The histone deacetylase NlHDAC1 regulates both female and male fertility in the brown planthopper, Nilaparvata lugens

Histone acetylation is a specific type of chromatin modification that serves as a key regulatory mechanism for many cellular processes in mammals. However, little is known about its biological function in invertebrates. Here, we identified 12 members of histone deacetylases (NlHDACs) in the brown planthopper (BPH), Nilaparvata lugens. RNAi-mediated silencing assay showed that NlHdac1, NlHdac3 and NlHdac4 played critical roles in female fertility via regulating ovary maturation or ovipositor development. Silencing of NlHdac1 substantially increased acetylation level of histones H3 and H4 in ovaries, indicating NlHDAC1 is the main histone deacetylase in ovaries of BPH. RNA sequencing (RNA-seq) analysis showed that knockdown of NlHdac1 impaired ovary development via multiple signalling pathways including the TOR pathway. Acoustic recording showed that males with NlHdac1 knockdown failed to make courtship songs, and thus were unacceptable to wild-type females, resulting in unfertilized eggs. Competition mating assay showed that wild-type females overwhelmingly preferred to mate with control males over NlHdac1-knockdown males. These findings improve our understanding of reproductive strategies controlled by HDACs in insects and provide a potential target for pest control.


Is the length of the paper justified? Yes
Should the paper be seen by a specialist statistical reviewer? No Is it clear how to make all supporting data available? Yes

Do you have any ethical concerns with this paper? No
Comments to the Author This is a fairly straight forward research. Although the idea is not completely novel, the testing is exhaustive and robust. The methodology, for the most part, is clear. The flow and organization of the manuscript are acceptable, albeit it needs to be streamlined. Also, authors could improve the phenotypic impact part of the research by quantifying the mating behavior with statistical power to go with the existing schematic drawings ( Figure 10) and the acoustic/auditory profiles ( Figure  11). Finally, this manuscript will benefit from more thorough English editing. The detailed comments and suggestions to improve the manuscript are provided in the attached PDF. Comments to the Author Zhang and coworkers identified several genes encoding histone deacetylase in Nilaparvata lugens. They study the function of NlHDAC1, NlHDAC3, and NlHDAC4, which are involved in female fertility. They show that NlHDAC1 is likely the main histone deacetylase in ovaries. They demostrate the function of NlHDAC1 using a varity of approcaches, from RNA-seq analysis to behavioral studies. Their investigation has been thoroughly performed and describe in detail the different phenotypes of NlHDAC1. It is an excellent manuscript exhaustively covering a phenotype with potential for pest control. The only criticisms I would raise is that the results show the effect of a pleiotropic gene, as expected by an overall regulator of chromatin function. Therefore, it is difficult to claim that a particular pathway is affected when the RNAseq experiments shows an effect in thousand of genes. I would suggest the authors to consider this point in the discussion, rather than listing all pathways possibly involved.

29-Oct-2018
Dear Dr Xu We are pleased to inform you that your manuscript RSOB-18-0158 entitled "The histone deacetylase NlHDAC1 regulates both female and male fertility in the brown planthopper, Nilaparvata lugens" has been accepted by the Editor for publication in Open Biology. The reviewer(s) have recommended publication, but also suggest some minor revisions to your manuscript. Therefore, we invite you to respond to the reviewer(s)' comments and revise your manuscript.
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Online supplementary material will also carry the title and description provided during submission, so please ensure these are accurate and informative. Note that the Royal Society will not edit or typeset supplementary material and it will be hosted as provided. Please ensure that the supplementary material includes the paper details (authors, title, journal name, article DOI Comments to the Author(s) This is a fairly straight forward research. Although the idea is not completely novel, the testing is exhaustive and robust. The methodology, for the most part, is clear. The flow and organization of the manuscript are acceptable, albeit it needs to be streamlined. Also, authors could improve the phenotypic impact part of the research by quantifying the mating behavior with statistical power to go with the existing schematic drawings ( Figure 10) and the acoustic/auditory profiles ( Figure  11). Finally, this manuscript will benefit from more thorough English editing. The detailed comments and suggestions to improve the manuscript are provided in the attached PDF.
Referee: 2 Comments to the Author(s) Zhang and coworkers identified several genes encoding histone deacetylase in Nilaparvata lugens. They study the function of NlHDAC1, NlHDAC3, and NlHDAC4, which are involved in female fertility. They show that NlHDAC1 is likely the main histone deacetylase in ovaries. They demostrate the function of NlHDAC1 using a varity of approcaches, from RNA-seq analysis to behavioral studies. Their investigation has been thoroughly performed and describe in detail the different phenotypes of NlHDAC1. It is an excellent manuscript exhaustively covering a phenotype with potential for pest control. The only criticisms I would raise is that the results show the effect of a pleiotropic gene, as expected by an overall regulator of chromatin function. Therefore, it is difficult to claim that a particular pathway is affected when the RNAseq experiments shows an effect in thousand of genes. I would suggest the authors to consider this point in the discussion, rather than listing all pathways possibly involved.

09-Nov-2018
Dear Dr Xu We are pleased to inform you that your manuscript entitled "The histone deacetylase NlHDAC1 regulates both female and male fertility in the brown planthopper, Nilaparvata lugens" has been accepted by the Editor for publication in Open Biology.
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