Aphid growth and reproduction on plants with altered sterol profiles: Novel insights using Arabidopsis mutant and overexpression lines

Chen, Ivy W.; Grebenok, Robert J.; Schaller, Hubert; Zhu‐Salzman, Keyan; Behmer, Spencer T.

doi:10.1016/j.jinsphys.2020.104054

Cited by 9 publications

(12 citation statements)

References 60 publications

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“…They tend to maintain constant cholesterol levels and adjust unsuitable sterols below a certain level, and the failure of this regulation can lead to death [ 13 , 36 ]. Therefore, disruption of the processes of sterol acquisition by changing plant sterol composition is a promising method for controlling many phytophagous pest species [ 29 ]. Genetically manipulated plants containing atypical phytosterols exhibit biological control potential [ 29 , 37 , 38 ].…”

Section: Discussionmentioning

confidence: 99%

“…Therefore, disruption of the processes of sterol acquisition by changing plant sterol composition is a promising method for controlling many phytophagous pest species [ 29 ]. Genetically manipulated plants containing atypical phytosterols exhibit biological control potential [ 29 , 37 , 38 ]. In this study, for the first time, we explored the sterol requirements of two closely related lepidopteran pests, M .…”

Section: Discussionmentioning

confidence: 99%

“…These sterol–metabolic limitations can be exploited to develop non-insecticidal strategies. For example, increasing the proportion of unsuitable sterols in plants or inhibiting metabolic targets were proved to be promising for controlling phytophagous pests [ 28 , 29 , 30 ].…”

Section: Introductionmentioning

confidence: 99%

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Discrepancy in Sterol Usage between Two Polyphagous Caterpillars, Mythimna separata and Spodoptera frugiperda

Tang

Liang

Jing

et al. 2022

Insects

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Insects are sterol auxotrophs and typically obtain sterols from food. However, the sterol demand and metabolic capacity vary greatly among species, even for closely related species. The low survival of many insects on atypical sterols, such as cholestanol and cholestanone, raises the possibility of using sterol-modified plants to control insect herbivore pests. In this study, we evaluated two devastating migratory crop pests, Mythimna separata and Spodoptera frugiperda, in response to atypical sterols and explored the reasons that caused the divergences in sterol nutritional biology between them. Contrary to M. separata, S. frugiperda had unexpectedly high survival on cholestanone, and nearly 80% of the individuals pupated. Comparative studies, including insect response to multiple diets and larval body sterol/steroids analysis, were performed to explain their differences in cholestanone usage. Our results showed that, in comparison to M. separata, the superiority of S. frugiperda on cholestanone can be attributed to its higher efficiency of converting ketone into available stanol and its lower demand for sterols, which resulted in a better survival when cholesterol was unavailable. This research will help us to better understand insect sterol nutritional biology and the potential of using atypical sterols to control herbivorous insect pests.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Discrepancy in Sterol Usage between Two Polyphagous Caterpillars, Mythimna separata and Spodoptera frugiperda

Tang

Liang

Jing

et al. 2022

Insects

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“…To analyze leaf sterols, we used 4-week-old plants from ve selected lines (Col-0 and HYD1 RNAi 7,10,12,25); each sample contained multiple leaves that were lyophilized and ground into a ne powder in liquid nitrogen. Individual samples (20 mg) were extracted with 4.5 mL chloroform-methanol (CHCl 3 -MeOH) (2:1, v/v); 5α-cholestane (1 µg/mL, Sigma-Aldrich, St. Louis, MO) was added to each sample as an internal standard and the sample was homogenized in a Branson 1510 Ultrasonic Cleaner (Branson-Emerson) at 50 ºC for 45 min.…”

Section: Sterol Analysismentioning

confidence: 99%

RNAi-mediated plant sterol modification: a novel strategy for controlling pest caterpillars

Chen

Grebenok

Zhao

et al. 2022

Preprint

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All eukaryotes use sterols as structural components in cell membranes and as precursors for key hormones. However, arthropods are unique among eukaryotes because they are unable to synthesize sterols de novo and must acquire sterols through their diet. Cholesterol is the dominant sterol in most insects, but because plants contain little cholesterol, most insect herbivores convert phytosterols to cholesterol. However, metabolic constraints limit which phytosterols insect herbivores can convert to cholesterol. In this study we used RNA interference to modify the sterol profile of Arabidopsis thaliana to generate phytosterols that would be problematic for insect herbivores. We did this by silencing the Δ8-Δ7-sterol isomerase gene (HYD1) that is responsible for the conversion of Δ8-sterols into Δ7-sterols. Sterol production decreased in Arabidopsis lines with > 95% transcript reduction and half of the total sterol profile in these plants showed a Δ8 configuration. These sterol-modified lines exhibited normal growth, but caterpillars (Plutella xylostella) reared on these plants showed reduced growth and survival, while adults showed decreased reproductive output. Sterol analysis of the pupae reared on sterol-modified plants suggests these negative effects are a function of reduced cholesterol levels and the accumulation of Δ8-sterols. Finally, we used our collective performance and reproduction data to model the effects of sterol-modified plants at the population level. We show that population numbers are significantly reduced, and generation time extended, after only two generations. Our results suggest that modifying plant sterols has real potential for management of pest caterpillars, especially multivoltine species.

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“…Myzus persicae, more commonly known as the green peach aphid (GPA), exhibits low reproduction and high mortality on tobacco (Nicotiana tabacum) that contain high levels of atypical sterols, which unlike cholesterol, the major sterol in aphids, lack double bonds in the sterol nucleus (Behmer et al, 2011). Also, GPA fecundity is lower on Arabidopsis thaliana mutants and transgenic lines that contain low levels of β-sitosterol than campesterol (Chen et al, 2020). Aphids lack the enzymatic machinery necessary for de novo synthesis of sterols, hence, presumably they can utilize plant-derived β-sitosterol but not atypical sterols to generate cholesterol (Behmer and Nes, 2003;Bouvaine et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Interplay between MYZUS PERSICAE-INDUCED LIPASE 1 and OPDA signaling in controlling green peach aphid infestation on Arabidopsis thaliana

Archer

Mondal

Behera

et al. 2022

Preprint

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MYZUS PERSICAE-INDUCED LIPASE1 (MPL1) encodes a lipase in Arabidopsis thaliana that is required for controlling infestation by the green peach aphid (GPA; Myzus persicae), an important phloem sap-consuming insect pest. Previously, we demonstrated that MPL1 expression was upregulated in response to GPA infestation, and GPA fecundity was higher on the mpl1 mutant, compared to the wild-type (WT), and lower on 35S:MPL1 plants that constitutively expressed MPL1 from the 35S promoter. Here, we show that the MPL1 promoter is active in the phloem and expression of the MPL1 coding sequence from the phloem-specific SUC2 promoter is sufficient to restore resistance to the GPA in the mpl1 mutant. The GPA infestation-associated upregulation of MPL1 requires CYCLOPHILIN 20-3 (CYP20-3), which encodes a 12-oxo-phytodienoic acid (OPDA)-binding protein that is involved in OPDA signaling and is required for controlling GPA infestation. OPDA promotes MPL1 expression to limit GPA fecundity, a process that requires CYP20-3 function. These results along with our observation that constitutive expression of MPL1 from the 35S promoter restores resistance to the GPA in the cyp20-3 mutant, and MPL1 feedbacks to limit OPDA levels in GPA-infested plants, suggest that an interplay between MPL1, OPDA, and CYP20-3 contributes to resistance to the GPA

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Aphid growth and reproduction on plants with altered sterol profiles: Novel insights using Arabidopsis mutant and overexpression lines

Cited by 9 publications

References 60 publications

Discrepancy in Sterol Usage between Two Polyphagous Caterpillars, Mythimna separata and Spodoptera frugiperda

Discrepancy in Sterol Usage between Two Polyphagous Caterpillars, Mythimna separata and Spodoptera frugiperda

RNAi-mediated plant sterol modification: a novel strategy for controlling pest caterpillars

Interplay between MYZUS PERSICAE-INDUCED LIPASE 1 and OPDA signaling in controlling green peach aphid infestation on Arabidopsis thaliana

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