In tomato (Solanum lycopersicum), as in other plants, the immunity hormone jasmonate (JA) triggers genome-wide transcriptional changes in response to pathogen and insect attack. These changes are largely regulated by the basic helix-loop-helix (bHLH) transcription factor MYC2. The function of MYC2 depends on its physical interaction with the MED25 subunit of the Mediator transcriptional coactivator complex. Although much has been learned about the MYC2-dependent transcriptional activation of JA-responsive genes, relatively less studied is the termination of JA-mediated transcriptional responses and the underlying mechanisms. Here, we report an unexpected function of MYC2 in regulating the termination of JA signaling through activating a small group of JA-inducible bHLH proteins, termed MYC2-TARGETED BHLH1 (MTB1), MTB2, and MTB3. MTB proteins negatively regulate JA-mediated transcriptional responses via their antagonistic effects on the functionality of the MYC2-MED25 transcriptional activation complex. MTB proteins impair the formation of the MYC2-MED25 complex and compete with MYC2 to bind to its target gene promoters. Therefore, MYC2 and MTB proteins form an autoregulatory negative feedback circuit to terminate JA signaling in a highly organized manner. We provide examples demonstrating that gene editing tools such as CRISPR/Cas9 open up new avenues to exploit MTB genes for crop protection.

Flowering time of plants must be tightly regulated to maximize reproductive success. Plants have evolved sophisticated signaling network to coordinate the timing of flowering in response to their ever-changing environmental conditions. Besides being a key immune signal, the lipid-derived plant hormone jasmonate (JA) also regulates a wide range of developmental processes including flowering time. Here, we report that the CORONATINE INSENSITIVE1 (COI1)-dependent signaling pathway delays the flowering time of Arabidopsis thaliana by inhibiting the expression of the florigen gene FLOWERING LOCUS T (FT). We provide genetic and biochemical evidence that the APETALA2 transcription factors (TFs) TARGET OF EAT1 (TOE1) and TOE2 interact with a subset of JAZ (jasmonate-ZIM domain) proteins and repress the transcription of FT. Our results support a scenario that, when plants encounter stress conditions, bioactive JA promotes COI1-dependent degradation of JAZs. Degradation of the JAZ repressors liberates the transcriptional function of the TOEs to repress the expression of FT and thereby triggers the signaling cascades to delay flowering. Our study identified interacting pairs of TF and JAZ transcriptional regulators that underlie JA-mediated regulation of flowering, suggesting that JA signals are converted into specific context-dependent responses by matching pairs of TF and JAZ proteins.

ORCID IDs: 0000-0001-6683-6415 (J.X.); 0000-0002-9910-3119 (J.M.); 0000-0002-4265-7399 (J.L.); 0000-0002-0757-5208 (Q.W.); 0000-0003-2959-6461 (S.Z.)Antimicrobial compounds have critical roles in plant immunity; for example, Arabidopsis thaliana and other crucifers deploy phytoalexins and glucosinolate derivatives in defense against pathogens. The pathogen-responsive MITOGEN-ACTIVATED PROTEIN KINASE3 (MPK3) and MPK6 have essential functions in the induction of camalexin, the major phytoalexin in Arabidopsis. In search of cyanide, a coproduct of ethylene and camalexin biosynthesis, we found that MPK3 and MPK6 also affect the accumulation of extracellular thiocyanate ion derived from the indole glucosinolate (IGS) pathway. Botrytis cinerea infection activates MPK3/MPK6, which promote indole-3-yl-methylglucosinolate (I3G) biosynthesis and its conversion to 4-methoxyindole-3-yl-methylglucosinolate (4MI3G). Gain-and loss-of-function analyses demonstrated that MPK3/MPK6 regulate the expression of MYB51 and MYB122, two key regulators of IGS biosynthesis, as well as CYP81F2 and IGMT1/ IGMT2, which encode enzymes in the conversion of I3G to 4MI3G, through ETHYLENE RESPONSE FACTOR6 (ERF6), a substrate of MPK3/MPK6. Under the action of PENETRATION2 (PEN2), an atypical myrosinase, and PEN3, an ATP binding cassette transporter, 4MI3G is converted to extracellular unstable antimicrobial compounds, possibly isothiocyanates that can react with nucleophiles and release the stable thiocyanate ion. Recent studies demonstrated the importance of PEN2/ PEN3-dependent IGS derivatives in plant immunity. Here, we report that MPK3/MPK6 and their substrate ERF6 promote the biosynthesis of IGSs and the conversion of I3G to 4MI3G, a target of PEN2/PEN3-dependent chemical defenses in plant immunity.

The tryptophan (Trp)‐derived plant secondary metabolites, including camalexin, 4‐hydroxy‐indole‐3‐carbonylnitrile, and indolic glucosinolate (IGS), show broad‐spectrum antifungal activity. However, the distinct regulations of these metabolic pathways among different plant species in response to fungus infection are rarely studied. In this study, our results revealed that WRKY33 directly regulates IGS biosynthesis, notably the production of 4‐methoxyindole‐3‐ylmethyl glucosinolate (4MI3G), conferring resistance to Alternaria brassicicola, an important pathogen which causes black spot in Brassica crops. WRKY33 directly activates the expression of CYP81F2, IGMT1, and IGMT2 to drive side‐chain modification of indole‐3‐ylmethyl glucosinolate (I3G) to 4MI3G, in both Arabidopsis and Chinese kale (Brassica oleracea var. alboglabra Bailey). However, Chinese kale showed a more severe symptom than Arabidopsis when infected by Alternaria brassicicola. Comparative analyses of the origin and evolution of Trp metabolism indicate that the loss of camalexin biosynthesis in Brassica crops during evolution might attenuate the resistance of crops to Alternaria brassicicola. As a result, the IGS metabolic pathway mediated by WRKY33 becomes essential for Chinese kale to deter Alternaria brassicicola. Our results highlight the differential regulation of Trp‐derived camalexin and IGS biosynthetic pathways in plant immunity between Arabidopsis and Brassica crops.

Attack of plants by both viruses and their vectors is common in nature. Yet the dynamics of the plant-virus-vector tripartite system, in particular the effects of viral infection on plant-insect interactions, have only begun to emerge in the last decade. Viruses can modulate the interactions between insect vectors and plants via the jasmonate, salicylic acid and ethylene phytohormone pathways, resulting in changes in fitness and viral transmission capacity of their insect vectors. Virus infection of plants may also modulate other phytohormones, such as auxin, gibberellins, cytokinins, brassinosteroids, and abscisic acid, with yet undefined consequences on plant-insect interactions. Moreover, virus infection in plants may incur changes to other plant traits, such as nutrition and secondary metabolites, that potentially contribute to virus-associated, phytohormone-mediated manipulation of plant-insect interactions. In this article, we review the research progress, discuss issues related to the complexity and variability of the viral modulation of plant interactions with insect vectors, and suggest future directions of research in this field.