Salivary proteins of plant-feeding hemipteroids – implication in phytophagy

Abstract

Many hemipteroids are major pests and vectors of microbial pathogens, infecting crops. Saliva of the hemipteroids is critical in enabling them to be voracious feeders on plants, including the economically important ones. A plethora of hemipteroid salivary enzymes is known to inflict stress in plants, either by degrading the plant tissue or by affecting their normal metabolism. Hemipteroids utilize one of the following three strategies of feeding behaviour: salivary sheath feeding, osmotic-pump feeding and cell-rupture feeding. The last strategy also includes several different tactics such as lacerate-and-flush, lacerate-and-sip and macerate-and-flush. Understanding hemipteroid feeding mechanisms is critical, since feeding behaviour directs salivary composition. Saliva of the Heteroptera that are specialized as fruit and seed feeders, includes cell-degrading enzymes, auchenorrhynchan salivary composition also predominantly consists of cell-degrading enzymes such as amylase and protease, whereas that of the Sternorhyncha includes a variety of allelochemical-detoxifying enzymes. Little is known about the salivary composition of the Thysanoptera. Cell-degrading proteins such as amylase, pectinase, cellulase and pectinesterase enable stylet entry into the plant tissue. In contrast, enzymes such as glutathione peroxidase, laccase and trehalase detoxify plant chemicals, enabling the circumvention of plant-defence mechanisms. Salivary enzymes such as M1-zinc metalloprotease and CLIP-domain serine protease as in Acyrthosiphon pisum (Aphididae), and non-enzymatic proteins such as apolipophorin, ficolin-3-like protein and 'lava-lamp' protein as in Diuraphis noxia (Aphididae) have the capacity to alter host-plant-defence mechanisms. A majority of the hemipteroids feed on phloem, hence Ca++-binding proteins such as C002 protein, calreticulin-like isoform 1 and calmodulin (critical for preventing sieve-plate occlusion) are increasingly being recognized in hemipteroid-plant interactions. Determination of a staggering variety of proteins shows the complexity of hemipteroid saliva: effector proteins localized in hemipteran saliva suggest a similarity to the physiology of pathogen-plant interactions.

Salivary gland structure of Ctenarytaina eucalypti (MASKELL, 1890) (Hemiptera) and phloem exudate in Eucalyptus globulus LABILLARDIÈRE, 1799 (Myrtaceae)

“…Production of quinones in the leaves of E. globulus leaves when infested by C. eucalypti was reported by TRONCOSO et al (2012). Cell-degrading enzymes, such as amylase, lipase and esterase, may enable C. eucalypti to pierce tissues of E. globulus (OTEN et al 2014, SHARMA et al 2013). Amylase and protease have been demonstrated in the saliva of Trioza jambolanae CRAWFORD, 1917 (Hemiptera: Psylloidea: Triozidae), which lives on Syzigium cumini LINNAEUS, 1753 (Myrtaceae) (RAJADURAI et al 1990).…”

“…The protein labelled 'band A' is approximately 64 kDa in molecular weight and may represent glucose-methanol-choline-oxidoreductase (53-66 kDa); Zn-binding dehydrogenase (67 kDa) and esterase (65-96 kDa). The protein labelled band B (58 kDa) could be cytochrome P-450 (50-55 kDa), trehalase (56 kDa), amylase (50-75 kDa) and lipase (48-52 kDa) (SHARMA et al 2013).…”

“…The gel-like saliva is implicated as an avoidance tactic to circumvent allelochemicals of the host plant during feeding (MILES 1999). For instance, oxidoreductases in the gel-like saliva polymerizes the phenolics sequestered in the plantcell apoplast as an induced defence mechanism and generates quinones (SHARMA et al 2013). Production of quinones in the leaves of E. globulus leaves when infested by C. eucalypti was reported by TRONCOSO et al (2012).…”

Feeding Biology and Nutritional Physiology of Psylloidea(Insecta:Hemiptera):Implications in Host-Plant Relations

“…During feeding, a modest level of mechanical damage eventuates during stylet insertion and movement in plant tissues. In contrast, the chemical injury by salivary enzymes induces intense transcriptomic changes 39 . Feeding action of Psylloidea alters the photosynthetic activity in host tissues significantly, which, in turn, affects primary-plant metabolism 40 .…”

“…The enzyme battery enables C. eucalypti to pierce leaf tissues of E. globulus and feed (Figure 9) 43 . The Sternorrhyncha form stylet sheaths during feeding; whereas the Auchenorrhyncha and Heteroptera rupture plant cells during feeding 39,41 . Although the stylet pathway of Psylloidea is intercellular, they probe and puncture mesophyll cells randomly along the path.…”