Joe Louis

A protein from the salivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant

In feeding, aphids inject saliva into plant tissues, gaining access to phloem sap and eliciting (and sometimes overcoming) plant responses. We are examining the involvement, in this aphid–plant interaction, of individual aphid proteins and enzymes, as identified in a salivary gland cDNA library. Here, we focus on a salivary protein we have arbitrarily designated Protein C002. We have shown, by using RNAi-based transcript knockdown, that this protein is important in the survival of the pea aphid (Acyrthosiphon pisum) on fava bean, a host plant. Here, we further characterize the protein, its transcript, and its gene, and we study the feeding process of knockdown aphids. The encoded protein fails to match any protein outside of the family Aphididae. By using in situ hybridization and immunohistochemistry, the transcript and the protein were localized to a subset of secretory cells in principal salivary glands. Protein C002, whose sequence contains an N-terminal secretion signal, is injected into the host plant during aphid feeding. By using the electrical penetration graph method on c002-knockdown aphids, we find that the knockdown affects several aspects of foraging and feeding, with the result that the c002-knockdown aphids spend very little time in contact with phloem sap in sieve elements. Thus, we infer that Protein C002 is crucial in the feeding of the pea aphid on fava bean.

Feeding Behavior by the Soybean Aphid (Hemiptera: Aphididae) on Resistant and Susceptible Soybean Genotypes

Abstract The soybean aphid,Aphis glycines Matsumura (Hemiptera: Aphididae), is a major pest of soybean,Glycine max (L.) Merr. Since 2000, whenA.glycines was detected in the United States, several studies on this insect have been done in different areas, but there is no report of any studies of stylet penetration behavior byA.glycines on resistant and susceptible soybean. Assessment of feeding behavior of this aphid species was compared on four resistant entries (K1639, Pioneer® 95B97, Dowling, and Jackson) and a susceptible check (KS4202) by using the electrical penetration graph (EPG) technique. Feeding behavior ofA.glycines adults was recorded during a 9-h period. The average time needed to reach the first sieve element phase byA.glycines was 3.5 h in KS4202, whereas it was 7.5 h in the resistant entries. The total duration in the sieve element phase was longer than an hour in KS4202, and only 2 to 7 min in the resistant entries. These results suggest that morphological or chemical factors in the phloem tissue of resistant plants affect stylet penetration activities ofA.glycines. In the majority of the recordings, however, the aphid stylet reached the xylem phase before penetrating the sieve element, and the time that aphids spent ingesting xylem sap was not different among all entries. Therefore, it is possible that xylem sap in the resistant entries may contain toxic substances that change aphid behavior and that affect further activities in the sieve element phase.

Arabidopsis thaliana—Myzus persicae interaction: shaping the understanding of plant defense against phloem-feeding aphids

The phloem provides a unique niche for several organisms. Aphids are a large group of Hemipteran insects that utilize stylets present in their mouthparts to pierce sieve elements and drink large volumes of phloem sap. In addition, many aphids also vector viral diseases. Myzus persicae, commonly known as the green peach aphid (GPA), is an important pest of a large variety of plants that includes Arabidopsis thaliana. This review summarizes recent studies that have exploited the compatible interaction between Arabidopsis and GPA to understand the molecular and physiological mechanisms utilized by plants to control aphid infestation, as well as genes and mechanisms that contribute to susceptibility. In addition, recent efforts to identify aphid-delivered elicitors of plant defenses and novel aphid salivary components that facilitate infestation are also discussed.

Discrimination of Arabidopsis PAD4 Activities in Defense against Green Peach Aphid and Pathogens

The Arabidopsis (Arabidopsis thaliana) lipase-like protein PHYTOALEXIN DEFICIENT4 (PAD4) is essential for defense against green peach aphid (GPA; Myzus persicae) and the pathogens Pseudomonas syringae and Hyaloperonospora arabidopsidis. In basal resistance to virulent strains of P. syringae and H. arabidopsidis, PAD4 functions together with its interacting partner ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1) to promote salicylic acid (SA)-dependent and SA-independent defenses. By contrast, dissociated forms of PAD4 and EDS1 signal effector-triggered immunity to avirulent strains of these pathogens. PAD4-controlled defense against GPA requires neither EDS1 nor SA. Here, we show that resistance to GPA is unaltered in an eds1 salicylic acid induction deficient2 (sid2) double mutant, indicating that redundancy between EDS1 and SID2-dependent SA, previously reported for effector-triggered immunity conditioned by certain nucleotide-binding-leucine-rich repeat receptors, does not explain the dispensability of EDS1 and SID2 in defense against GPA. Mutation of a conserved serine (S118) in the predicted lipase catalytic triad of PAD4 abolished PAD4-conditioned antibiosis and deterrence against GPA feeding, but S118 was dispensable for deterring GPA settling and promoting senescence in GPA-infested plants as well as for pathogen resistance. These results highlight distinct molecular activities of PAD4 determining particular aspects of defense against aphids and pathogens.

Host‐specific salivary elicitor(s) of European corn borer induce defenses in tomato and maize

Plants turn on induced defenses upon insect herbivory. In the current study, we evaluated the role of European corn borer (ECB) elicitors (molecules secreted by herbivores) that either induce/suppress defenses in Solanum lycopersicum (tomato) and Zea mays (maize), two very important crop plants that are grown for food and/or fuel throughout the world. We used a combination of molecular, biochemical, confocal and scanning electron microscopy, caterpillar spinneret ablation/cauterization, and conventional insect bioassay methods to determine the role of ECB elicitors in modulating defenses in both tomato and maize crop plants. Our results clearly demonstrate that the components present in the ECB saliva induce defense-related proteinase inhibitors in both tomato (PIN2) and maize (MPI). Presence of glucose oxidase in the ECB saliva induced defenses in tomato, but not in maize. However, ECB saliva induced genes present in the jasmonic acid biosynthesis pathway in both tomato and maize. Although ECB saliva can induce defenses in both tomato and maize, our results suggest that host-specific salivary components are responsible for inducing host plant defenses. Proteomic analysis of ECB salivary elicitors and plant receptors/signaling mechanisms involved in recognizing different ECB elicitors remains to be determined.

PAD4-dependent antibiosis contributes to the ssi2-conferred hyper-resistance to the green peach aphid.

Myzus persicae, commonly known as green peach aphid (GPA), is a sap-sucking insect with a broad host range. Arabidopsis thaliana responds to GPA infestation with elevated expression of the PHYTOALEXIN DEFICIENT4 (PAD4) gene. Previously, we had demonstrated that the loss of PAD4 gene function compromises Arabidopsis resistance to GPA. In contrast, a mutation in the Arabidopsis SUPPRESSOR OF SALICYLIC ACID INSENSITIVITY2 (SSI2) gene, which encodes a desaturase involved in lipid metabolism, resulted in hyper-resistance to GPA. We demonstrate here that PAD4 is required for the ssi2-dependent heightened resistance to GPA. Based on electrical monitoring of insect behavior and bioassays in which the insect was given a choice between the wild type and the ssi2 mutant, it is concluded that the ssi2-conferred resistance is not due to deterrence of insect settling or feeding from the phloem of the mutant. Instead, hyper-resistance in the ssi2 mutant results from heightened antibiosis that curtails insect reproduction. Petiole exudates collected from uninfested ssi2 plants contain elevated levels of an activity that interferes with aphid reproduction in synthetic diets. PAD4 was required for the accumulation of this antibiotic activity in petiole exudates, supporting the role of PAD4 in phloem-based resistance. Because PAD4 expression is not elevated in the ssi2 mutant, we suggest that basal PAD4 expression contributes to this antibiosis.

Arabidopsis thaliana—Aphid Interaction

Aphids are important pests of plants that use their stylets to tap into the sieve elements to consume phloem sap. Besides the removal of photosynthates, aphid infestation also alters source-sink patterns. Most aphids also vector viral diseases. In this chapter, we will summarize on recent significant findings in plant-aphid interaction, and how studies involving Arabidopsis thaliana and Myzus persicae (Sülzer), more commonly known as the green peach aphid (GPA), are beginning to provide important insights into the molecular basis of plant defense and susceptibility to aphids. The recent demonstration that expression of dsRNA in Arabidopsis can be used to silence expression of genes in GPA has further expanded the utility of Arabidopsis for evaluating the contribution of the aphid genome-encoded proteins to this interaction.

Ethylene Contributes to maize insect resistance1-Mediated Maize Defense against the Phloem Sap-Sucking Corn Leaf Aphid

An endogenous defensive protein in maize that encodes a Cys protease, provides enhanced resistance to phloem sap-consuming pests through the action of an ethylene-signaling pathway. Signaling networks among multiple phytohormones fine-tune plant defense responses to insect herbivore attack. Previously, it was reported that the synergistic combination of ethylene (ET) and jasmonic acid (JA) was required for accumulation of the maize insect resistance1 (mir1) gene product, a cysteine (Cys) proteinase that is a key defensive protein against chewing insect pests in maize (Zea mays). However, this study suggests that mir1-mediated resistance to corn leaf aphid (CLA; Rhopalosiphum maidis), a phloem sap-sucking insect pest, is independent of JA but regulated by the ET-signaling pathway. Feeding by CLA triggers the rapid accumulation of mir1 transcripts in the resistant maize genotype, Mp708. Furthermore, Mp708 provided elevated levels of antibiosis (limits aphid population)- and antixenosis (deters aphid settling)-mediated resistance to CLA compared with B73 and Tx601 maize susceptible inbred lines. Synthetic diet aphid feeding trial bioassays with recombinant Mir1-Cys Protease demonstrates that Mir1-Cys Protease provides direct toxicity to CLA. Furthermore, foliar feeding by CLA rapidly sends defensive signal(s) to the roots that trigger belowground accumulation of the mir1, signifying a potential role of long-distance signaling in maize defense against the phloem-feeding insects. Collectively, our data indicate that ET-regulated mir1 transcript accumulation, uncoupled from JA, contributed to heightened resistance to CLA in maize. In addition, our results underscore the significance of ET acting as a central node in regulating mir1 expression to different feeding guilds of insect herbivores.

Ethylene contributes to mir1-mediated maize defense against the phloem-sap sucking insect Rhopalosiphum maidis

An endogenous defensive protein in maize that encodes a Cys protease, provides enhanced resistance to phloem sap-consuming pests through the action of an ethylene-signaling pathway. Signaling networks among multiple phytohormones fine-tune plant defense responses to insect herbivore attack. Previously, it was reported that the synergistic combination of ethylene (ET) and jasmonic acid (JA) was required for accumulation of the maize insect resistance1 (mir1) gene product, a cysteine (Cys) proteinase that is a key defensive protein against chewing insect pests in maize (Zea mays). However, this study suggests that mir1-mediated resistance to corn leaf aphid (CLA; Rhopalosiphum maidis), a phloem sap-sucking insect pest, is independent of JA but regulated by the ET-signaling pathway. Feeding by CLA triggers the rapid accumulation of mir1 transcripts in the resistant maize genotype, Mp708. Furthermore, Mp708 provided elevated levels of antibiosis (limits aphid population)- and antixenosis (deters aphid settling)-mediated resistance to CLA compared with B73 and Tx601 maize susceptible inbred lines. Synthetic diet aphid feeding trial bioassays with recombinant Mir1-Cys Protease demonstrates that Mir1-Cys Protease provides direct toxicity to CLA. Furthermore, foliar feeding by CLA rapidly sends defensive signal(s) to the roots that trigger belowground accumulation of the mir1, signifying a potential role of long-distance signaling in maize defense against the phloem-feeding insects. Collectively, our data indicate that ET-regulated mir1 transcript accumulation, uncoupled from JA, contributed to heightened resistance to CLA in maize. In addition, our results underscore the significance of ET acting as a central node in regulating mir1 expression to different feeding guilds of insect herbivores.

Plant defence against aphids: the PAD4 signalling nexus

In Arabidopsis thaliana, PHYTOALEXIN DEFICIENT 4 (PAD4) functions as a key player in modulating defence against the phloem sap-feeding aphid Myzus persicae (Sülzer), more commonly known as the green peach aphid (GPA), an important pest of a wide variety of plants. PAD4 controls antibiosis and antixenosis against the GPA. In addition, PAD4 deters aphid feeding from sieve elements on Arabidopsis. In the past few years, substantial progress has been made in dissecting the role of PAD4 and its interaction with other signalling components in limiting aphid infestation. Several key genes/mechanisms involved in providing aphid resistance/susceptibility in Arabidopsis regulate the aphid infestation-stimulated expression of PAD4. Together, PAD4 and its interacting signalling partners provide a critical barrier to curtail GPA colonization of Arabidopsis.