Molecular basis of Colorado potato beetle adaptation to potato plant defence at the level of digestive cysteine proteinases

Gruden, Kristina; Kuipers, A.; Gunčar, Gregor; Slapar, N.; Štrukelj, Borut; Jongsma, Maarten A.

doi:10.1016/j.ibmb.2004.01.003

Cited by 65 publications

(78 citation statements)

References 30 publications

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“…approximately 0.5%). In this perspective, SlCYS8 variants such as P2F and P2L, which exhibit IC 50 values decreased by 2-to 3-fold for the Colorado potato beetle cystatin-sensitive proteases (Table II), could provide improved antidigestive effects at given expression rates in planta and thus help avoid effective compensatory processes in this target herbivore (Cloutier et al, , 2000Gruden et al, 2003Gruden et al, , 2004Brunelle et al, 2004). An inhibitory spectrum extended to the so-called cystatininsensitive proteases for these same two variants also could make them more effective in vivo, as suggested by a recent study reporting increased deleterious effects for a hybrid corn cystatin II bearing an extra protease inhibitory function (Brunelle et al, 2005).…”

Section: Discussionmentioning

confidence: 99%

Tailoring the Specificity of a Plant Cystatin toward Herbivorous Insect Digestive Cysteine Proteases by Single Mutations at Positively Selected Amino Acid Sites

et al. 2008

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Plant cystatins, similar to other defense proteins, include hypervariable, positively selected amino acid sites presumably impacting their biological activity. Using 29 single mutants of the eighth domain of tomato (Solanum lycopersicum) multicystatin, SlCYS8, we assessed here the potential of site-directed mutagenesis at positively selected amino acid sites to generate cystatin variants with improved inhibitory potency and specificity toward herbivorous insect digestive cysteine (Cys) proteases. Compared to SlCYS8, several mutants (22 out of 29) exhibited either improved or lowered potency against different model Cys proteases, strongly suggesting the potential of positively selected amino acids as target sites to modulate the inhibitory specificity of the cystatin toward Cys proteases of agronomic significance. Accordingly, mutations at positively selected sites strongly influenced the inhibitory potency of SlCYS8 against digestive Cys proteases of the insect herbivore Colorado potato beetle (Leptinotarsa decemlineata). In particular, several variants exhibited improved potency against both cystatin-sensitive and cystatininsensitive digestive Cys proteases of this insect. Of these, some variants also showed weaker activity against leaf Cys proteases of the host plant (potato [Solanum tuberosum]) and against a major digestive Cys protease of the two-spotted stinkbug Perillus bioculatus, an insect predator of Colorado potato beetle showing potential for biological control. Overall, these observations suggest the usefulness of site-directed mutagenesis at positively selected amino acid sites for the engineering of recombinant cystatins with both improved inhibitory potency toward the digestive proteases of target herbivores and weaker potency against nontarget Cys proteases in the host plant or the environment.

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Section: Discussionmentioning

confidence: 99%

Tailoring the Specificity of a Plant Cystatin toward Herbivorous Insect Digestive Cysteine Proteases by Single Mutations at Positively Selected Amino Acid Sites

et al. 2008

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“…Alternatively, it is possible that CPB larvae adapted to lower levels of defenses induced by untreated larvae. It was shown that CPB larvae can overcome induced defenses by changing the profile of their digestive proteases (30).…”

Section: Tomato (Simentioning

confidence: 99%

Herbivore exploits orally secreted bacteria to suppress plant defenses

Chung¹,

Rosa²,

Scully

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

380

381

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Significance The role of herbivore-associated microbes in modifying plant defenses has received scant attention. The Colorado potato beetle secretes symbiotic bacteria to wounds to manipulate plant defenses. The bacteria elicit salicylic acid (SA)-regulated defenses, and because SA signaling often negatively cross-talks with jasmonate signaling, plants are unable to fully activate their jasmonate-mediated resistance against the herbivore. From the plants’ perspective, they recognize herbivores not as such, but as microbial threats. We identified the specific bacteria from the beetle secretions and also characterized one of the bacterial effectors responsible for defense suppression. This clever, deceptive strategy for suppressing defenses has not been previously documented. Our results add a significant, unique concept to plant–insect interactions and how herbivores hijack plant defense signaling.

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“…These insects have developed over time effective strategies to elude the inhibitory effects of plant protease inhibitors, involving the use of complex digestive protease systems with proteases from different mechanistic classes acting in a complementary, coordinated manner (Brunelle et al, 1999;Hernandez et al, 2003;Gruden et al, 2003;Vinokurov et al, 2006a,b;Prabhakar et al, 2007); the over-expression of target proteases following cystatin ingestion to outnumber the inhibitory proteins (Cloutier et al, 2000;Ahn et al, 2004); the constitutive or diet-induced expression of cysteine cathepsins weakly sensitive to the ingested cystatin, the so-called 'cystatin-insensitive proteases' (Michaud et al, 1993(Michaud et al, , 1995aGirard et al, 1998a;Cloutier et al, 1999Cloutier et al, , 2000ZhuSalzman et al, 2003;Brunelle et al, 2004;Gruden et al, 2004;Liu et al, 2004;Koo et al, 2008); the over-expression of proteases from alternative mechanistic classes following cystatin ingestion (Zhu-Salzman et al, 2003;Brunelle et al, 2004;Rivard et al, 2004;Oppert et al, 2005); and the degradation of defensive protease inhibitors using non-target, insensitive proteases (Michaud et al, 1995b;Girard et al, 1998b;Giri et al, 1998;Gruden et al, 2003;Zhu-Salzman et al, 2003).…”

Section: Discussionmentioning

confidence: 99%

“…The negative effects of E-64 on growth and fecundity of several coleopteran species, including cystatin-resistant insects such as the Colorado potato beetle Leptinotarsa decemlineata (Bolter and Latoszek-Green, 1997) and the cowpea weevil Callosobruchus maculatus (Murdock et al, 1988), were systematically associated with a broadspectrum inhibition of cysteine proteases in midgut extracts (Michaud et al, 1993;Fabrick et al, 2002;Kim and Mullin, 2003). By contrast, the reported inefficiency of plant cystatins against a number of Coleoptera was typically associated with the presence of cystatin-insensitive cysteine proteases, thought to help the target insects compensating for the loss of sensitive protease activities following cystatin intake (Cloutier et al, , 2000Zhu-Salzman et al, 2003;Gruden et al, 2003Gruden et al, , 2004. In line with previous studies reporting detrimental effects for cystatins or other plant cysteine-type inhibitors against some coleopteran species (Zhao et al, 1996;Koiwa et al, 2000;Fabrick et al, 2002), the negative effects of OsCYS1 and CpCYS1 against the banana Plant cystatins against the banana weevil Page 16 weevil were correlated with a broad inhibitory spectrum of the two cystatins against Z-FR-MCA-(cathepsin L-like) and Z-RR-MCA-hydrolyzing (cathepsin B-like) cysteine proteases in midgut extracts, comparable to the overall inhibitory effect of E-64 against the same enzymes.…”

Section: Discussionmentioning

confidence: 99%

“…Several papers have been published assessing the effectiveness of plant cystatins against herbivorous Coleoptera, with conclusive results in some cases (Leplé et al, 1995;Kuroda et al, 1996;Lecardonnel et al, 1999;Koiwa et al, 2000;Alvarez-Alfageme et al 2007;Ninkovic et al, 2007) but disappointing results in other cases owing to the ability of the target insects to readily elude or even counteract the antidigestive effects of natural or recombinant inhibitors (e.g. Girard et al, 1998a,b;Cloutier et al, 1999Cloutier et al, , 2000Zhu-Salzman et al, 2003;Gruden et al, 2003Gruden et al, , 2004Ahn et al, 2004Ahn et al, , 2007Oppert et al, 2005;Koo et al, 2008). Here we document the broad inhibitory effects of plant cystatins against midgut cysteine cathepsins of the banana weevil, and the detrimental effects of these proteins on larval growth using a novel bioassay set-up with cystatin-infiltrated banana tissues.…”

Section: Introductionmentioning

confidence: 99%

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Deleterious effects of plant cystatins against the banana weevil Cosmopolites sordidus

Kiggundu

Muchwezi

Vyver

et al. 2009

Arch Insect Biochem Physiol

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The general potential of plant cystatins for the development of insect-resistant transgenic plants still remains to be established given the natural ability of several insects to compensate for the loss of active cysteine proteases following inhibitor ingestion. Here we assessed the potential of cystatins for the development of banana lines resistant to the banana weevil Cosmopolites sordidus, a major pest of banana and plantain in Africa. Protease inhibitory assays were first conducted with protein and methylcoumarin (MCA) peptide substrates to measure the inhibitory efficiency of different cystatins in vitro, followed by a diet bioassay with cystatin-infiltrated banana stem disks to monitor the impact of two plant cystatins, oryzacystatin I (OC-I, or OsCYS1)and papaya cystatin (CpCYS1), on the overall growth rate of young weevil larvae. As observed earlier for other Coleoptera, banana weevils produce a variety of proteases for dietary protein digestion, including in particular Z-Phe-Arg-MCA-hydrolyzing (cathepsin L-like) and Z-Arg-Arg- MCA-hydrolyzing (cathepsin B-like) proteases active in mildly acidic conditions. Both enzyme populations were sensitive to the diagnostic cysteine protease inhibitor E-64 and to different plant cystatins including OsCYS1. In line with these broad inhibitory effects of cystatins, OsCYS1 andCpCYS1 caused an important growth delay in young larvae developing for 10 days in cystatininfiltrated banana stem disks. These promising results, which illustrate the natural susceptibility of C. sordidus to plant cystatins, are discussed in the light of current genomic data on coleopteran cysteine cathepsins and recent hypotheses suggesting a key role for digestive cathepsin B-like enzymes as a determinant for resistance or susceptibility to plant cystatins in Coleoptera.Keywords: Banana weevil (Cosmopolites sordidus); banana (Musa spp.); cathepsin B-like proteases; cysteine cathepsins; plant cystatins; oryzacystatin I Plant cystatins against the banana weevil Page 3 INTRODUCTIONThe banana weevil Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae) is an insect pest of considerable importance in Africa, associated with the rapid decline of banana and plantain plantations (Gold, 1999a(Gold, , 2000Swennen and Vuylsteke, 2001;Gold et al., 2005). At the adult stage, banana weevil females deposit their eggs inside host plant tissues, at the base of the pseudostem or on an exposed corm. On hatching, the larvae tunnel through the corm to feed and develop, where they damage tissues, compromise water and mineral uptake, and weaken the colonized organs. Banana weevil infestations cause important losses in the field by a direct negative impact on harvestable bunch weight and a weakening effect on infested organs causing plant toppling during windstorms (Sengooba, 1986;Rukazambuga et al., 1998).Banana weevil control in Africa relies essentially on cultural and sanitation practices such as the use of clean planting material, the systematic trapping of adult weevils to prevent population build-up, an...

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Molecular basis of Colorado potato beetle adaptation to potato plant defence at the level of digestive cysteine proteinases

Cited by 65 publications

References 30 publications

Tailoring the Specificity of a Plant Cystatin toward Herbivorous Insect Digestive Cysteine Proteases by Single Mutations at Positively Selected Amino Acid Sites

Tailoring the Specificity of a Plant Cystatin toward Herbivorous Insect Digestive Cysteine Proteases by Single Mutations at Positively Selected Amino Acid Sites

Herbivore exploits orally secreted bacteria to suppress plant defenses

Deleterious effects of plant cystatins against the banana weevil Cosmopolites sordidus

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