Organ-specific responses during acclimation of mycorrhizal and non-mycorrhizal tomato plants to a mild water stress reveal differential local and systemic hormonal and nutritional adjustments.

MAIN CONCLUSION: Tomato plant acclimation to a mild water stress implied tissue-specific hormonal and nutrient adjustments, being the root one of the main modulators of this response. Phytohormones are key regulators of plant acclimation to water stress. However, it is not yet clear if these hormonal responses follow specific patterns depending on the plant tissue. In this study, we evaluated the organ-specific physiological and hormonal responses to a 14 day-long mild water stress in tomato plants (Solanum lycopersicum cv. Moneymaker) in the presence or absence of the arbuscular mycorrhizal fungus Rhizoglomus irregulare, a frequently used microorganism in agriculture. Several physiological, production, and nutritional parameters were evaluated throughout the experiments. Additionally, endogenous hormone levels in roots, leaves, and fruits at different developmental stages were quantified by ultrahigh-performance liquid chromatography coupled to tandem mass spectrometry (UHPLC-MS/MS). Water deficit drastically reduced shoot growth, while it did not affect fruit production. In contrast, fruit production was enhanced by mycorrhization regardless of the water treatment. The main tissue affected by water stress was the root system, where huge rearrangements in different nutrients and stress-related and growth hormones took place. Abscisic acid content increased in every tissue and fruit developmental stage, suggesting a systemic response to drought. On the other hand, jasmonate and cytokinin levels were generally reduced upon water stress, although this response was dependent on the tissue and the hormonal form. Finally, mycorrhization improved plant nutritional status content of certain macro and microelements, specially at the roots and ripe fruits, while it affected jasmonate response in the roots. Altogether, our results suggest a complex response to drought that consists in systemic and local combined hormonal and nutrient responses.

Water stress protection by the arbuscular mycorrhizal fungus Rhizoglomus irregulare involves physiological and hormonal responses in an organ-specific manner.

Arbuscular mycorrhizal fungi may alleviate water stress in plants. Although several protection mechanisms have already been described, little information is available on how these fungi influence the hormonal response to water stress at an organ-specific level. In this study, we evaluated the physiological and hormonal responses to water stress in above and below-ground tissues of the legume grass Trifolium repens colonized by the arbuscular mycorrhizal fungus Rhizoglomus irregulare. Plants were subjected to progressive water stress and recovery. Different leaf and root physiological parameters, as well as phytohormone levels, were quantified. Water-stressed mycorrhizal plants showed an improved water status and no photoinhibition compared to uncolonized individuals, while some stress markers like α-tocopherol and malondialdehyde content, an indicator of the extent of lipid peroxidation, transiently increased in roots, but not in leaves. Water stress protection exerted by mycorrhiza appeared to be related to a differential root-to-shoot redox signaling, probably mediated by jasmonates, and mycorrhization enhanced the production of the cytokinin trans-zeatin in both roots and leaves. Overall, our results suggest that mycorrhization affects physiological, redox and hormonal responses to water stress at an organ-specific level, which may eventually modulate the final protection of the host from water stress.

Differential Tissue-Specific Jasmonic Acid, Salicylic Acid, and Abscisic Acid Dynamics in Sweet Cherry Development and Their Implications in Fruit-Microbe Interactions.

Sweet cherry is an important non-climacteric fruit with a high commercial interest, but exploitation of sweet cherry trees (Prunus avium L.) in orchards is usually subject to important economic losses due to fruit decay by pathogenic fungi and other microorganisms. Sweet cherries development and ripening are characterized by profound physiological changes in the fruit, among which the phytohormone abscisic acid (ABA) plays a pivotal role. In addition, sweet cherries are usually affected by fruit decay pathogens, and the role of other stress-related hormones such as jasmonic acid (JA) and salicylic acid (SA) may also be of paramount importance, not only from a developmental point of view, but also from a fruit-microbe interaction perspective. Here, a tissue-specific hormone quantification by LC-MS/MS, including the contents of JA, SA, and ABA, in the fruit exocarp and mesocarp of sweet cherries during fruit development from trees growing in a commercial orchard was carried out. Additionally, this study was complemented with the characterization of the culturable epiphytic and endophytic microbial communities of sweet cherries at various stages of fruit development and during cracking lesion formation. Our results revealed a completely differential behavior of phytohormones between both tissues (the exocarp and mesocarp), with a more dynamic exocarp in front of a more stable mesocarp, and with marked variations during fruit development. Microbial epiphytic community was mainly composed by yeasts, although rot-causing fungi like Alternaria spp. were always also present throughout fruit development. Endophytic colonization was poor, but it increased throughout fruit development. Furthermore, when the exocarp was naturally disrupted in sweet cherries suffering from cracking, the colonization by Alternaria spp. markedly increased. Altogether, results suggest that the fruit exocarp and mesocarp are very dynamic tissues in which endogenous phytohormones not only modulate fruit development and ripening but also fruit-microbe interactions.

Pattern-triggered immunity restricts host colonization by endophytic fusaria, but does not affect endophyte-mediated resistance.

Fusarium oxysporum (Fo) is best known as a host-specific vascular pathogen causing major crop losses. Most Fo strains, however, are root endophytes potentially conferring endophyte-mediated resistance (EMR). EMR is a mechanistically poorly understood root-specific induced resistance response induced by endophytic or nonhost pathogenic Fo strains. Like other types of induced immunity, such as systemic acquired resistance or induced systemic resistance, EMR has been proposed to rely on the activation of the pattern-triggered immunity (PTI) system of the plant. PTI is activated upon recognition of conserved microbe-associated molecular patterns (MAMPs) of invading microbes. Here, we investigated the role of PTI in controlling host colonization by Fo endophytes and their ability to induce EMR to the tomato pathogen Fo f. sp. lycopersici (Fol). Transgenic tomato and Arabidopsis plants expressing the Fo effector gene Avr2 are hypersusceptible to bacterial and fungal infection. Here we show that these plants are PTI-compromised and are nonresponsive to bacterial- (flg22) and fungal- (chitosan) MAMPs. We challenged the PTI-compromised tomato mutants with the EMR-conferring Fo endophyte Fo47, the nonhost pathogen Fom (a melon pathogen), and with Fol. Compared to wild-type plants, Avr2-tomato plants became hypercolonized by Fo47 and Fom. Surprisingly, however, EMR towards Fol, induced by either Fo47 or Fom, was unaffected in these plants. These data show that EMR-based disease resistance is independent from the conventional defence pathways triggered by PTI, but that PTI is involved in restricting host colonization by nonpathogenic Fo isolates.

Abscisic Acid Connects Phytohormone Signaling with RNA Metabolic Pathways and Promotes an Antiviral Response that Is Evaded by a Self-Controlled RNA Virus.

A complex network of cellular receptors, RNA targeting pathways, and small-molecule signaling provides robust plant immunity and tolerance to viruses. To maximize their fitness, viruses must evolve control mechanisms to balance host immune evasion and plant-damaging effects. The genus Potyvirus comprises plant viruses characterized by RNA genomes that encode large polyproteins led by the P1 protease. A P1 autoinhibitory domain controls polyprotein processing, the release of a downstream functional RNA-silencing suppressor, and viral replication. Here, we show that P1Pro, a plum pox virus clone that lacks the P1 autoinhibitory domain, triggers complex reprogramming of the host transcriptome and high levels of abscisic acid (ABA) accumulation. A meta-analysis highlighted ABA connections with host pathways known to control RNA stability, turnover, maturation, and translation. Transcriptomic changes triggered by P1Pro infection or ABA showed similarities in host RNA abundance and diversity. Genetic and hormone treatment assays showed that ABA promotes plant resistance to potyviral infection. Finally, quantitative mathematical modeling of viral replication in the presence of defense pathways supported self-control of polyprotein processing kinetics as a viral mechanism that attenuates the magnitude of the host antiviral response. Overall, our findings indicate that ABA is an active player in plant antiviral immunity, which is nonetheless evaded by a self-controlled RNA virus.

Corrigendum: Xylem Sap Proteomics Reveals Distinct Differences Between R Gene- and Endophyte-Mediated Resistance Against Fusarium Wilt Disease in Tomato.

[This corrects the article DOI: 10.3389/fmicb.2018.02977.].

Xylem Sap Proteomics Reveals Distinct Differences Between R Gene- and Endophyte-Mediated Resistance Against Fusarium Wilt Disease in Tomato.

Resistance (R) genes and endophytic organisms can both protect plants against pathogens. Although the outcome of both processes is the same, little is known about the commonalities and differences between both immune responses. Here we set out to phenotypically characterize both responses in the tomato-Fusarium pathosystem, and to identify markers to distinguish these responses at the molecular level. As endophyte Fusarium oxysporum (Fo) strain Fo47 was employed, which confers protection against various pathogens, including the vascular wilt fungus F. oxysporum f.sp. lycopersici (Fol). As R-gene conferring Fol resistance, the I-2 gene of tomato (Solanum lycopersicum) was used. Fol colonizes the xylem vessels of susceptible and I-2 resistant tomato plants, but only causes disease in the former. Fol was found to colonize the vasculature of endophyte-colonized plants, and could be isolated from stems of non-diseased plants co-inoculated with Fo47 and Fol. Because the xylem vessels form the main interface between plant and pathogen, the xylem sap proteomes during R gene- and Endophyte-Mediated Resistance (RMR and EMR) were compared using label-free quantitative nLC-MS/MS. Surprisingly, both proteomes were remarkably similar to the mock, revealing only one or two differentially accumulated proteins in the respective resistant interactions. Whereas in I-2 plants the accumulation of the pathogenesis-related protein PR-5x was strongly induced by Fol, the endophyte triggered induction of both NP24, another PR-5 isoform, and of a ß-glucanase in the presence of Fol. Notably, over 54% of the identified xylem sap proteins have a predicted intracellular localization, which implies that these might be present in exosomes. In conclusion, whereas both resistance mechanisms permit the pathogen to colonize the vasculature, this does not result in disease and this resistance coincides with specific induction of two distinct PR-5 isoforms and a ß-glucanase.