The mirid bug Apolygus lucorum deploys a glutathione peroxidase as a candidate effector to enhance plant susceptibility

Abstract

The mirid bug Apolygus lucorum has become a major agricultural pest since the large-scale cultivation of Bt-cotton. It was assumed that A. lucorum, similarly to other phloem sap insects, could secrete saliva that contains effector proteins into plant interfaces to perturb host cellular processes during feeding. However, the secreted effectors of A. lucorum are still uncharacterized and unstudied. In this study, 1878 putative secreted proteins were identified from the transcriptome of A. lucorum, which either had homology with published aphid effectors or shared common features with plant pathogens and insect effectors. One hundred and seventy-two candidate effectors were used for cell death-inducing/suppressing assays, and a putative salivary gland effector, Apolygus lucorum cell death inhibitor 6 (Al6), was characterized. The mRNAs of Al6 were enriched at feeding stages (nymph and adult) and, in particular, in salivary glands. Moreover, we revealed that the secreted Al6 encoded an active glutathione peroxidase that reduced reactive oxygen species (ROS) accumulation induced by INF1 or Flg22. Expression of the Al6 gene in planta altered insect feeding behavior and promoted plant pathogen infections. Inhibition of cell death and enhanced plant susceptibility to insect and pathogens are dependent on glutathione peroxidase activity of Al6. Thus, this study shows that a candidate salivary gland effector, Al6, functions as a glutathione peroxidase and suppresses ROS induced by pathogen-associated molecular pattern to inhibit pattern-triggered immunity (PTI)-induced cell death. The identification and molecular mechanism analysis of the Al6 candidate effector in A. lucorum will provide new insight into the molecular mechanisms of insect–plant interactions.

A salivary calcium‐binding protein from Laodelphax striatellus acts as an effector that suppresses defense in rice

“…These substances may positively 11–17 or negatively 3, 18, 19 regulate insect performance on plant hosts. For example, salivary effectors such as Armet, Mp1, Mp2, Me47, Bt56, Bsp9, migration inhibitory factor, ferritin glutathione peroxidase and others impair plant defense responses 2, 3, 11, 12, 14, 17, 20–22 …”

Identification of Riptortus pedestris Salivary Proteins and Their Roles in Inducing Plant Defenses

“…Therefore, cell death and alteration in the hormone pathways of transfected plants may be positively correlated with ROS burst [ 20 ]. Although the five proteins are found to induce plant defenses, there may be other salivary components that suppress these detrimental effects, such as macrophage migration inhibitory factor in M. percicae , [ 25 ] and Al6 in Apolygus lucorum [ 27 ]. Further studies are warranted to unveil the complex mechanisms of R. pedestris saliva in insect–plant interaction.…”

“…Besides, salivary DNase II assists in the colonization of planthopper on host plants by degrading DAMPs released from damaged cells [ 26 ]. Recently, mirid bug was found to secrete a glutathione peroxidase that eliminates ROS accumulation and inhibits the pattern-triggered, immunity-induced cell death [ 27 ]. Such result indicates that salivary proteins are also important for true bugs.…”

Screening Candidate Effectors of the Bean Bug Riptortus pedestris by Proteomic and Transcriptomic Analyses

“…Still, the studies paid main attention to digestive enzymes again, whereas very few discussed the effector functions of the salivary proteins. However, a recent study found that a glutathione peroxidase was highly expressed in the salivary glands of A. lucorum, who probably use it to eliminate the reactive oxygen species (ROS) accumulation in plants (Dong et al, 2020).…”