Compensatory proteolytic responses to dietary proteinase inhibitors in the red flour beetle, Tribolium castaneum (Coleoptera: Tenebrionidae)

Oppert, Brenda; Morgan, Thomas D.; Hartzer, Kris; Kramer, Karl J.

doi:10.1016/j.cca.2005.01.006

Cited by 58 publications

(65 citation statements)

References 22 publications

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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%

“…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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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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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“…Similarly, expression of a fusion protein composed of a cystatin and a serine PI has been used to control certain nematode pathogens in transgenic plants [245]. Oppert and colleagues [246] demonstrated synergism between soybean Kunitz trypsin inhibitor and the cysteine protease inhibitor L-trans-epoxysuccinyleucylamide [4-guanidino] butane (E64) in artificial diet bioassays with Tribolium castaneum (red flour beetle, Coleoptera).…”

Section: Use Of Multiple Inhibitorsmentioning

confidence: 99%

Biotechnological Approaches for the Control of Insect Pests in Crop Plants

Stevens¹,

Dunse²,

Fox³

et al. 2012

Pesticides - Advances in Chemical and Botanical Pesticides

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“…It has been demonstrated that the combination of cysteine and serine protease inhibitors of soya caused inhibition and significant mortality of the larvae of Tribolium castaneum (brown flower beetle.) (Oppert et al, 2005). In 2005, it was shown that the gene SBTI introduced in Trifolium repens (white clover) allowed the plant to resist the attacks of Teleogryllus commodus (black field cricket) and Costelytra zealandica (grass grub) (McManus et al, 2005).…”

Section: Application Of Spi In Genetic Engineeringmentioning

confidence: 99%

The serine protease inhibitors and plant-insect interaction

Mendoza-Blanco¹,

Casaretto

2012

Idesia

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Plants respond to a physical injury or biological attack by producing, among other compounds, an arsenal of defense proteins, secondary metabolites and phytohormones, all necessary for plant survival. Defense proteins include the group of serine protease inhibitors (SPI), proteins that interact with the active site of their target enzymes. The activity of these protease inhibitors has been exploited to combat insect pests. SPI is an interesting alternative to produce plants with improved resistance characters through selection in the field or expressing their genes in sensitive plants by genetic engineering. The alternative that these natural products offer makes them valuable for the control of several crop pests.Key words: biological control, defense proteins, serine protease inhibitors. RESUMEN

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Compensatory proteolytic responses to dietary proteinase inhibitors in the red flour beetle, Tribolium castaneum (Coleoptera: Tenebrionidae)

Cited by 58 publications

References 22 publications

Deleterious effects of plant cystatins against the banana weevil Cosmopolites sordidus

Deleterious effects of plant cystatins against the banana weevil Cosmopolites sordidus

Biotechnological Approaches for the Control of Insect Pests in Crop Plants

The serine protease inhibitors and plant-insect interaction

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