Inheritance and Characterization of Strong Resistance to Phosphine in Sitophilus oryzae (L.)

Abstract

Sitophilus oryzae (Linnaeus) is a major pest of stored grain across Southeast Asia and is of increasing concern in other regions due to the advent of strong resistance to phosphine, the fumigant used to protect stored grain from pest insects. We investigated the inheritance of genes controlling resistance to phosphine in a strongly resistant S. oryzae strain (NNSO7525) collected in Australia and find that the trait is autosomally inherited and incompletely recessive with a degree of dominance of -0.66. The strongly resistant strain has an LC50 52 times greater than a susceptible reference strain (LS2) and 9 times greater than a weakly resistant strain (QSO335). Analysis of F2 and backcross progeny indicates that two or more genes are responsible for strong resistance, and that one of these genes, designated So_rph1, not only contributes to strong resistance, but is also responsible for the weak resistance phenotype of strain QSO335. These results demonstrate that the genetic mechanism of phosphine resistance in S. oryzae is similar to that of other stored product insect pests. A unique observation is that a subset of the progeny of an F1 backcross generation are more strongly resistant to phosphine than the parental strongly resistant strain, which may be caused by multiple alleles of one of the resistance genes.

Genetic characterization of field-evolved resistance to phosphine in the rusty grain beetle, Cryptolestes ferrugineus (Laemophloeidae: Coleoptera)

“…Analysis of reciprocal F 1 hybrids from the three crosses, S-strain x Weak-R, S-strain x Strong-R and Weak-R x Strong-R, failed to detect any maternal influence, thus the genes in both the weak and strong resistance phenotypes are autosomal, as was also observed with weak and strong resistance in R. dominica, T. castaneum and S. oryzae [6][7][8]. These results indicate that phosphine resistance is not due to genetic changes within the mitochondrial genome, even though key mitochondrial proteins have been identified as important for phosphine toxicity [28] or resistance [29,30].…”

“…In homozygous isolation, each of these genes confers only weak resistance, ~4-30×, however, when they occur together in one individual, they interact synergistically and provide a very high level of resistance, up to ~600× [6][7][8]. Genes rph1 and rph2 are expressed as incompletely recessive in all the three species, irrespective of the phenotypes, and are not sex linked [6][7][8][9]. This genetic information together with well-established efficacy data against R.…”

“…The possibility of an additional dominant factor contributing to phosphine resistance was also observed in R. dominica [6] in heterozygotes from a cross of Weak-R x Strong-R. However, this effect was not observed either in T. castaneum [7] or S. oryzae [8,9], indicating the existence of differences between species in background genetic factors contributing to the expression of the resistance phenotype. Similarly, higher survival of F 1 (R x S) hybrids than expected in permethrin-resistant tobacco budworm, Heliothis virescens (F.), was attributed to the presence of minor dominant factors in addition to a major recessive factor, regulating the overall expression of resistance phenotype in this pest [31].…”

“…This information is crucial to the development of rational and sustainable resistance management. Strong resistance to phosphine in the lesser grain borer, Rhyzopertha dominca (Fabricius) [6], the red flour beetle, Tribolium castaneum (Herbst) [7], and the rice weevil, Sitophilus oryzae (Linnaeus) [8], is mediated by two major autosomal recessive genes, rph1 and rph2. In homozygous isolation, each of these genes confers only weak resistance, ~4-30×, however, when they occur together in one individual, they interact synergistically and provide a very high level of resistance, up to ~600× [6][7][8].…”

“…Strong resistance to phosphine in the lesser grain borer, Rhyzopertha dominca (Fabricius) [6], the red flour beetle, Tribolium castaneum (Herbst) [7], and the rice weevil, Sitophilus oryzae (Linnaeus) [8], is mediated by two major autosomal recessive genes, rph1 and rph2. In homozygous isolation, each of these genes confers only weak resistance, ~4-30×, however, when they occur together in one individual, they interact synergistically and provide a very high level of resistance, up to ~600× [6][7][8]. Genes rph1 and rph2 are expressed as incompletely recessive in all the three species, irrespective of the phenotypes, and are not sex linked [6][7][8][9].…”