SignificancePlant roots nurture a large diversity of soil microbes via exudation of chemical compounds into the rhizosphere. In turn, beneficial root microbiota promote plant growth and immunity. The root-specific transcription factor MYB72 has emerged as a central regulator in this process. Here, we show that MYB72 regulates the excretion of the coumarin scopoletin, an iron-mobilizing phenolic compound with selective antimicrobial activity that shapes the root-associated microbial community. Selected soil-borne fungal pathogens appeared to be highly sensitive to the antimicrobial activity of scopoletin, while two MYB72-inducing beneficial rhizobacteria were tolerant. Our results suggest that probiotic root-associated microbes that activate the iron-deficiency response during colonization stimulate MYB72-dependent excretion of scopoletin, thereby potentially improving their niche establishment and enhancing plant growth and protection.

Antagonism between the defense hormones salicylic acid (SA) and jasmonic acid (JA) plays a central role in the modulation of the plant immune signaling network, but the molecular mechanisms underlying this phenomenon are largely unknown. Here, we demonstrate that suppression of the JA pathway by SA functions downstream of the E3 ubiquitin-ligase Skip-Cullin-F-box complex SCF COI1 , which targets JASMONATE ZIM-domain transcriptional repressor proteins (JAZs) for proteasomemediated degradation. In addition, neither the stability nor the JA-induced degradation of JAZs was affected by SA. In silico promoter analysis of the SA/JA crosstalk transcriptome revealed that the 1-kb promoter regions of JA-responsive genes that are suppressed by SA are significantly enriched in the JA-responsive GCC-box motifs. Using GCC:GUS lines carrying four copies of the GCC-box fused to the b-glucuronidase reporter gene, we showed that the GCC-box motif is sufficient for SA-mediated suppression of JA-responsive gene expression. Using plants overexpressing the GCC-box binding APETALA2/ETHYLENE RESPONSE FACTOR (AP2/ERF) transcription factors ERF1 or ORA59, we found that SA strongly reduces the accumulation of ORA59 but not that of ERF1. Collectively, these data indicate that the SA pathway inhibits JA signaling downstream of the SCF COI1 -JAZ complex by targeting GCC-box motifs in JA-responsive promoters via a negative effect on the transcriptional activator ORA59.

SUMMARYIn nature, plants have to cope with a wide range of stress conditions that often occur simultaneously or in sequence. To investigate how plants cope with multi-stress conditions, we analyzed the dynamics of whole-transcriptome profiles of Arabidopsis thaliana exposed to six sequential double stresses inflicted by combinations of: (i) infection by the necrotrophic fungus Botrytis cinerea, (ii) herbivory by chewing larvae of Pieris rapae, and (iii) drought stress. Each of these stresses induced specific expression profiles over time, in which one-third of all differentially expressed genes was shared by at least two single stresses. Of these, 394 genes were differentially expressed during all three stress conditions, albeit often in opposite directions. When two stresses were applied in sequence, plants displayed transcriptome profiles that were very similar to the second stress, irrespective of the nature of the first stress. Nevertheless, significant first-stress signatures could be identified in the sequential stress profiles. Bioinformatic analysis of the dynamics of coexpressed gene clusters highlighted specific clusters and biological processes of which the timing of activation or repression was altered by a prior stress. The first-stress signatures in second stress transcriptional profiles were remarkably often related to responses to phytohormones, strengthening the notion that hormones are global modulators of interactions between different types of stress. Because prior stresses can affect the level of tolerance against a subsequent stress (e.g. prior herbivory strongly affected resistance to B. cinerea), the first-stress signatures can provide important leads for the identification of molecular players that are decisive in the interactions between stress response pathways.

SummaryIn Arabidopsis roots, the transcription factor MYB72 plays a dual role in the onset of rhizobacteria‐induced systemic resistance (ISR) and plant survival under conditions of limited iron availability. Previously, it was shown that MYB72 coordinates the expression of a gene module that promotes synthesis and excretion of iron‐mobilizing phenolic compounds in the rhizosphere, a process that is involved in both iron acquisition and ISR signaling. Here, we show that volatile organic compounds (VOCs) from ISR‐inducing Pseudomonas bacteria are important elicitors of MYB72. In response to VOC treatment, MYB72 is co‐expressed with the iron uptake‐related genes FERRIC REDUCTION OXIDASE 2 (FRO2) and IRON‐REGULATED TRANSPORTER 1 (IRT1) in a manner that is dependent on FER‐LIKE IRON DEFICIENCY TRANSCRIPTION FACTOR (FIT), indicating that MYB72 is an intrinsic part of the plant's iron‐acquisition response that is typically activated upon iron starvation. However, VOC ‐induced MYB72 expression is activated independently of iron availability in the root vicinity. Moreover, rhizobacterial VOC‐mediated induction of MYB72 requires photosynthesis‐related signals, while iron deficiency in the rhizosphere activates MYB72 in the absence of shoot‐derived signals. Together, these results show that the ISR‐ and iron acquisition‐related transcription factor MYB72 in Arabidopsis roots is activated by rhizobacterial volatiles and photosynthesis‐related signals, and enhances the iron‐acquisition capacity of roots independently of the iron availability in the rhizosphere. This work highlights the role of MYB72 in plant processes by which root microbiota simultaneously stimulate systemic immunity and activate the iron‐uptake machinery in their host plants.

Jasmonic acid (JA) is a critical hormonal regulator of plant growth and defense. To advance our understanding of the architecture and dynamic regulation of the JA gene regulatory network, we performed a high-resolution RNA-seq time series of methyl JA-treated Arabidopsis thaliana at 15 time points over a 16-h period. Computational analysis showed that methyl JA (MeJA) induces a burst of transcriptional activity, generating diverse expression patterns over time that partition into distinct sectors of the JA response targeting specific biological processes. The presence of transcription factor (TF) DNA binding motifs correlated with specific TF activity during temporal MeJA-induced transcriptional reprogramming. Insight into the underlying dynamic transcriptional regulation mechanisms was captured in a chronological model of the JA gene regulatory network. Several TFs, including MYB59 and bHLH27, were uncovered as early network components with a role in pathogen and insect resistance. Analysis of subnetworks surrounding the TFs ORA47, RAP2.6L, MYB59, and ANAC055, using transcriptome profiling of overexpressors and mutants, provided insights into their regulatory role in defined modules of the JA network. Collectively, our work illuminates the complexity of the JA gene regulatory network, pinpoints and validates previously unknown regulators, and provides a valuable resource for functional studies on JA signaling components in plant defense and development.