Investigation of the Association between the Energy Metabolism of the Insect Vector Laodelphax striatellus and Rice Stripe Virus (RSV)

Viruses. 2022 Oct 19;14(10):2298. doi: 10.3390/v14102298.

Abstract

Viruses, as intracellular parasites, rely on the host organism to complete their life cycle. Although over 70% of plant viruses are transmitted by insect vectors, the role of vector energy metabolism on the infection process of insect-borne plant viruses is unclear. In this study, full-length cDNAs of three energy metabolism-related genes (LsATPase, LsMIT13 and LsNADP-ME) were obtained from the small brown planthopper (SBPH, Laodelphax striatellus), which transmits the Rice stripe virus (RSV). Expression levels of LsATPase, LsMIT13 and LsNADP-ME increased by 105%, 1120% and 259%, respectively, due to RSV infection. The repression of LsATPase, LsMIT13 or LsNADP-ME by RNAi had no effect on RSV nucleocapsid protein (NP) transcripts or protein levels. The repression of LsATPase caused a significant increase in LsMIT13 and LsNADP-ME transcript levels by 230% and 217%, respectively, and the repression of LsMIT13 caused a significant increase in LsNADP-ME mRNA levels. These results suggested that the silencing of LsATPase induced compensatory upregulation of LsMIT13 and LsNADP-ME, and silencing LsMIT13 induced compensatory upregulation of LsNADP-ME. Further study indicated that the co-silencing of LsATPase, LsMIT13 and LsNADP-ME in viruliferous SBPHs increased ATP production and RSV loads by 182% and 117%, respectively, as compared with nonviruliferous SBPHs. These findings indicate that SBPH energy metabolism is involved in RSV infection and provide insight into the association between plant viruses and energy metabolism in the insect vector.

Keywords: ATP synthase; Laodelphax striatellus; NAD-dependent malic enzyme; RSV; energy metabolism; mitochondrial import inner membrane translocases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Animals
  • Energy Metabolism
  • Hemiptera* / physiology
  • Insect Vectors
  • Nucleocapsid Proteins / metabolism
  • Oryza*
  • Plant Diseases
  • Plant Viruses* / genetics
  • RNA, Messenger / genetics
  • Tenuivirus* / genetics

Substances

  • RNA, Messenger
  • Nucleocapsid Proteins
  • Adenosine Triphosphate

Grants and funding

This research was funded by the National Natural Science Foundation of China grant numbers 31801732; 31701786; 32272533; 32272637.