As sessile organisms, plants must tolerate various environmental stresses. Plant hormones play vital roles in plant responses to biotic and abiotic stresses. Among these hormones, jasmonic acid (JA) and its precursors and derivatives (jasmonates, JAs) play important roles in the mediation of plant responses and defenses to biotic and abiotic stresses and have received extensive research attention. Although some reviews of JAs are available, this review focuses on JAs in the regulation of plant stress responses, as well as JA synthesis, metabolism, and signaling pathways. We summarize recent progress in clarifying the functions and mechanisms of JAs in plant responses to abiotic stresses (drought, cold, salt, heat, and heavy metal toxicity) and biotic stresses (pathogen, insect, and herbivore). Meanwhile, the crosstalk of JA with various other plant hormones regulates the balance between plant growth and defense. Therefore, we review the crosstalk of JAs with other phytohormones, including auxin, gibberellic acid, salicylic acid, brassinosteroid, ethylene, and abscisic acid. Finally, we discuss current issues and future opportunities in research into JAs in plant stress responses.

Function and Mechanism of Jasmonic Acid in Plant Responses to Abiotic and Biotic Stresses.

The whitefly Bemisia tabaci is one of the world’s most important invasive crop pests, possibly because it manipulates plant defense signaling. Upon infestation by whiteflies, plants mobilize salicylic acid (SA)-dependent defenses, which mainly target pathogens. In contrast, jasmonic acid (JA)-dependent defenses are gradually suppressed in whitefly-infested plants. The down-regulation of JA defenses make plants more susceptible to insects, including whiteflies. Here, we report that this host–plant manipulation extends to neighboring plants via airborne signals. Plants respond to insect attack with the release of a blend of inducible volatiles. Perception of these volatiles by neighboring plants usually primes them to prepare for an imminent attack. Here, however, we show that whitefly-induced tomato plant volatiles prime SA-dependent defenses and suppress JA-dependent defenses, thus rendering neighboring tomato plants more susceptible to whiteflies. Experiments with volatiles from caterpillar-damaged and pathogen-infected plants, as well as with synthetic volatiles, confirm that whiteflies modify the quality of neighboring plants for their offspring via whitefly-inducible plant volatiles.

https://www.pnas.org/content/pnas/116/15/7387.full.pdf

Airborne host-plant manipulation by whiteflies via an inducible blend of plant volatiles.

Phytohormone, particularly jasmonate (JA) and salicylate (SA) signaling, plays a central role in plant responses to herbivore and pathogen attack. Generally, SA mediates resistance responses against biotrophic pathogens and phloem-feeding insects, while JA mediates responses against necrotrophic pathogens and chewing insects. The phytohormonal responses mediating rice resistance to a piercing-sucking herbivore, the brown planthopper (BPH), remains unknown. Here, we combined transcriptome analysis, hormone measurements, genetic analysis and a field study to address this issue. Infestation by BPH adult females resulted in significant transcriptional reprograming. The upregulated genes were enriched in the JA signaling pathway. Consistently, the concentrations of JAs, but not SA, were dramatically increased in response to BPH attack. Two JA-deficient lines (AOC and MYC2 knockout) and two SA-deficient lines (nahG overexpression and NPR1 knockout) were constructed. BPH performed better on JA-deficient lines than on wild-type (WT) plants, but similarly on SA-deficient and WT plants. During BPH attack, the accumulation of defensive secondary metabolites was attenuated in JA-deficient lines compared with WT plants. Moreover, MYC2 mutants were more susceptible to planthoppers than WT plants in nature. This study reveals that JA signaling functions in rice defense against BPH.

Molecular dissection of rice phytohormone signaling involved in resistance to a piercing-sucking herbivore

Most plant viruses are vectored by insects and the interactions of virus-plant-vector have important ecological and evolutionary implications. Insect vectors often perform better on virus-infected plants. This indirect mutualism between plant viruses and insect vectors promotes the spread of virus and has significant agronomical effects. However, few studies have investigated how plant viruses manipulate plant defenses and promote vector performance. Begomoviruses are a prominent group of plant viruses in tropical and sub-tropical agro-ecosystems and are transmitted by whiteflies. Working with the whitefly Bemisia tabaci, begomoviruses and tobacco, we revealed that C2 protein of begomoviruses lacking DNA satellites was responsible for the suppression of plant defenses against whitefly vectors. We found that infection of plants by tomato yellow leaf curl virus (TYLCV), one of the most devastating begomoviruses worldwide, promoted the survival and reproduction of whitefly vectors. TYLCV C2 protein suppressed plant defenses by interacting with plant ubiquitin. This interaction compromised the degradation of JAZ1 protein, thus inhibiting jasmonic acid defense and the expression of MYC2-regulated terpene synthase genes. We further demonstrated that function of C2 protein among begomoviruses not associated with satellites is well conserved and ubiquitination is an evolutionarily conserved target of begomoviruses for the suppression of plant resistance to whitefly vectors. Taken together, these results demonstrate that ubiquitination inhibition by begomovirus C2 protein might be a general mechanism in begomovirus, whitefly and plant interactions.

/pdf/plant-begomoviruses-subvert-ubiquitination-to-suppress-plant-1brck8yfv3.pdf

Plant begomoviruses subvert ubiquitination to suppress plant defenses against insect vectors.

The Bemisia tabaci is a major leaf feeding insect pest to pepper (Capsicum annuum), causing serious damage to pepper growth and yield. It is particularly important to study the mechanism of pepper resistance to B. tabaci, and to breed and promote the varieties of pepper resistant to B. tabaci. However, very limited molecular mechanism is available about how plants perceive and defend themselves from the destructive pest. Proteome technologies have provided an idea method for studying plant physiological processes in response to B. tabaci. Here, a highly resistant genotype and a highly susceptible genotype were exposed to B. tabaci feeding for 48 h to explore the defense mechanisms of pepper resistance to B. tabaci. The proteomic differences between both genotypes were compared using isobaric tag for relative and absolute quantification (iTRAQ). The quantitative data were validated by parallel reaction monitoring (PRM). The results showed that 37 differential abundance proteins (DAPs) were identified in the RG (resistant genotype), while 17 DAPs were identified in the SG (susceptible genotype) at 48 h after B. tabaci feeding. 77 DAPs were identified when comparing RG with SG without feeding. The DAP functions were determined for the classification of the pathways, mainly involved in redox regulation, stress response, protein metabolism, lipid metabolism and carbon metabolism. Some candidate DAPs are closely related to B. tabaci resistance such as annexin D4-like (ANN4), calreticulin-3 (CRT3), heme-binding protein 2-like (HBP1), acidic endochitinase pcht28-like (PR3) and lipoxygenase 2 (LOX2). Taken together, this study indicates complex resistance-related events in B. tabaci interaction, provides novel insights into the molecular mechanism underlying the response of plant to B. tabaci, and identifies some candidate proteins against B. tabaci attack.

/pdf/proteomic-analysis-by-itraq-prm-provides-integrated-insight-2tuyz266lu.pdf

Proteomic analysis by iTRAQ-PRM provides integrated insight into mechanisms of resistance in pepper to Bemisia tabaci (Gennadius)

The silverleaf whitefly Bemisia tabaci is an important and invasive crop pest in many countries. Previous laboratory studies with Arabidopsis thaliana demonstrated that B. tabaci can suppress jasmonic acid (JA) defenses and thereby enhance B. tabaci performance. Whether B. tabaci has similar effects on other plants and in the field is unknown. In the present study, we found that, relative to wild-type (WT) tomato plants, transgenic tomato mutants that activated JA defenses (35s::prosys) or impaired JA defenses (spr-2 and def-1) did not affect the survival or reproduction of B. tabaci adults in growth chamber experiments. In contrast, tomato mutants that activated JA defenses slowed B. tabaci nymphal development, while mutants that impaired JA defenses accelerated nymphal development. These effects of JA defenses on nymphal development were also documented under semi-field conditions. Changes in the expression of defense genes and in the production of phytohormones indicated that B. tabaci can suppress JA-dependent defenses after infestation for > 72 h. The suppression of JA was correlated with the induction of SA in B. tabaci-infested leaves under laboratory and under semi-field conditions. If SA signaling was blocked, JA accumulation increased in infested leaves and B. tabaci nymphal development was delayed. These results indicate that, although JA signalling helps in mediating tomato responses against B. tabaci nymphs, B. tabaci can inhibit JA biosynthesis and its action in an SA-dependent manner.

/pdf/jasmonic-acid-dependent-defenses-play-a-key-role-in-3brn5mxo3h.pdf

Jasmonic Acid-Dependent Defenses Play a Key Role in Defending Tomato Against Bemisia tabaci Nymphs, but Not Adults.

Widespread mislabeling of nonnative apple snails (Ampullariidae: Pomacea) as native field snails (Viviparidae: Cipangopaludina) on the Chinese food markets

Background Herbivore-induced plant volatiles (HIPVs) can prime plant defenses and enhance herbivore resistance in neighboring plants. Although a trade-off between constitutive defense and HIPV emission has been documented in many plant species, little is known about the effect of HIPV variation on defense priming, and whether there is a trade-off between defense priming and constitutive defense in neighboring plants. Results Using three tomato genotypes, including two wild types [Moneymaker (MM) and Castlemart (CM)] and one jasmonic acid (JA) overexpression 35S::prosys genotype, we investigated the effects of exposure to volatiles from plants infested by beet armyworm (Spodoptera exigua) caterpillars on the defenses and resistance of conspecific neighboring plants. We also analyzed the HIPV emissions from the three genotypes and their constitutive defense and resistance. Exposure to volatiles from S. exigua-infested MM plants primed an array of defensive responses (including the accumulation of JA and PI-II protein and the expression of the defense genes PI-I and PI-II), and enhanced plant resistance against the caterpillars. In contrast, exposure to volatiles from S. exigua-infested CM or 35S::prosys did not result in defense priming or an increase in plant resistance. Analyses of HIPVs and gene expression indicated that defense priming in MM was due to enhanced emission of β-ocimene and linalool. We further demonstrated that levels of constitutive defense and resistance are low in MM and high in CM and 35S::prosys, suggesting a negative correlation between defense priming and constitutive defense. Conclusion Our findings suggest that there is a trade-off between defense priming by HIPVs and constitutive defense in tomato. This suggests that defense priming should be used with caution in agriculture. © 2020 Society of Chemical Industry.

Trade-off between defense priming by herbivore-induced plant volatiles and constitutive defense in tomato.

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Jasmonic Acid-Dependent Defenses Play a Key Role in Defending Tomato Against Bemisia tabaci Nymphs, but Not Adults.

Widespread mislabeling of nonnative apple snails (Ampullariidae: Pomacea) as native field snails (Viviparidae: Cipangopaludina) on the Chinese food markets

Trade-off between defense priming by herbivore-induced plant volatiles and constitutive defense in tomato.