 75 the activation of the MYC-branch (Anderson et al., 2004; Bodenhausen and 76 Reymond, 2007; Sánchez-Vallet et al., 2012; Vos et al., 2013b). For example, in the 77 ABA-deficient mutant aba2-1, expression of the JA-responsive gene VSP1 was 78 reduced upon feeding by caterpillars of Pieris rapae (small cabbage white) compared 79 to wild-type Col-0 plants (Vos et al., 2013b). In contrast to the herbivore-induced 80 MYC-branch, the ERF-branch is activated upon infection with necrotrophic 81 pathogens. The transcription factors EIN3 and EIL1 and the ERF transcription 82 factors ERF1 and ORA59 activate a large set of JA-responsive ERF-branch 83 regulated genes, including PDF1.2 (Caarls et al., 2015). The expression of ERF1, 84 ORA59 and PDF1.2 is im...

Insights Into the Mechanisms Implicated in Pinus pinaster Resistance to Pinewood Nematode

“…The role of ABA in plant immunity seems to be an ambivalent one (Ton et al, 2009 ). In some interactions, ABA can inhibit SA and JA/ET response (Lorenzo et al, 2004 ; Adie et al, 2007 ; Nahar et al, 2012 ; Hillwig et al, 2016 ), while in others it enhances JA response against fungi or herbivory (Ton and Mauch-Mani, 2004 ; Bodenhausen and Reymond, 2007 ; Ton et al, 2009 ; Liu et al, 2020b ), activating the MYC branch of JA pathway (Pieterse et al, 2011 ; Vos et al, 2019 ). In this work, the similar levels of ABA seen in both inoculated and control plants suggests it does not play a part in defense response to PWN, as it was concluded for P. pinaster response to Fusarium circinatum (Hernandez-Escribano et al, 2020 ).…”

Effects of Mycorrhizal Colonization on Transcriptional Expression of the Responsive Factor JERF3 and Stress-Responsive Genes in Banana Plantlets in Response to Combined Biotic and Abiotic Stresses

“…Yazawa et al (2012) found that minimizing the ABA levels in rice plants increased their resistance to Magnaporthe oryzae, the causing agent of rice blast, by impairing the pathogen penetration ability and leading to a reduction in the disease incidence. However, their inducing effect on the plant defense was also reported (Vos et al, 2019). Furthermore, ABA modulates the mycorrhizal establishment by inducing the AMF colonization at low levels but impairs it at the high ABA levels (Charpentier et al, 2014).…”

Priming by Timing: Arabidopsis thaliana Adjusts Its Priming Response to Lepidoptera Eggs to the Time of Larval Hatching

“…In the study here, not only SA and JA-Ile levels but also ABA levels were significantly higher in previously egg-laden, feeding-damaged than in egg-free, feeding-damaged plants ( Figures 4B , 7B ). ABA-mediated signaling may synergistically interact with JA-mediated plant responses to chewing insects ( Pieterse et al, 2012 ; Nguyen et al, 2016 ; Vos et al, 2019 ). Our results show that an egg-mediated increase of JA-Ile levels 3 h after the onset of feeding preceded the ABA burst after 12 h feeding upon egg-laden plants ( Figure 4B ).…”