Effects of a potato cysteine proteinase inhibitor on midgut proteolytic enzyme activity and growth of the southern corn rootworm, Diabrotica undecimpunctata howardi (Coleoptera: Chrysomelidae)

Fabrick, Jeffrey A.; Behnke, Craig A.; Czapla, T.H.; Bala, Kiran; Rao, A. G. Appu; Kramer, Karl J.; Reeck, Gerald R.

doi:10.1016/s0965-1748(01)00117-5

Cited by 32 publications

(26 citation statements)

References 33 publications

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“…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. Our data support, in sum, the hypothesis of a close relationship between the inhibitory spectrum of plant cystatins against E-64-sensitive cysteine proteases in midgut extracts and the potential of these inhibitors as effective candidates for the development of transgenic plant lines resistant to coleopteran pests.…”

Section: Discussionsupporting

confidence: 77%

“…As suggested from studies reporting detrimental effects for the broad-spectrum inhibitor of papain-like proteases E-64 against Coleoptera, these negative effects of OsCYS1 and CpCYS1 were likely the result of a broad sensitivity of the insect digestive cathepsins to the ingested inhibitors. 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.…”

Section: Discussionmentioning

confidence: 99%

“…Murdock et al, 1988;Bolter and Latoszek-Green, 1997;Fabrick et al, 2002). In this study, we assessed the potential of OC-I and other plant cystatins as possible tools for the production of transgenic banana lines resistant to the banana weevil.…”

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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Section: Discussionsupporting

confidence: 77%

Section: Discussionmentioning

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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“…However, other compounds, such as proteinase inhibitors (PIs), can play a role in plant defense, affecting the digestibility of proteins and decreasing the availability of free amino acids required by insects for growth, development, and reproduction (8). Cysteine proteinases are common in the slightly acidic midgut (pH 5-7) of many coleopterans (9,10), and cysteine PIs (CystPIs) in plant tissues decrease growth and development by inhibiting these proteinases (10,11). Induction of the jasmonate signaling pathway in plants by herbivore damage leads to increased synthesis of CystPIs (12).…”

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confidence: 99%

Anthropogenic increase in carbon dioxide compromises plant defense against invasive insects

Zavala

Casteel

DeLucia

et al. 2008

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

199

163

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Elevated levels of atmospheric carbon dioxide (CO 2 ), a consequence of anthropogenic global change, can profoundly affect the interactions between crop plants and insect pests and may promote yet another form of global change: the rapid establishment of invasive species. Elevated CO 2 increased the susceptibility of soybean plants grown under field conditions to the invasive Japanese beetle ( Popillia japonica ) and to a variant of western corn rootworm ( Diabrotica virgifera virgifera ) resistant to crop rotation by down-regulating gene expression related to defense signaling [lipoxygenase 7 ( lox7 ), lipoxygenase 8 ( lox8 ), and 1-aminocyclopropane-1-carboxylate synthase ( acc-s )]. The down-regulation of these genes, in turn, reduced the production of cysteine proteinase inhibitors (CystPIs), which are specific deterrents to coleopteran herbivores. Beetle herbivory increased CystPI activity to a greater degree in plants grown under ambient than under elevated CO 2 . Gut cysteine proteinase activity was higher in beetles consuming foliage of soybeans grown under elevated CO 2 than in beetles consuming soybeans grown in ambient CO 2 , consistent with enhanced growth and development of these beetles on plants grown in elevated CO 2 . These findings suggest that predicted increases in soybean productivity under projected elevated CO 2 levels may be reduced by increased susceptibility to invasive crop pests.

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“…The general usefulness of PhyCys for pest control have been shown, particularly against phytophagous coleopteran species which rely mostly on cysteine protease activities for the digestión of dietary proteins (Fabrick et al 2002;Lalitha et al 2005;Alvarez-Alfágeme et al 2007). Moreover, many other studies have shown that PhyCys also affect the growth or survival of other inseets, nematodes and slugs on artificial diets or delivered through transgenic plants (Walker et al 1999;Lilley et al 2004;Ribeiro et al 2006;Konrad et al 2009;Carrillo et al 2010).…”

Section: Discussionmentioning

confidence: 99%

Expression of a barley cystatin gene in maize enhances resistance against phytophagous mites by altering their cysteine-proteases

et al. 2010

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Phytocystatins are inhibitors of cysteine-proteases from plants putatively involved in plant defence based on their capability of inhibit heterologous enzymes. We have previously characterised the whole cystatin gene family members from barley (HvCPI-1 to HvCPI-13). The aim of this study was to assess the effects of barley cystatins on two phytophagous spider mites, Tetranychus urticae and Brevipalpus chilensis. The determination of proteolytic activity profile in both mite species showed the presence of the cysteine-proteases, putative targets of cystatins, among other enzymatic activities. All barley cystatins, except HvCPI-1 and HvCPI-7, inhibited in vitro mite cathepsin L-and/or cathepsin B-like activities, HvCPI-6 being the strongest inhibitor for both mite species. Transgenic maize plants expressing HvCPI-6 protein were generated and the functional integrity of the cystatin transgene was confirmed by in vitro inhibitory effect observed against T urticae and B. chilensis protein extracts. Feeding experiments impaired on transgenic lines performed with T urticae impaired mite development and reproductive performance. Besides, a significant reduction of cathepsin L-like and/or cathepsin B-like activities was observed when the spider mite fed on maize plants expressing HvCPI-6 cystatin. These findings reveal the potential of barley cystatins as acaricide proteins to protect plants against two important mite pests.

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Effects of a potato cysteine proteinase inhibitor on midgut proteolytic enzyme activity and growth of the southern corn rootworm, Diabrotica undecimpunctata howardi (Coleoptera: Chrysomelidae)

Cited by 32 publications

References 33 publications

Deleterious effects of plant cystatins against the banana weevil Cosmopolites sordidus

Deleterious effects of plant cystatins against the banana weevil Cosmopolites sordidus

Anthropogenic increase in carbon dioxide compromises plant defense against invasive insects

Expression of a barley cystatin gene in maize enhances resistance against phytophagous mites by altering their cysteine-proteases

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