Chitin Deacetylase Gene Family Positively Regulates the Accumulation of Rice Stripe Virus in Laodelphax striatellus Fallén (Hemiptera: Delphacidae) Ovaries

TL;DR

This study shows that a specific chitin deacetylase gene in a rice pest helps the virus accumulate in its ovaries and supports pest reproduction.

Contribution

The study reveals a novel role of LsCDA1 in promoting rice stripe virus accumulation and insect reproduction.

Findings

RSV infection increases LsCDA1 and LsCDA2 expression in the pest.

LsCDA1 interacts with RSV proteins and enhances viral accumulation in ovaries.

Inhibiting LsCDA1 reduces virus levels and pest reproduction.

Abstract

Laodelphax striatellus Fallén (Hemiptera: Delphacidae), the small brown planthopper (SBPH), transmits the rice stripe virus (RSV), causing substantial losses in rice production. In this study, we identified four Chitin deacetylase genes (LsCDA1~LsCDA4) from the genome of SBPH. RSV infection increased the expression of LsCDA1 and LsCDA2 in SBPH. Additionally, RSV enhanced the expression of LsCDA1 in SBPH ovaries. The direct interaction between LsCDA1 and RSV proteins NP and NS2 was demonstrated. The inhibition of LsCDA1 expression decreased viral accumulation in SBPH ovaries by regulating vitellogenin receptor (VgR) expression and completely suppressed SBPH reproduction. These results indicate that LsCDA1 positively regulates RSV accumulation in the ovaries and SBPH reproduction by altering VgR expression.

Chitin deacetylase modifies chitin and has critical functions in the growth and development of insects; however, whether it has other roles is unclear. Laodelphax striatellus not only directly feeds on the phloem sap of rice but also transmits RSV, leading to significant losses in rice production. In this study, four CDA genes were identified based on SBPH genomic data and were classified into groups I and III based on a phylogenetic analysis. The expression of LsCDA1 and LsCDA2 in RSV-infected SBPH was increased by 282% and 159%, respectively, relative to the non-infected SBPH control. Additionally, RSV enhanced the expression of LsCDA1 (increased by 194%) in the ovaries. Yeast two-hybrid and glutathione-S-transferase pull-down assays demonstrated the interaction between LsCDA1 and RSV proteins NP and NS2. Furthermore, the knockdown of LsCDA1 expression decreased viral loads in RSV-infected SBPH and its ovaries by 66% and 72% relative to the dsGFP control. Silencing LsCDA1 significantly decreased VgR expression in SBPH and its ovaries and reduced fecundity. These results indicate that LsCDA1 positively regulates RSV accumulation in the ovaries and SBPH reproduction by modulating VgR expression, which offers a novel strategy for controlling both RSV and SBPH by targeting LsCDA1.

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