Caterpillar- and Salivary-Specific Modification of Plant Proteins

Abstract

Though there is overlap, plant responses to caterpillar herbivory show distinct variations from mechanical wounding. In particular, effectors in caterpillar oral secretions modify wound-associated plant responses. Previous studies have focused on transcriptional and protein abundance differences in response to caterpillar herbivory. This study investigated Spodoptera exigua caterpillar-specific post-translational modification of Arabidopsis thaliana soluble leaf proteins by liquid chromatography/electrospray ionization/mass spectroscopy/mass spectroscopy (LC/ESI/MS/MS). Given that caterpillar labial saliva contains oxidoreductases, such as glucose oxidase, particular attention was paid to redox-associated modifications, such as the oxidation of protein cysteine residues. Caterpillar- and saliva-specific protein modifications were observed. Differential phosphorylation of the jasmonic acid biosynthetic enzyme, lipoxygenase 2, and a chaperonin protein is seen in plants fed upon by caterpillars with intact salivary secretions compared to herbivory by larvae with impaired labial salivary secretions. Often a systemic suppression of photosynthesis is associated with caterpillar herbivory. Of the five proteins modified in a caterpillar-specific manner (a transcription repressor, a DNA-repair enzyme, PS I P700, Rubisco and Rubisco activase), three are associated with photosynthesis. Oxidative modifications are observed, such as caterpillar-specific denitrosylation of Rubisco activase and chaperonin, cysteine oxidation of Rubisco, DNA-repair enzyme, and chaperonin and caterpillar-specific 4-oxo-2-nonenal modification of the DNA-repair enzyme.

Cues from chewing insects — the intersection of DAMPs, HAMPs, MAMPs and effectors

“…The Bede laboratory has been investigating the effect of saliva from larval S. exigua on modification of host proteins, and found that saliva is responsible for the cysteine oxidation of Rubisco and other proteins [46], which is not surprising considering the relatively high level of GOX in this insect [47]. Perhaps more intriguing were changes in the phosphorylation patterns of host proteins when dephosphorylation of a chaperonin at the Thr 59 and lipoxygenase 2 at Ser 600 occurred [46]. The effects of phosphorylation or oxidation on protein activity were not reported in this study, but the results with lipoxygenase 2 are particularly interesting because of its role in JA biosynthesis.…”

Prioritized contingencies: context-dependent regeneratory effects of grazer saliva

“…We suggest that these findings reflect an intricate prioritization of plant responses to prevailing and anticipated challenges, according to their expected harshness and cumulative long-term costs. Herbivore saliva was suggested to enable plants to differentiate between herbivory and physical damage (Korth and Dixon 1997;Thivierge et al 2010); however, the correlation between present and future herbivory might be rather limited (Karban and Adler 1996), reducing the predictive value of salivary cues. On the other hand, prevailing competition and nutrient deficiency often present severe stresses, which are highly autocorrelated with continued stress.…”

“…Specifically, plastic responses to herbivory can be elicited by two sources of information-(a) biomass loss and mechanical injury, which typically generate both direct damages and resource-level cues (sensu Aphalo and Ballare 1995) and (b) salivary cues, which are considered pure cues and were suggested to be used by plants to differentiate herbivory from other mechanical damages (Korth and Dixon 1997;Thivierge et al 2010).…”

Friend or Foe? Exploring the Factors that Determine the Difference Between Positive and Negative Effects on Photosynthesis in Response to Insect Herbivory

“…Proteomic investigations provided further evidence of the vulnerability of the CO 2 fixing process to insect attack by showing that herbivory, or even the application of the insect´s saliva, also reduced the abundance of Rubisco activase (RCA) in Nicotiana attenuata and Arabidopsis (Giri et al, 2006;Thivierge et al, 2010). RCA is a key regulatory enzyme of photosynthetic carbon assimilation that modulates the activity of Rubisco by facilitating the removal of inhibiting sugar phosphates from its active site (Portis, 1995).…”

“…RCA is a key regulatory enzyme of photosynthetic carbon assimilation that modulates the activity of Rubisco by facilitating the removal of inhibiting sugar phosphates from its active site (Portis, 1995). Additional findings derived from the proteomic experimental approaches indicated that Rubisco large subunit and RCA, in addition to PS I P700 apoprotein A1 suffered several caterpillar-specific modifications, including the conversion of Cys192 in Rubisco to the the thiolate anion, which may lead to decreased enzyme activity and protein degradation, and adverse modifications, in RCA, of the protein domains involved in ATP binding (Thivierge et al, 2010).…”