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Combining plant resistance against virus and vector presents an attractive approach to reduce virus transmission and virus proliferation in crops. Restricted Tobacco-etch virus Movement (RTM) genes confer resistance to potyviruses by limiting their long-distance transport. Recently, a close homologue of one of the RTM genes, SLI1, has been discovered but this gene instead confers resistance to Myzus persicae aphids, a vector of potyviruses. The functional connection between resistance to potyviruses and aphids, raises the question whether plants have a basic defense system in the phloem against biotic intruders. This paper provides an overview on restricted potyvirus phloem transport and restricted aphid phloem feeding and their possible interplay, followed by a discussion on various ways in which viruses and aphids gain access to the phloem sap. From a phloem-biological perspective, hypotheses are proposed on the underlying mechanisms of RTM- and SLI1-mediated resistance, and their possible efficacy to defend against systemic viruses and phloem-feeding vectors.

Background Phloem is the long-distance transport tissue of vascular plants in which photoassimilates are distributed from sources (e.g., leaves) to sinks (e.g., roots, fruits). Phloem transport occurs under pressure, making it very sensitive to manipulation and almost experimentally inaccessible. Therefore, functional data on phloem speed and dynamic distribution of photoassimilates along the transport pathway are still scarce, both in trees and herbaceous plants. This study presents a methodological pipeline to image phloem transport in very thin shoots of the model plant Arabidopsis using photosynthetic uptake of 11 CO 2 and state-of-the-art positron emission tomography (PET). Results Successful application of the latest generation preclinical PET scanners allowed in vivo visualization of internal movement of 11 C-labelled photoassimilates inside primary and secondary shoots of 1 to 2 mm diameter every 5 min. Using this data as input in a compartmental model enabled estimation of (i) phloem front speed, and (ii) radial carbon partitioning between leakage-retrieval phloem, carbon storage and respiratory efflux. The methodology shows that the phloem front speed of recently fixed carbon in primary shoots was almost two-fold the speed in secondary shoots (128 vs. 70 µm s −1 ). Furthermore, it was estimated that the fraction of recently fixed 11 CO 2 that was unloaded from the phloem to the surrounding storage cells and retrieved back into the phloem was higher in primary shoots than in secondary shoots, and that allocation to the storage compartment was higher in secondary shoots. Within the primary shoot, the fraction of unloading and retrieval of the 11 C-labelled photosynthates increased towards the inflorescence. Conclusion Here, we demonstrate the synergistic application of high-resolution PET scanning and compartmental modelling as a promising approach to advance our understanding of phloem dynamics in small-dimension plants, such as the model plant Arabidopsis. With this, an opportunity is created to explore the genetic basis of phloem dynamics.

Genes involved in plant defences against herbivores and pathogens are often highly polymorphic. This is a putative sign that balancing selection may have operated reciprocally on the hosts and their herbivores. Spatial and temporal variations (for example, in soil nutrients and the plants' ontogenetic development) may also modulate resistance traits, and thus selection pressures, but have been largely overlooked in theories of plant defences. Important elements of defences in Populus tremula (hereafter aspen) are phenolic compounds, including condensed tannins (CTs). Concentrations of CTs vary considerably with both variations in external factors and time, but they are also believed to provide genotype‐dependent resistance, mainly against chewing herbivores and pathogens. However, evidence of their contributions to resistance is sparse. Detailed studies of co‐evolved plant–herbivore associations could provide valuable insights into these contributions. Therefore, we examined correlations between CT levels in aspen leaves and both the feeding behavior and reproduction of the specialist aspen leaf aphid (Chaitophorus tremulae) in varied conditions. We found that xylem sap intake and probing difficulties were higher on genotypes with high‐CT concentrations. However, aphids engaged in more nonprobing activities on low‐CT genotypes, indicating that CTs were not the only defence traits involved. Thus, high‐CT genotypes were not necessarily more resistant than low‐CT genotypes, but aphid reproduction was generally negatively correlated with local CT accumulation. Genotype‐specific resistance ranking also depended on the experimental conditions. These results support the hypothesis that growth conditions may affect selection pressures mediated by aphids in accordance with balancing selection theory. The contributions of condensed tannins (CTs) to aspen resistance provided clear indications of complex interactions between host genotype and both environmental and ontogenetic factors. Induced foliar CT levels correlated negatively with aphid reproduction, and aphids on high‐CT genotypes spent more time on probing and xylem feeding and they more frequently showed signs of penetration difficulties. However, genotype‐resistance rankings depended on both plant age and growth conditions.

Defence priming by organismal and non-organismal stimulants can reduce effects of biotic stress in plants. Thus, it could help efforts to enhance the sustainability of agricultural production by reducing use of agrochemicals in protection of crops from pests and diseases. We have explored effects of applying this approach to both Arabidopsis plants and seeds of various crops in meta-analyses. The results show that its effects on Arabidopsis plants depend on both the priming agent and antagonist. Fungi and vitamins can have strong priming effects, and priming is usually more effective against bacterial pathogens than against herbivores. Moreover, application of bio-stimulants (particularly vitamins and plant defence elicitors) to seeds can have promising defence priming effects. However, the published evidence is scattered, does not include Arabidopsis, and additional studies are required before we can draw general conclusions and understand the molecular mechanisms involved in priming of seeds’ defences. In conclusion, defence priming of plants has clear potential and application of bio-stimulants to seeds may protect plants from an early age, promises to be both labour- and resource-efficient, poses very little environmental risk, and is thus both economically and ecologically promising.

Aphids induce many transcriptional perturbations in their host plants, but the signalling cascades responsible and the effects on plant resistance are largely unknown. Through a genome-wide association (GWA) mapping study in Arabidopsis thaliana, we identified WRKY22 as a candidate gene associated with feeding behaviour of the green peach aphid, Myzus persicae. The transcription factor WRKY22 is known to be involved in pathogen-triggered immunity, and WRKY22 gene expression has been shown to be induced by aphids. Assessment of aphid population development and feeding behaviour on knockout mutants and overexpression lines showed that WRKY22 increases susceptibility to M. persicae via a mesophyll-located mechanism. mRNA sequencing analysis of aphid-infested wrky22 knockout plants revealed the up-regulation of genes involved in salicylic acid (SA) signalling and down-regulation of genes involved in plant growth and cell-wall loosening. In addition, mechanostimulation of knockout plants by clip cages up-regulated jasmonic acid (JA)-responsive genes, resulting in substantial negative JA–SA crosstalk. Based on this and previous studies, WRKY22 is considered to modulate the interplay between the SA and JA pathways in response to a wide range of biotic and abiotic stimuli. Its induction by aphids and its role in suppressing SA and JA signalling make WRKY22 a potential target for aphids to manipulate host plant defences.

The plant cell wall plays an important role in damage-associated molecular pattern-induced resistance to pathogens and herbivorous insects. Our current understanding of cell wall-mediated resistance is largely based on the degree of pectin methylesterification. However, little is known about the role of pectin acetylesterification in plant immunity. This study describes how one pectin-modifying enzyme, PECTIN ACETYLESTERASE 9 (PAE9), affects the Arabidopsis (Arabidopsis thaliana) transcriptome, secondary metabolome, and aphid performance. Electro-penetration graphs showed that Myzus persicae aphids established phloem feeding earlier on pae9 mutants. Whole-genome transcriptome analysis revealed a set of 56 differentially expressed genes (DEGs) between uninfested pae9-2 mutants and wild-type plants. The majority of the DEGs were enriched for biotic stress responses and down-regulated in the pae9-2 mutant, including PAD3 and IGMT2, involved in camalexin and indole glucosinolate biosynthesis, respectively. Relative quantification of more than 100 secondary metabolites revealed decreased levels of several compounds, including camalexin and oxylipins, in two independent pae9 mutants. In addition, absolute quantification of phytohormones showed that jasmonic acid (JA), jasmonoyl-Ile, salicylic acid, abscisic acid, and indole-3-acetic acid were compromised due to PAE9 loss of function. After aphid infestation, however, pae9 mutants increased their levels of camalexin, glucosinolates, and JA, and no long-term effects were observed on aphid fitness. Overall, these data show that PAE9 is required for constitutive up-regulation of defense-related compounds, but that it is not required for aphid-induced defenses. The signatures of phenolic antioxidants, phytoprostanes, and oxidative stress-related transcripts indicate that the processes underlying PAE9 activity involve oxidation-reduction reactions.

Background Piercing-sucking insects cause severe damage in crops. Breeding for host-plant resistance can significantly reduce the yield losses caused by these insects, but host-plant resistance is a complex trait that is difficult to phenotype quickly and reliably. Current phenotyping methods mainly focus on labor-intensive and time-consuming end-point measurements of plant fitness. Characterizing insect behavior as a proxy for host-plant resistance could be a promising time-saving alternative to end-point measurements. Results We present a phenotyping platform that allows screening for host-plant resistance against Western flower thrips (WFT, Frankliniella occidentalis (Pergande)) in a parallel two-choice setup using automated video tracking of thrips behavior. The platform was used to establish host-plant preference of WFT with a large plant population of 345 wild Arabidopsis accessions and the method was optimized with two extreme accessions from this population that differed in resistance towards WFT. To this end, the behavior of 88 WFT individuals was simultaneously tracked in 88 parallel two-choice arenas during 8 h. Host-plant preference of WFT was established both by the time thrips spent on either accession and various behavioral parameters related to movement (searching) and non-movement (feeding) events. Conclusion In comparison to 6-day end-point choice assays with whole plants or detached leaves, the automated video-tracking choice assay developed here delivered similar results, but with higher time- and resource efficiency. This method can therefore be a reliable and effective high throughput phenotyping tool to assess host-plant resistance to thrips in large plant populations.

Plants are exposed to combinations of various biotic and abiotic stresses, but stress responses are usually investigated for single stresses only. Here, we investigated the genetic architecture underlying plant responses to 11 single stresses and several of their combinations by phenotyping 350 Arabidopsis thaliana accessions. A set of 214 000 single nucleotide polymorphisms (SNPs) was screened for marker-trait associations in genome-wide association (GWA) analyses using tailored multi-trait mixed models. Stress responses that share phytohormonal signaling pathways also share genetic architecture underlying these responses. After removing the effects of general robustness, for the 30 most significant SNPs, average quantitative trait locus (QTL) effect sizes were larger for dual stresses than for single stresses. Plants appear to deploy broad-spectrum defensive mechanisms influencing multiple traits in response to combined stresses. Association analyses identified QTLs with contrasting and with similar responses to biotic vs abiotic stresses, and below-ground vs above-ground stresses. Our approach allowed for an unprecedented comprehensive genetic analysis of how plants deal with a wide spectrum of stress conditions.

Prey sharing in predatory mammals and birds has been shown to reduce fights for food between predators, increase predation efficacy, and safeguard food availability by reciprocal sharing, providing immediate and delayed benefits for the sharers. However, little is known about the incidence of prey sharing in arthropods and the implications for biological control have been mostly overlooked. In this study, the feeding behavior of two aphid predators, Micromus angulatus and Chrysoperla carnea , was investigated to assess the incidence of prey sharing and its possible consequences for biological control of aphids. A video-recording setup was used to investigate the feeding behavior of the predators at various predator/prey ratios. Different numbers of predatory larvae were placed into arenas containing five Myzus persicae subsp. nicotianae . The behavior of the predators was recorded for four hours and the number of prey killed was scored. Our results indicate that prey sharing is a density-dependent behavior, increasing at higher predator/prey ratios. Larvae of M. angulatus performed prey sharing seven times more often than C. carnea and accepted higher numbers of predators sharing a single aphid. Interestingly, a positive correlation between the number of prey-sharing events and the number of aphids killed by the predators was found, suggesting that prey sharing could increase the kill rate of the predators. Additionally, the presence of conspecific larvae enhanced the predation success of M. angulatus . Our findings indicate that prey sharing is an adaptive behavior that could improve the foraging efficacy and kill rate of arthropod predators.

The role of phloem proteins in plant resistance to aphids is still largely elusive. By genome-wide association mapping of aphid behavior on 350 natural Arabidopsis thaliana accessions, we identified the small heat shock-like SIEVE ELEMENT-LINING CHAPERONE1 (SLI1). Detailed behavioral studies on near-isogenic and knockout lines showed that SLI1 impairs phloem feeding. Depending on the haplotype, aphids displayed a different duration of salivation in the phloem. On sli1 mutants, aphids prolonged their feeding sessions and ingested phloem at a higher rate than on wild-type plants. The largest phenotypic effects were observed at 26°C, when SLI1 expression is upregulated. At this moderately high temperature, sli1 mutants suffered from retarded elongation of the inflorescence and impaired silique development. Fluorescent reporter fusions showed that SLI1 is confined to the margins of sieve elements where it lines the parietal layer and colocalizes in spherical bodies around mitochondria. This localization pattern is reminiscent of the clamp-like structures observed in previous ultrastructural studies of the phloem and shows that the parietal phloem layer plays an important role in plant resistance to aphids and heat stress.