Phytohormonal signaling in plant responses to aphid feeding

Aphid feeding induces various defense signaling mechanisms in plants. The recognition of feeding activities by plants occurs through the use of transmembrane pattern recognition receptors (PRRS) or, acting largely inside the cell, polymorphic nucleotide-binding leucine-rich-repeat (NB-LRR) protein products, encoded by most R genes. Activation may induce defensive reactions which are the result of highly coordinated sequential changes at the cellular level comprising, among other changes, the synthesis of signaling molecules. The ensuing plant responses are followed by the transmission of defense response signal cascades. Signals are mediated by bioactive endogenous molecules, i.e. phytohormones, such as jasmonic acid (JA), salicylic acid (SA), ethylene (ET), abscisic acid (ABA), gibberellic acid (GA) and free radicals such as hydrogen peroxide (H₂O₂) and nitric oxide (NO) which independently provide direct chemical resistance. Plant-induced defenses are also regulated by a network of inter-connecting signaling pathways, in which JA, SA, and ET play dominant roles. Both synergistic and inhibitory aspects of the cross-talk among these pathways have been reported. This paper presents molecular mechanisms of plant response to aphid feeding, the precise activation of various endogenous bioactive molecules signaling in the response of many plant species and their participation in the regulation of numerous defense genes, which lead to a specific metabolic effect. Selected important points in signal transduction pathways were also discussed in studies on plant response to aphid feeding.     

The molecular bases of plant resistance and defense responses to aphid feeding: current status

Plant genes participating in the recognition of aphid herbivory in concert with plant genes involved in defense against herbivores mediate plant resistance to aphids. Several such genes involved in plant disease and nematode resistance have been characterized in detail, but their existence has only recently begun to be determined for arthropod resistance. Hundreds of different genes are typically involved and the disruption of plant cell wall tissues during aphid feeding has been shown to induce defense responses in Arabidopsis, Triticum, Sorghum, and Nicotiana species. Mi‐1.2, a tomato gene for resistance to the potato aphid, Macrosiphum euphorbiae (Thomas), is a member of the nucleotide‐binding site and leucine‐rich region Class II family of disease, nematode, and arthropod resistance genes. Recent studies into the differential expression of Pto‐ and Pti1‐like kinase genes in wheat plants resistant to the Russian wheat aphid, Diuraphis noxia (Mordvilko), provide evidence of the involvement of the Pto class of resistance genes in arthropod resistance. An analysis of available data suggests that aphid feeding may trigger multiple signaling pathways in plants. Early signaling includes gene‐for‐gene recognition and defense signaling in aphid‐resistant plants, and recognition of aphid‐inflicted cell damage in both resistant and susceptible plants. Furthermore, signaling is mediated by several compounds, including jasmonic acid, salicylic acid, ethylene, abscisic acid, giberellic acid, nitric oxide, and auxin. These signals lead to the development of direct chemical defenses against aphids and general stress‐related responses that are well characterized for a number of abiotic and biotic stresses. In spite of major plant taxonomic differences, similarities exist in the types of plant genes expressed in response to feeding by different species of aphids. However, numerous differences in plant signaling and defense responses unique to specific aphid–plant interactions have been identified and warrant further investigation.     

New perspectives on plant defense responses through modulation of developmental pathways

Invasion mechanisms of pathogens and counteracting defense mechanisms of plants are highly diverse and perpetually evolving. While most classical studies of plant defense have focused only on defense-specific factor-mediated responses, recent work is beginning to shed light on the involvement of non-stress signal components, especially growth and developmental processes. This shift in focus links plant resistance more closely with growth and development. In this review, we summarize our current understanding of how pathogens manipulate host developmental processes and, conversely, of how plants deploy their developmental processes for self-protection. We conclude by introducing our recent work on UNI, a novel R protein in Arabidopsis which mediates cross-talk between developmental processes and defense responses.     

Electroantennogram responses of aphid nymphs to plant volatiles

Abstract. Electroantennogram (EAG) responses of immature aphids were investigated for 30 plant volatile compounds in third‐ and fourth‐stadium nymphs of the black bean aphid, Aphis fabae. The nymphs were destined to develop into adult alate (winged) virginoparae. The EAG response profiles were similar to those previously reported in the adults. Among the compounds tested, hexanonitrile elicited the largest EAG responses in both nymphal stadia, corresponding to previously reported results with adults. Six‐carbon aliphatic compounds showed relatively higher EAG activities in the nymphs but, in contrast, (E)‐2‐hexenal, benzaldehyde, α‐pinene and β‐pinene, and citronellal elicited relatively smaller EAG responses in nymphs than adults. Although overall EAG response profiles were similar between the third and the fourth stadia for the majority of the volatiles, four aldehyde compounds, hexanal (E)‐2‐heptenal, 2‐hydroxybenzaldehyde and citronellal, showed relatively higher EAG activities in the third than in the fourth stadium. The present study indicates that aphid nymphs possess a functional olfactory receptor system before the antennae are fully developed morphologically and physiologically.     

Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana

Endophytic actinobacteria, isolated from healthy wheat tissue, which are capable of suppressing a number wheat fungal pathogens both in vitro and in planta, were investigated for the ability to activate key genes in the systemic acquired resistance (SAR) or the jasmonate/ethylene (JA/ET) pathways in Arabidopsis thaliana. Inoculation of A. thaliana (Col-0) with selected endophytic strains induced a low level of SAR and JA/ET gene expression, measured using quantitative polymerase chain reaction. Upon pathogen challenge, endophyte-treated plants demonstrated a higher abundance of defense gene expression compared with the non-endophyte-treated controls. Resistance to the bacterial pathogen Erwinia carotovora subsp. carotovora required the JA/ET pathway. On the other hand, resistance to the fungal pathogen Fusarium oxysporum involved primarily the SAR pathway. The endophytic actinobacteria appear to be able to "prime" both the SAR and JA/ET pathways, upregulating genes in either pathway depending on the infecting pathogen. Culture filtrates of the endophytic actinobacteria were investigated for the ability to also activate defense pathways. The culture filtrate of Micromonospora sp. strain EN43 grown in a minimal medium resulted in the induction of the SAR pathway; however, when grown in a complex medium, the JA/ET pathway was activated. Further analysis using Streptomyces sp. strain EN27 and defense-compromised mutants of A. thaliana indicated that resistance to E. carotovora subsp. carotovora occurred via an NPR1-independent pathway and required salicylic acid whereas the JA/ET signaling molecules were not essential. In contrast, resistance to F. oxysporum mediated by Streptomyces sp. strain EN27 occurred via an NPR1-dependent pathway but also required salicylic acid and was JA/ET independent.     

Molecular and ecological plant defense responses along an elevational gradient in a boreal ecosystem

Plants have the capacity to alter their phenotype in response to environmental factors, such as herbivory, a phenomenon called phenotypic plasticity. However, little is known on how plant responses to herbivory are modulated by environmental variation along ecological gradients. To investigate this question, we used bilberry (Vaccinium myrtillus L.) plants and an experimental treatment to induce plant defenses (i.e., application of methyl jasmonate; MeJA), to observe ecological responses and gene expression changes along an elevational gradient in a boreal system in western Norway. The gradient included optimal growing conditions for bilberry in this region (ca. 500 m a.s.l.), and the plant's range limits at high (ca. 900 m a.s.l.) and low (100 m a.s.l.) elevations. Across all altitudinal sites, MeJA‐treated plants allocated more resources to herbivory resistance while reducing growth and reproduction than control plants, but this response was more pronounced at the lowest elevation. High‐elevation plants growing under less herbivory pressure but more resource‐limiting conditions exhibited consistently high expression levels of defense genes in both MeJA‐treated and untreated plants at all times, suggesting a constant state of “alert.” These results suggest that plant defense responses at both the molecular and ecological levels are modulated by the combination of climate and herbivory pressure, such that plants under different environmental conditions differentially direct the resources available to specific antiherbivore strategies. Our findings are important for understanding the complex impact of future climate changes on plant–herbivore interactions, as this is a major driver of ecosystem functioning and biodiversity.     

Fractionated extracts of Russian wheat aphid eliciting defense responses in wheat

It is hypothesized that the interaction between aphids and plants follows a gene-for-gene model. The recent appearance of several new Russian wheat aphid, Diuraphis noxia (Kurdjumov) (Homoptera: Aphididae), biotypes in the United States and the differential response of wheat, Triticum aestivum L., genotypes containing different resistance genes also suggest a gene-for-gene interaction. However, aphid elicitors remain unknown. This study was conducted to identify fractionated Russian wheat aphid extracts capable of eliciting differential responses between resistant and susceptible wheat genotypes. We extracted whole soluble compounds and separated proteins and metabolites from two Russian wheat aphid biotypes (1 and 2), injected these extracts into seedlings of susceptible wheat Gamtoos (dn7) and resistant 94M370 (Dn7), and determined phenotypic and biochemical plant responses. Injections of whole extract or protein extract from both biotypes induced the typical susceptible symptom, leaf rolling, in the susceptible cultivar, but not in the resistant cultivar. Furthermore, multiple injections with protein extract from biotype 2 induced the development of chlorosis, head trapping, and stunting in susceptible wheat. Injection with metabolite, buffer, or chitin, did not produce any susceptible symptoms in either genotype. The protein extract from the two biotypes also induced significantly higher activities of three defense-response enzymes (catalase, peroxidase, and beta-glucanase) in 94M370 than in Gamtoos. These results indicate that a protein elicitor from the Russian wheat aphid is recognized by a plant receptor, and the recognition is mediated by the Dn7-gene product. The increased activities of defense-response enzymes in resistant plants after injection with the protein fraction suggest that defense response genes are induced after recognition of aphid elicitors by the plant.     

Genes controlling expression of defense responses in Arabidopsis.

In the past year, two regulatory defense-related genes, EDS1l and COl1, have been cloned. Several other genes with regulatory functions have been identified by mutation, including DND1, PAD4, CPR6, and SSl1. It has become clear that jasmonate signaling plays an important role in defense response signaling, and that the jasmonate and salicylic acid signaling pathways are interconnected.     

Redox responses of Arabidopsis thaliana to the green peach aphid,Myzus persicae

The green peach aphid (Myzus persicae) is a phloem-feeding insect that causes economic damage on a wide array of crops. Using a luminol-based assay, a superoxide-responsive reporter gene (Zat12::luciferase), and a probe specific to hydrogen peroxide (HyPer), we demonstrated that this aphid induces accumulation of reactive oxygen species (ROS) in Arabidopsis thaliana. Similar to the apoplastic oxidative burst induced by pathogens, this response to aphids was rapid and transient, with two peaks occurring within 1 and 4 hr after infestation. Aphid infestation also induced an oxidative response in the cytosol and peroxisomes, as measured using a redox-sensitive variant of green fluorescent protein (roGFP2). This intracellular response began within minutes of infestation but persisted 20 hr or more after inoculation, and the response of the peroxisomes appeared stronger than the response in the cytosol. Our results suggest that the oxidative response to aphids involves both apoplastic and intracellular sources of ROS, including ROS generation in the peroxisomes, and these different sources of ROS may potentially differ in their impacts on host suitability for aphids.     

Regulatory mechanisms of host plant defense responses to arbuscular mycorrhiza

Arbuscular mycorrhizal (AM) fungi colonize the roots of over 80% of terrestrial plant species, forming mutually beneficial symbioses. During the colonization process, symbiotic partners recognize each other, and undergo observable morphological and physiological changes; indicating that symbiosis formation involves multiple factors that are finely regulated. Sometimes host plants generate a transient, weak, defense response. This response and its down-regulation play a very important role in the development of AM symbioses. Although AM fungi can infect a wide range of host root tissues, which host defense may play a crucial role is hypothesized from the fact that hyphal expansion is only observed in the root cortex.
We discuss five defense mechanisms. (1) The degradation of exogenous elicitors. The host’s weak defense response may be due to the degradation of the exogenous elicitor chitin, or the prevention of release of an endogenous inductor from the plant cell wall. (2) The inactivation of defense signal molecules. Some defense signal molecules such as hydrogen peroxidase, salicylic acid (SA), and jasmonic acid (JA), are inactivated in host plants. This helps to avoid the turn-on of defense-related genes and facilitate mycorrhizal formation. (3) The regulation of plant hormones and plant photosynthates. Plant hormone levels and plant photosynthate metabolism both change during AM colonization. These mechanisms need further exploration. (4) Changes in levels of phosphorous (P), and (iso)flavonoids. High P levels can induce some defense genes to express hydrogen peroxidase, chitinase, and glucanase. These gene products can repress colonization by AM fungi. The plant defense response regulatory effect for different (iso)flavonoids varies, and their levels are regulated by P. (5) The suppressed expression of symbiotic genes. Some symbiosis-related genes inhibit plant defense responses, but it is still unclear which mechanisms underlie gene regulation. We provide here a theoretical basis for research into AM symbiosis that may promote study of host plant resistance and the mechanisms of symbiosis formation.
We provide a deeper insight into the signal transduction pathways of mycorrhization that will aid understanding and analysis of plant defense mechanisms in the AM context. The on-going development of genome sequencing technology will contribute greatly to the detailed study of symbiosis-related genes, and pathogenesis-related protein genes. These related genes may be induced to express corresponding proteins, be repressed, postpone expression or even shutdown, or both may work together to form symbioses. Elucidation of these features will help us understand the roles that plant defenses play in mycorrhizal formation; providing an unprecedented opportunity for research into mycorrhizal molecular biology and the interaction of symbiotic partners, and allowing the underlying mechanisms to be gradually uncovered.     

Regulatory mechanisms of host plant defense responses to arbuscular mycorrhiza

Arbuscular mycorrhizal (AM) fungi colonize the roots of over 80% of terrestrial plant species, forming mutually beneficial symbioses. During the colonization process, symbiotic partners recognize each other, and undergo observable morphological and physiological changes; indicating that symbiosis formation involves multiple factors that are finely regulated. Sometimes host plants generate a transient, weak, defense response. This response and its down-regulation play a very important role in the development of AM symbioses. Although AM fungi can infect a wide range of host root tissues, which host defense may play a crucial role is hypothesized from the fact that hyphal expansion is only observed in the root cortex.
We discuss five defense mechanisms. (1) The degradation of exogenous elicitors. The host’s weak defense response may be due to the degradation of the exogenous elicitor chitin, or the prevention of release of an endogenous inductor from the plant cell wall. (2) The inactivation of defense signal molecules. Some defense signal molecules such as hydrogen peroxidase, salicylic acid (SA), and jasmonic acid (JA), are inactivated in host plants. This helps to avoid the turn-on of defense-related genes and facilitate mycorrhizal formation. (3) The regulation of plant hormones and plant photosynthates. Plant hormone levels and plant photosynthate metabolism both change during AM colonization. These mechanisms need further exploration. (4) Changes in levels of phosphorous (P), and (iso)flavonoids. High P levels can induce some defense genes to express hydrogen peroxidase, chitinase, and glucanase. These gene products can repress colonization by AM fungi. The plant defense response regulatory effect for different (iso)flavonoids varies, and their levels are regulated by P. (5) The suppressed expression of symbiotic genes. Some symbiosis-related genes inhibit plant defense responses, but it is still unclear which mechanisms underlie gene regulation. We provide here a theoretical basis for research into AM symbiosis that may promote study of host plant resistance and the mechanisms of symbiosis formation.
We provide a deeper insight into the signal transduction pathways of mycorrhization that will aid understanding and analysis of plant defense mechanisms in the AM context. The on-going development of genome sequencing technology will contribute greatly to the detailed study of symbiosis-related genes, and pathogenesis-related protein genes. These related genes may be induced to express corresponding proteins, be repressed, postpone expression or even shutdown, or both may work together to form symbioses. Elucidation of these features will help us understand the roles that plant defenses play in mycorrhizal formation; providing an unprecedented opportunity for research into mycorrhizal molecular biology and the interaction of symbiotic partners, and allowing the underlying mechanisms to be gradually uncovered.     

Regulation of plant defense responses in Arabidopsis by EDR2, a PH and START domain-containing protein

We have identified an Arabidopsis mutant that displays enhanced disease resistance (edr2) to the biotrophic powdery mildew pathogen Erysiphe cichoracearum. Inhibition of fungal growth on edr2 mutant leaves occurred at a late stage of the infection process and coincided with formation of necrotic lesions approximately 5 days after inoculation. Double-mutant analysis revealed that edr2-mediated resistance is suppressed by mutations that inhibit salicylic acid (SA)-induced defense signaling, including npr1, pad4 and sid2, demonstrating that edr2-mediated disease resistance is dependent on SA. However, edr2 showed normal responses to the bacterial pathogen Pseudomonas syringae pv. tomato strain DC3000. EDR2 appears to be constitutively transcribed in all tissues and organs and encodes a novel protein, consisting of a putative pleckstrin homology (PH) domain and a steroidogenic acute regulatory protein-related lipid-transfer (START) domain, and contains an N-terminal mitochondrial targeting sequence. The PH and START domains are implicated in lipid binding, suggesting that EDR2 may provide a link between lipid signaling and activation of programmed cell death mediated by mitochondria.