Making a better home: modulation of plant defensive response by brevipalpus mites.

False-spider mites of the genus Brevipalpus are highly polyphagous pests that attack hundreds of plant species of distinct families worldwide. Besides causing direct damage, these mites may also act as vectors of many plant viruses that threaten high-value ornamental plants like orchids and economically important crops such as citrus and coffee. To better understand the molecular mechanisms behind plant-mite interaction we used an RNA-Seq approach to assess the global response of Arabidopsis thaliana (Arabidopsis) plants along the course of the infestation with Brevipalpus yothersi, the main vector species within the genus. Mite infestation triggered a drastic transcriptome reprogramming soon at the beginning of the interaction and throughout the time course, deregulating 1755, 3069 and 2680 genes at 6 hours after infestation (hai), 2 days after infestation (dai), and 6 dai, respectively. Gene set enrichment analysis revealed a clear modulation of processes related to the plant immune system. Co-expressed genes correlated with specific classes of transcription factors regulating defense pathways and developmental processes. Up-regulation of defensive responses correlated with the down-regulation of growth-related processes, suggesting the triggering of the growthdefense crosstalk to optimize plant fitness. Biological processes (BPs) enriched at all time points were markedly related to defense against herbivores and other biotic stresses involving the defense hormones salicylic acid (SA) and jasmonic acid (JA). Levels of both hormones were higher in plants challenged with mites than in the noninfested ones, supporting the simultaneous induction of genes from both pathways. To further clarify the functional relevance of the plant hormonal pathways on the interaction, we evaluated the mite performance on Arabidopsis mutants impaired in SA- or JAmediated response. Mite oviposition was lower on mutants defective in SA biosynthesis (sid2) and signaling (npr1), showing a function for SA pathway in improving the mite reproduction, an unusual mechanism compared to closely-related spider mites. Here we provide the first report on the global and dynamic plant transcriptome triggered by Brevipalpus feeding, extending our knowledge on plant-mite interaction. Furthermore, our results suggest that Brevipalpus mites manipulate the plant defensive response to render the plant more susceptible to their colonization by inducing the SA-mediated pathway

Acylsugars protect Nicotiana benthamiana against insect herbivory and desiccation.

peer reviewedKEY MESSAGE: Nicotiana benthamiana acylsugar acyltransferase (ASAT) is required for protection against desiccation and insect herbivory. Knockout mutations provide a new resource for investigation of plant-aphid and plant-whitefly interactions. Nicotiana benthamiana is used extensively as a transient expression platform for functional analysis of genes from other species. Acylsugars, which are produced in the trichomes, are a hypothesized cause of the relatively high insect resistance that is observed in N. benthamiana. We characterized the N. benthamiana acylsugar profile, bioinformatically identified two acylsugar acyltransferase genes, ASAT1 and ASAT2, and used CRISPR/Cas9 mutagenesis to produce acylsugar-deficient plants for investigation of insect resistance and foliar water loss. Whereas asat1 mutations reduced accumulation, asat2 mutations caused almost complete depletion of foliar acylsucroses. Three hemipteran and three lepidopteran herbivores survived, gained weight, and/or reproduced significantly better on asat2 mutants than on wildtype N. benthamiana. Both asat1 and asat2 mutations reduced the water content and increased leaf temperature. Our results demonstrate the specific function of two ASAT proteins in N. benthamiana acylsugar biosynthesis, insect resistance, and desiccation tolerance. The improved growth of aphids and whiteflies on asat2 mutants will facilitate the use of N. benthamiana as a transient expression platform for the functional analysis of insect effectors and resistance genes from other plant species. Similarly, the absence of acylsugars in asat2 mutants will enable analysis of acylsugar biosynthesis genes from other Solanaceae by transient expression

Manipulation of Plant Defense Responses by the Tomato Psyllid (Bactericerca cockerelli) and Its Associated Endosymbiont Candidatus Liberibacter Psyllaurous

Some plant pathogens form obligate relationships with their insect vector and are vertically transmitted via eggs analogous to insect endosymbionts. Whether insect endosymbionts manipulate plant defenses to benefit their insect host remains unclear. The tomato psyllid, Bactericerca cockerelli (Sulc), vectors the endosymbiont “Candidatus Liberibacter psyllaurous” (Lps) during feeding on tomato (Solanum lycopersicum L.). Lps titer in psyllids varied relative to the psyllid developmental stage with younger psyllids harboring smaller Lps populations compared to older psyllids. In the present study, feeding by different life stages of B. cockerelli infected with Lps, resulted in distinct tomato transcript profiles. Feeding by young psyllid nymphs, with lower Lps levels, induced tomato genes regulated by jasmonic acid (JA) and salicylic acid (SA) (Allene oxide synthase, Proteinase inhibitor 2, Phenylalanine ammonia-lyase 5, Pathogenesis-related protein 1) compared to feeding by older nymphs and adults, where higher Lps titers were found. In addition, inoculation of Lps without insect hosts suppressed accumulation of these defense transcripts. Collectively, these data suggest that the endosymbiont-like pathogen Lps manipulates plant signaling and defensive responses to benefit themselves and the success of their obligate insect vector on their host plant

Impacts of climate change on herbivore induced plant signaling and defenses

The accumulation of CO2 and O3 in the troposphere alters phytochemistry which in turn influences the interactions between plants and insects. To examine the effect of elevated atmospheric CO2 and O3 concentrations on plant-insect interaction, I measured changes in transcription using microarray analysis of field-grown soybean (Glycine max). I found that the number of transcripts in the leaves affected by Japanese beetle (JB; Popillia japonica) herbivory was greater when plants were grown under elevated CO2, O3 and the combination of both compared to ambient atmosphere. The effect of herbivory on transcription diminished strongly with time, and elevated CO2 interacted more strongly with herbivory than did elevated O3 in my study. Constitutive levels and the induction by herbivory of key transcripts associated with defense and hormone signaling were down-regulated under elevated CO2, suggesting susceptibility may be altered. To examine the impact of elevated CO2 exposure on susceptibility to herbivory in soybeans in more detail, the magnitude and timing of transcripts related to three major hormone signaling pathways (jasmonic acid [JA], salicylic acid [SA], ethylene [ET]) and related defenses were examined in field environments under elevated CO2 after JB feeding. In addition, JB preference between elevated and ambient-grown tissue was determined. Elevated CO2 decreased the induction of JA and ET related transcripts (lox7, aos, hpl and acc1), resulting in decreased accumulation of defenses (polyphenol oxidase, protease inhibitors) over time compared to ambient-grown plants. Elevated CO2-grown tissue was preferred by JB in choice experiments. Elevated CO2 also increased the accumulation of SA in soybeans. SA and JA are known to have an antagonistic relationship in other plants, and this antagonism may explain the reduction in JA related transcripts. These results suggest elevated CO2 exposure could cause increases in insect damage and reduction in diseases caused by pathogen sensitive to the SA defense pathway in the future. In addition to elevated CO2, models predict that plants will also experience increased drought in the future, possibly altering plant-insect dynamics in unanticipated ways. To investigate the combined effects of drought and elevated CO2 on plant-insect interactions, components of susceptibility and palatability in soybeans were examined under field conditions. The effect of elevated CO2 exposure on phytohormone signaling was consistent with previous studies. Exposure to mild drought stimulated the induction of the JA/ET signaling pathways but had no impact on nutritional components. However, elevated CO2 exposure in combination with drought amplified the induction of JA and ET signaling transcripts and the accumulation of related defenses in soybeans after beetle herbivory. Overall, in combination with drought exposure, increased susceptibility of soybean to herbivores resulting from elevated CO2 exposure was removed. This study suggests soybean in areas experiencing elevated drought will have an advantage over well-watered plants grown under elevated CO2. It is not known if the impact of elevated CO2 on phytohormones and induced defenses is a generalized response in soybean or if it varies across plant species. In an attempt to address these questions, phytohormone signaling was examined under ambient and elevated CO2 concentrations across six soybean cultivars and six different plant species using a common protocol across all experiments to aid in comparison. Elevated CO2 reduced constitutive levels of JA in some but not all soybean cultivars; there was extensive variation in the response. Unexpectedly, constitutive and induced ET signaling increased in some soybean cultivars. In contrast to the variation seen in JA and ET, constitutive levels of SA were elevated universally across soybean cultivars grown under elevated CO2 with little variation in the response. Across species examined, elevated CO2 had a similar impact as with soybean cultivars, generally reducing constitutive JA signaling transcripts in most species examined. However, in contrast to soybean there was no impact of elevated CO2 on levels of SA across species. This study suggests some pathways may experience generalized changes for a species with little variation (e.g. SA in soybean), while others may not (JA/ET) and interactions with herbivores can change the response (constitutive versus induced). Thus, the modulation of hormone signaling by elevated CO2 may cause increases in chewing insect damage and reduction in pathogen infections sensitive to the SA defense pathway in the future. However, the interactions between different aspects of global change with elevated CO2 may alter the response, playing a more important role in determining plant-insect interactions than previously hypothesized. In conclusion, the impact of elevated CO2 on phytohormone signaling appears complex, dependent on interactions, individual signaling pathways, cultivars and species examined

Vector-Borne Bacterial Plant Pathogens: Interactions with Hemipteran Insects and Plants

Hemipteran insects are devastating pests of crops due to their wide host range, rapid reproduction, and ability to transmit numerous plant-infecting pathogens as vectors. While the field of plant-virus-vector interactions has flourished in recent years, plant-bacteria-vector interactions remain poorly understood. Leafhoppers and psyllids are by far the most important vectors of bacterial pathogens, yet there are still significant gaps in our understanding of their feeding behavior, salivary secretions, and plant responses as compared to important viral vectors, such as whiteflies and aphids. Even with an incomplete understanding of plant-bacteria-vector interactions, some common themes have emerged: 1) all known vector-borne bacteria share the ability to propagate in the plant and insect host; 2) particular hemipteran families appear to be incapable of transmitting vector-borne bacteria; 3) all known vector-borne bacteria have highly reduced genomes and coding capacity, resulting in host-dependence; and 4) vector-borne bacteria encode proteins that are essential for colonization of specific hosts, though only a few types of proteins have been investigated. Here, we review the current knowledge on important vector-borne bacterial pathogens, including Xylella fastidiosa, Spiroplasma spp., Liberibacter spp., and 'Candidatus Phytoplasma spp.’. We then highlight recent approaches used in the study of vector-borne bacteria. Finally, we discuss the application of this knowledge for control and future directions that will need to be addressed in the field of vector-plant-bacteria interactions

XAP5 CIRCADIAN TIMEKEEPER Affects Both DNA Damage Responses and Immune Signaling in Arabidopsis

Numerous links have been reported between immune response and DNA damage repair pathways in both plants and animals but the precise nature of the relationship between these fundamental processes is not entirely clear. Here, we report that XAP5 CIRCADIAN TIMEKEEPER (XCT), a protein highly conserved across eukaryotes, acts as a negative regulator of immunity in Arabidopsis thaliana and plays a positive role in responses to DNA damaging radiation. We find xct mutants have enhanced resistance to infection by a virulent bacterial pathogen, Pseudomonas syringae pv. tomato DC3000, and are hyper-responsive to the defense-activating hormone salicylic acid (SA) when compared to wild-type. Unlike most mutants with constitutive effector-triggered immunity (ETI), xct plants do not have increased levels of SA and retain enhanced immunity at elevated temperatures. Genetic analysis indicates XCT acts independently of NONEXPRESSOR OF PATHOGENESIS RELATED GENES1 (NPR1), which encodes a known SA receptor. Since DNA damage has been reported to potentiate immune responses, we next investigated the DNA damage response in our mutants. We found xct seedlings to be hypersensitive to UV-C and γ radiation and deficient in phosphorylation of the histone variant H2A.X, one of the earliest known responses to DNA damage. These data demonstrate that loss of XCT causes a defect in an early step of the DNA damage response pathway. Together, our data suggest that alterations in DNA damage response pathways may underlie the enhanced immunity seen in xct mutants

Manipulation of plant defense responses by the tomato psyllid (Bactericerca cockerelli) and its associated endosymbiont Candidatus Liberibacter psyllaurous.

Some plant pathogens form obligate relationships with their insect vector and are vertically transmitted via eggs analogous to insect endosymbionts. Whether insect endosymbionts manipulate plant defenses to benefit their insect host remains unclear. The tomato psyllid, Bactericerca cockerelli (Sulc), vectors the endosymbiont "Candidatus Liberibacter psyllaurous" (Lps) during feeding on tomato (Solanum lycopersicum L.). Lps titer in psyllids varied relative to the psyllid developmental stage with younger psyllids harboring smaller Lps populations compared to older psyllids. In the present study, feeding by different life stages of B. cockerelli infected with Lps, resulted in distinct tomato transcript profiles. Feeding by young psyllid nymphs, with lower Lps levels, induced tomato genes regulated by jasmonic acid (JA) and salicylic acid (SA) (Allene oxide synthase, Proteinase inhibitor 2, Phenylalanine ammonia-lyase 5, Pathogenesis-related protein 1) compared to feeding by older nymphs and adults, where higher Lps titers were found. In addition, inoculation of Lps without insect hosts suppressed accumulation of these defense transcripts. Collectively, these data suggest that the endosymbiont-like pathogen Lps manipulates plant signaling and defensive responses to benefit themselves and the success of their obligate insect vector on their host plant

Reciprocal plant‐mediated interactions between a virus and a non‐vector herbivore

Vector‐borne viruses alter many physical and chemical traits of their plant hosts, indirectly affecting the fitness and behavior of vectors in ways that promote virus transmission. However, it is unclear whether viruses induce plant‐mediated shifts in the behavior and fitness of non‐vector herbivores, or if non‐vectors affect the dynamics of vector‐borne viruses. Here we evaluated reciprocal interactions between Pea enation mosaic virus (PEMV), a pathogen transmitted by the aphid Acrythosiphon pisum, and a non‐vector weevil, Sitona lineatus. In the field, PEMV‐infected plants experienced more defoliation from S. lineatus than uninfected plants; behavioral assays similarly showed S. lineatus adults preferred to feed on infected plants. In turn, infectious A. pisum preferred plants damaged by S. lineatus, and S. lineatus herbivory led to increased PEMV titer. These interactions may be mediated by plant phytohormone levels, as S. lineatus induced jasmonic acid, while PEMV induced salicylic acid. Levels of abscisic acid were not affected by attack from either PEMV or S. lineatus alone, but plants challenged by both had elevated levels of this phytohormone. As plant viruses and their vectors often exist in diverse communities, our study highlights the importance of non‐vector species in influencing plant pathogens and their vectors through host‐mediated effects