Stress- and pathway-specific impacts of impaired jasmonoyl-isoleucine (JA-Ile) catabolism on defense signaling and biotic stress resistance in Arabidopsis

Abstract

20 21 Jasmonate (JA) synthesis and signaling are essential for plant defense upregulation upon 22 46 47 48 identification of jasmonoyl-isoleucine (JA-Ile) as the critical bioactive form in 2007 (Chini et 54 al. 2007; Thines et al. 2007), many derivatives of jasmonic acid (JA) were described, resulting 55 from hydroxylation, conjugation to sugars (Miersch et al. 2008), amino acids or amino 56 cyclopropane carboxylic acid, sulfation (Gidda et al. 2003), decarboxylation and many more 57 (Wasternack and Song 2017). The enzymes responsible for these modifications have not all 58 been identified and the function of these derivatives, if any, are generally unknown. The master 59 regulator jasmonoyl-(L)-isoleucine (JA-Ile) results from a specific conjugation reaction of 60 jasmonic acid (JA) by the enzyme JASMONATE RESISTANT 1 (JAR1). In the core 61 perception and signaling pathways, JA-Ile acts as a ligand promoting the assembly of the co-62 receptor CORONATINE INSENSITIVE 1 (COI1) with distinct JASMONATE ZIM-DOMAIN 63 PROTEIN (JAZ) that otherwise powerfully repress target transcription factors and responses. 64 After assembly, COI1-JAZ is recruited into the E3 ubiquitin ligase SCF COI1 that tags JAZs for 65 proteolytic degradation, and provides the basis for JA-Ile-responsive gene de-repression (Chini 66 et al. 2007; Thines et al. 2007). Several hundreds to thousands of genes are under this control, 67 and depending on developmental stage, organ, nature of stimulus, and crosstalks with other 68 hormones, a wide array of JAZ-transcription factor combinations provide specificity to the 69 system with only one major hormonal ligand (Chini et al. 2016). Distinct JA-Ile-triggered 70 networks regulate leaf defenses against different types of aggressors and are integrated by 71 separate sets of transcription factors (TF). MYC2, a bHLH type TF, integrates (together with 72 MYC3 and MYC4) simultaneous JA/abscisic acid stimuli and defines a wound/insect-specific 73 branch reflected by induction of markers such as vegetative storage protein (VSP); 74 ERF1/ORA59 TFs integrate concomitant JA/ethylene signals into a microbe-specific branch 75 probed by plant defensin PDF1.2 (Pieterse et al. 2012; Wasternack and Hause 2013). 76 77 JA signaling, like any hormonal pathway, needs to be tightly controlled in time and space, 78 particularly because defense upregulation is costly and linked to overall growth inhibition. This 79 antagonism was long thought to be merely imposed by limited resources that need to be re-80 allocated from developmental to defense sinks (Havko et al. 2016), but recent advances have 81 shown that additional hardwire connections control growth-defense tradeoffs (Campos et al. 82 2014; Guo et al. 2018). For appropriate control of JA responses, plants rely on a number of 83 negative feedback mechanisms. In addition to JAZ repressor proteins, other negative regulators 84 were identified that repress JA responses at the promoter level, including JAV (Yan et al. 2018) 85 and the JAM subclass of bHLH (Sasaki-Sekimoto ...

Use of sugarcane mosaic virus for virus-induced gene silencing in maize

“…Our observation of decreased S. frugiperda growth due to ZmCYP94B1 expression silencing is different from what was observed with Arabidopsis, where S. littoralis larval growth on a cyp94B1 cyp94B3 cyp94C1 triple mutant was improved relative to wildtype plants (Marquis et al, 2020). The faster caterpillar weight gain on this triple mutant was ascribed to the higher expression of JAZ repressor proteins, which negatively regulate defense-induced genes, in the triple mutant.…”

“…A phylogenetic analysis (Figure 7) showed that ZmJIH1 (GRMZM2G090779) is the closest maize homolog of Nicotiana attenuata JIH1 (Woldemariam et al, 2012), rice AH8 (Hazman et al, 2019), and Arabidopsis IAR3 (Marquis et al, 2020), which have previously been identified as JA-Ile hydrolases. We cloned a fragment of this gene into SCMV-CS3 for VIGS experiments.…”

“…Whereas the JAR1 protein conjugates jasmonate and isoleucine to form JA-Ile (Staswick et al, 2002;Koo and Howe, 2009), experiments with Nicotiana attenuata showed that JA-Ile can be inactivated by JIH1-mediated cleavage to jasmonate and isoleucine (Woldemariam et al, 2012;Woldemariam et al, 2014). Similarly, Arabidopsis thaliana (Arabidopsis) iar3 ill6 double knockouts, which are defective in JA-Ile deconjugation, exhibited increased JA-Ile accumulation (Marquis et al, 2020). The Oryza sativa (rice) genes IAR3 and AH8 encode similar JA-Ile hydrolases (Hazman et al, 2019).…”

“…Research with Arabidopsis showed that JA-Ile can be hydroxylated by CYP94B1 and CYP94B3 to produce 12-hydroxy jasmonate-isoleucine (12OH-JA-Ile), which is less efficient than JA-Ile in eliciting COI1-mediated JAZ protein degradation (Kitaoka et al, 2011;Koo et al, 2011;Koo et al, 2014;Marquis et al, 2020). A rice gene, CYP94B5 also encodes a JA-Ile C12hydroxylase (Hazman et al, 2019).…”

“…Similarly, knockout of the two Arabidopsis JA-Ile hydrolase genes, IAR3 and ILL6, decreased S. littoralis caterpillar growth (Marquis et al, 2020) and knockout of jasmonate hydroxylases increased resistance to multiple biotic and abiotic stresses (Caarls et al, 2017;Smirnova et al, 2017;Marquis et al, 2021).…”