Pleiotropic Functions of <i>FoxN1</i>: Regulating Different Target Genes during Embryogenesis and Nymph Molting in the Brown Planthopper

<i>FoxN1</i> gene belongs to the forkhead box gene family that comprises a diverse group of “winged helix” transcription factors that have been implicated in a variety of biochemical and cellular processes. In the brown planthopper (BPH), <i>FoxN1</i> is highly expressed in t...

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Main Authors: Yu-Xuan Ye, Chuan-Xi Zhang
Format: Article
Language:English
Published: MDPI AG 2020-06-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/21/12/4222
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spelling doaj-945a762f96a14f4fa4c1bd2618a24f172020-11-25T03:27:41ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-06-01214222422210.3390/ijms21124222Pleiotropic Functions of <i>FoxN1</i>: Regulating Different Target Genes during Embryogenesis and Nymph Molting in the Brown PlanthopperYu-Xuan Ye0Chuan-Xi Zhang1Institute of Insect Science, Zhejiang University, Hangzhou 310058, ChinaInstitute of Insect Science, Zhejiang University, Hangzhou 310058, China<i>FoxN1</i> gene belongs to the forkhead box gene family that comprises a diverse group of “winged helix” transcription factors that have been implicated in a variety of biochemical and cellular processes. In the brown planthopper (BPH), <i>FoxN1</i> is highly expressed in the ovaries and newly laid eggs, where it acted as an indispensable gene through its molecular targets to regulate early embryonic development. Moreover, the results of the RNAi experiments indicated that <i>Nilaparvata</i><i> </i><i>lugens</i> <i>FoxN1</i> (<i>NlFoxN1</i>) exhibited pleiotropism: they not only affected the embryogenesis, but also played an important role in molting. RNA-seq and RNAi were further used to reveal potential target genes of <i>NlFox</i><i>N1</i> in different stages. In the eggs, ten downregulated genes were defined as potential target genes of <i>NlFox</i><i>N1</i> because of the similar expression patterns and functions with <i>NlFoxN1</i>. Knockdown of <i>NlFox</i><i>N1</i> or any of these genes prevented the development of the eggs, resulting in a zero hatchability. In the nymphs, <i>Nl</i><i>FoxN1</i> regulated the expression of a keratin gene, type I cytoskeletal keratin 9 (<i>NlKrt9</i>), to participate in the formation of an intermediate filament framework. Depletion of <i>Nl</i><i>FoxN1</i> or <i>NlKrt9</i> in nymphs, BPHs failed to shed their old cuticle during nymph-to-nymph or nymph-to-adult molting and the mortality was almost 100%. Altogether, the pleiotropic roles of<i> Nl</i><i>FoxN1</i> during embryogenesis and nymph molting were supported by the ability to coordinate the temporal and spatial gene expression of their target genes.https://www.mdpi.com/1422-0067/21/12/4222FoxN1brown planthopperpleiotropismembryogenesiskeratin gene
collection DOAJ
language English
format Article
sources DOAJ
author Yu-Xuan Ye
Chuan-Xi Zhang
spellingShingle Yu-Xuan Ye
Chuan-Xi Zhang
Pleiotropic Functions of <i>FoxN1</i>: Regulating Different Target Genes during Embryogenesis and Nymph Molting in the Brown Planthopper
International Journal of Molecular Sciences
FoxN1
brown planthopper
pleiotropism
embryogenesis
keratin gene
author_facet Yu-Xuan Ye
Chuan-Xi Zhang
author_sort Yu-Xuan Ye
title Pleiotropic Functions of <i>FoxN1</i>: Regulating Different Target Genes during Embryogenesis and Nymph Molting in the Brown Planthopper
title_short Pleiotropic Functions of <i>FoxN1</i>: Regulating Different Target Genes during Embryogenesis and Nymph Molting in the Brown Planthopper
title_full Pleiotropic Functions of <i>FoxN1</i>: Regulating Different Target Genes during Embryogenesis and Nymph Molting in the Brown Planthopper
title_fullStr Pleiotropic Functions of <i>FoxN1</i>: Regulating Different Target Genes during Embryogenesis and Nymph Molting in the Brown Planthopper
title_full_unstemmed Pleiotropic Functions of <i>FoxN1</i>: Regulating Different Target Genes during Embryogenesis and Nymph Molting in the Brown Planthopper
title_sort pleiotropic functions of <i>foxn1</i>: regulating different target genes during embryogenesis and nymph molting in the brown planthopper
publisher MDPI AG
series International Journal of Molecular Sciences
issn 1661-6596
1422-0067
publishDate 2020-06-01
description <i>FoxN1</i> gene belongs to the forkhead box gene family that comprises a diverse group of “winged helix” transcription factors that have been implicated in a variety of biochemical and cellular processes. In the brown planthopper (BPH), <i>FoxN1</i> is highly expressed in the ovaries and newly laid eggs, where it acted as an indispensable gene through its molecular targets to regulate early embryonic development. Moreover, the results of the RNAi experiments indicated that <i>Nilaparvata</i><i> </i><i>lugens</i> <i>FoxN1</i> (<i>NlFoxN1</i>) exhibited pleiotropism: they not only affected the embryogenesis, but also played an important role in molting. RNA-seq and RNAi were further used to reveal potential target genes of <i>NlFox</i><i>N1</i> in different stages. In the eggs, ten downregulated genes were defined as potential target genes of <i>NlFox</i><i>N1</i> because of the similar expression patterns and functions with <i>NlFoxN1</i>. Knockdown of <i>NlFox</i><i>N1</i> or any of these genes prevented the development of the eggs, resulting in a zero hatchability. In the nymphs, <i>Nl</i><i>FoxN1</i> regulated the expression of a keratin gene, type I cytoskeletal keratin 9 (<i>NlKrt9</i>), to participate in the formation of an intermediate filament framework. Depletion of <i>Nl</i><i>FoxN1</i> or <i>NlKrt9</i> in nymphs, BPHs failed to shed their old cuticle during nymph-to-nymph or nymph-to-adult molting and the mortality was almost 100%. Altogether, the pleiotropic roles of<i> Nl</i><i>FoxN1</i> during embryogenesis and nymph molting were supported by the ability to coordinate the temporal and spatial gene expression of their target genes.
topic FoxN1
brown planthopper
pleiotropism
embryogenesis
keratin gene
url https://www.mdpi.com/1422-0067/21/12/4222
work_keys_str_mv AT yuxuanye pleiotropicfunctionsofifoxn1iregulatingdifferenttargetgenesduringembryogenesisandnymphmoltinginthebrownplanthopper
AT chuanxizhang pleiotropicfunctionsofifoxn1iregulatingdifferenttargetgenesduringembryogenesisandnymphmoltinginthebrownplanthopper
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