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In low nutritive environments, the uptake of N by arbuscular mycorrhizal (AM) fungi may confer competitive advantages for the host. The present study aims to understand how mycorrhizal tomato plants perceive and then prepare for an N depletion in the root environment. Plants colonized by Rhizophagus irregularis displayed improved responses to a lack of N than nonmycorrhizal (NM) plants. These responses were accomplished by a complex metabolic and transcriptional rearrangement that mostly affected the gibberellic acid and jasmonic acid pathways involving DELLA and JAZ1 genes, which were responsive to changes in the C/N imbalance of the plant. N starved mycorrhizal plants showed lower C/N equilibrium in the shoots than starved NM plants and concomitantly a downregulation of the JAZ1 repressor and the increased expression of the DELLA gene, which translated into a more active oxylipin pathway in mycorrhizal plants. In addition, the results support a priorization in AM plants of stress responses over growth. Therefore, these plants were better prepared for an expected stress. Furthermore, most metabolites that were severely reduced in NM plants following the N depletion remained unaltered in starved AM plants compared with those normally fertilized, suggesting that the symbiosis buffered the stress, improving plant development in a stressed environment.

Arbuscular mycorrhizal symbiosis is restricted in roots, but it also improves shoot responses against leaf challenges, a phenomenon known as Mycorrhiza-Induced Resistance (MIR). This study focuses on mycorrhizal root signals that may orchestrate shoot defence responses. Metabolomic analysis of non-mycorrhizal and mycorrhizal plants upon Botrytis cinerea infection showed that roots rearrange their metabolome mostly in response to the symbiosis, whereas in shoots a stronger impact of the infection is observed. Specific clusters of compounds in shoots and roots display a priming profile suggesting an implication in the enhanced resistance observed in mycorrhizal plants. Among the primed pathways in roots, lignans showed the highest number of hits followed by oxocarboxylic acids, compounds of the amino acid metabolism, and phytohormones. The lignan yatein was present at higher concentrations in roots, root efflux and leaves of mycorrhizal plants This lignan displayed in vitro antimicrobial activity against B. cinerea and it was also functional protecting tomato plants. Besides, several JA defence-related genes were upregulated in mycorrhizal roots regardless of the pathogen infection, whereas PIN-II was primed in roots of mycorrhizal infected plants. These observations suggest that the enhanced resistance in shoots during MIR may be coordinated by lignans and oxylipins with the participation of roots., We thank the Serveis Centrals of Universitat Jaume I for the technical support. This work was financially supported by the Spanish Ministry MINECO RTL2018-094350-B-C33 and the grant to VP IJCI- 2015-24527 , by the Plan de Promoción de la Investigación-Universitat Jaume I P1.1B2015-33 and the GV/2018/115 from the program Apoyo para Grupos Emergentes, from the Generalitat Valenciana and to the Diputación de Castellón for funding the PRIMA-INTOMED consortium. We thank the grant BES-2016-077208 to NS.

Indole-3-carboxylic acid (I3CA) is an indolic compound that induces resistance in Arabidopsis adult plants against the necrotrophic fungus Plectosphaerella cucumerina through primed callose accumulation. In this study, we confirm the relevance of ATL31 and SYP121 genes involved in vesicular trafficking in I3CA priming of defenses and we discard camalexin as a mediator of I3CA-induced resistance (IR) in adult plants. In addition, we observed that an intact I3CA biosynthetic pathway is necessary for I3CA-IR functionality.

A fast callose accumulation has been shown to mediate defence priming in certain plant–pathogen interactions, but the events upstream of callose assembly following chemical priming are poorly understood, mainly because those steps comprise sugar transfer to the infection site. β-Amino butyric acid (BABA)-induced resistance in Arabidopsis against Plectosphaerella cucumerina is known to be mediated by callose priming. Indole-3-carboxylic acid (ICOOH, also known as I3CA) mediates BABA-induced resistance in Arabidopsis against P. cucumerina. This indolic compound is found in a common fingerprint of primed metabolites following treatments with various priming stimuli. In the present study, we show that I3CA induces resistance in Arabidopsis against P. cucumerina and primes enhancement of callose accumulation. I3CA treatment increased abscisic acid (ABA) levels before infection with P. cucumerina. An intact ABA synthesis pathway is needed to activate a starch amylase (BAM1) to trigger augmented callose deposition against P. cucumerina during I3CA-IR. To verify the relevance of the BAM1 amylase in I3CA-IR, knockdown mutants and overexpressors of the BAM1 gene were tested. The mutant bam1 was impaired to express I3CA-IR, but complemented 35S::BAM1-YFP lines in the background of bam1 restored an intact I3CA-IR and callose priming. Therefore, a more active starch metabolism is a committed step for I3CA-IR, inducing callose priming in adult plants. Additionally, I3CA treatments induced expression of the ubiquitin ligase ATL31 and syntaxin SYP131, suggesting that vesicular trafficking is relevant for callose priming. As a final element in the callose priming, an intact Powdery Mildew resistant4 (PMR4) gene is also essential to fully express I3CA-IR., The authors thank the Serveis Centrals de la Universitat Jaume I and particularly Cristian Barrera for their technical support. This work was financially supported by the Plan de Promoción de la Investigación de la Universitat Jaume I UJI‐B2016‐43, MINECO AGL2015‐64990‐C2‐2 and the Generalitat Valenciana AICO/2016/029.