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Table 3 H. halys salivary effectors with homologs previously implicated in mediating herbivorous hemipterans’ interaction with plant hosts

From: Brown marmorated stink bug, Halyomorpha halys (Stål), genome: putative underpinnings of polyphagy, insecticide resistance potential and biology of a top worldwide pest

Salivary effector

Gene symbol

Protein Reference

Pea aphid homolog

BLAST E-value

Comment

Armet/mesencephalic astrocyte -derived neurotrophic factor

LOC106681713

XP_014277663.1

ACYPI008001

1.6e-45

Found in pea aphid saliva and aphid-fed plants. RNAi targeting Armet expression disrupted aphid feeding behavior leading to reduced life span [91].

Mp10/ejaculatory bulb-specific protein

LOC106681352

XP_014277113.1

ACYPI000097

1.6e-26

Mp10 from green peach aphid induced chlorosis, localized cell death in planta, and triggered plant defenses [92, 93].

Angiotensin-converting enzyme, Ace2

LOC106681465

XP_014277274.1

ACYPI007204

0

Ace, a M2 metalloprotease, potentially degrade short signaling peptides capable of inducing plant defense. RNAi simultaneously targeting Ace1 and Ace2 expression in pea aphid caused significant mortality [90, 94].

Mucin-like

LOC106684151

XP_014281554.1

ACYPI001019

1.6e-41

Found in both gelling and watery saliva of rice brown planthopper. RNAi targeting its expression disrupted the salivary sheath formation leading to disordered developmental duration and poor performance [95, 96].

Calreticulin

LOC106681650

XP_014277576.1

ACYPI002622

0

Calcium binding proteins found in saliva of southern green stink bug and various aphid species, putatively involved in suppressing the activation of defense cascades [82, 90, 97].

Sarcalumenin

LOC106681164

XP_014276825.1

ACYPI001446

0

Endoplasmin

LOC106681661

XP_014277591.1

ACYPI009915

0

Digestive cysteine proteinase 1

LOC106685481

XP_014283673.1

ACYPI003954

5.4e-170

Cysteine proteinase-like cathepsins have been found in saliva of southern green stink bug [82], these enzymes potentially degrade plant defense peptides and/or perform extra-oral digestion of dietary proteins.

Cathepsin B

LOC106690036

XP_014290885.1

ACYPI000003

3.2e-139

Cysteine proteinase

LOC106682432

XP_014278766.1

ACYPI000376

1.7e-123

Cathepsin L1

LOC106682597

XP_014279027.1

ACYPI006974

3e-114

Disulfide isomerase

LOC106677432

XP_014270846.1

ACYPI005594

0

Found in saliva of southern green stink bug and various aphid species, potentially aid in gelling nature of sheath saliva by catalyzing the formation of disulfide bridges in proteins [90, 98].

LOC106678635

XP_014272751.1

ACYPI009755

0

LOC106686982

XP_014286089.1

ACYPI008926

1e-172

Superoxide dismutase

LOC106681155

XP_014276814.1

ACYPI003921

2.56e-58

Antioxidant enzymes have been found in saliva of southern green stink bug and various aphid species [82, 90, 99,100,101,102], and supposedly degrade reactive oxygen species, plant’s initial defense response.

Peroxidase-like isoform X1

LOC106692485

XP_014293941.1

ACYPI000817

1.2e-108

Peroxiredoxin-2

LOC106681766

XP_014277748.1

ACYPI003960

9.2e-138

Selenoprotein-like

LOC106691878

XP_014293266.1

ACYPI003278

3.7e-69

Neutral alpha-glucosidase

LOC106679031

XP_014273428.1

ACYPI009457

0

Found in saliva of plant tarnished bug, glassy-winged sharpshooter, and potato aphid, potentially break down complex carbohydrates such as cellulose in plant cell wall [103,104,105].

Trehalase

LOC106681721

XP_014277675.1

ACYPI002298

0

Found in saliva of various aphid species; putatively suppresses the activation of plant defenses by disrupting signal transduction [90, 97, 98, 106].

Aminopeptidase N

LOC106686134

XP_014284771.1

ACYPI002258

0

Found in saliva of southern green stink bug, tarnished plant bug, and pea aphid; potentially destroy plant defense and signaling peptides [82, 90, 105].

Carboxypeptidase E

LOC106686022

XP_014284587.1

ACYPI001238

0

Found in saliva of various hemipteran species [90, 107], potentially degrade plant defense peptides and/or perform extra-oral digestion of dietary proteins.

Pancreatic triacylglycerol lipase

LOC106692440

XP_014293875.1

ACYPI009369

3.0e-60

Lipases have been found in saliva of various hemipteran species [99, 103, 107,108,109], potentially interfere plant defense by binding to lipids and/or perform extra-oral digestion of dietary proteins

Pancreatic lipase-related protein

LOC106679755

XP_014274569.1

ACYPI003852

0

Apolipophorins

LOC106679717

XP_014274514.1

ACYPI004198

1.1e-76

Found in saliva of various aphid species [90, 99, 108], potentially interfere plant defense signaling.

Glycosyltransferase

LOC106688290

XP_014288163.1

ACYPI002729

0

Several glycosyltransferases have been found in saliva of southern green stink bug [82].

Protein yellow

LOC106690949

XP_014292045.1

ACYPI000479

1e-168

Found in two cereal aphid species, it potentially targets the phenoloxidase-based defense in plants [106].

 

LOC106680598

XP_014275905.1

ACYPI001857

9e-112

Several glycosyltransferases have been found in saliva of southern green stink bug [82].