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Journal of Integrative Agriculture  2024, Vol. 23 Issue (3): 938-947    DOI: 10.1016/j.jia.2023.06.019
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Silencing transformer and transformer-2 in Zeugodacus cucurbitae causes defective sex determination with inviability of most pseudomales

Qin Ma1*, Zizhen Fan2*, Ping Wang1*, Siya Ma2, Jian Wen1, Fengqin Cao1, 3, Xianwu Lin1#, Rihui Yan1, 3#

1 Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests of Ministry of Education, School of Plant Protection, Hainan University, Haikou 570228, China

2 School of Life Sciences, Hainan University, Haikou 570228, China 

3 Hainan Yazhou Bay Seed Lab, Sanya 572000, China

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摘要  

在双翅目昆虫中,transformer是调控性别决定的开关基因,与在两性中均表达的transformer-2基因共同调节雌雄分化。然而,双翅目害虫瓜实蝇作为世界上广泛分布的重要农业害虫,其性别决定调控机制目前仍未阐明。本文研究发现,在胚胎早期通过RNA干扰下调transformertransformer-2表达能够显著减少雌性比例;在由抑制了transformertransformer-2表达的胚胎发育而成的雄虫中,大部分都能与雌虫交配并产生雌雄混合的正常后代,仅有一只雄虫在与雌虫交配后产生全雌后代,同时有少部分雄虫因不能与雌虫交配而无法产生后代。通过检测Y染色体连锁基因Maleness-on-the-Y发现,这些无法产生后代或后代性比异常的雄虫均是基因型为XX的假雄虫。性比数据和杂交实验结合分析表明,大部分的XX假雄虫无法存活。本研究结果表明transformertransformer-2是瓜实蝇雌性发育所必需的,并在性别决定中起着关键作用。我们的研究结果将有助于理解瓜实蝇性别决定机制,并开发用于生物防治的遗传性别品系提供思路



Abstract  
transformer is a switch gene for sex determination in many insects, which cooperates with transformer-2 that is expressed in both sexes to regulate female differentiation, particularly in dipterans.  Zeugodacus cucurbitae (Coquillett) is a very destructive pest worldwide, however, its sex determination pathway remains largely uncharacterized.  Here, we show that the female sex ratio is sharply reduced with knockdown of either transformer or transformer-2 by RNA interference in early embryos of Zcucurbitae.  Most of the males grown from the embryos with transient transformer and transformer-2 suppression mated with wild-type females and produced mixed sex progeny, with one exception that produced only female progeny, and all of the few remaining males failed to mate with wild-type females and produced no progeny.  The exceptional male and those males with mating failure were XX pseudomales as determined by the detection of Y chromosome-linked Maleness-on-the-Y, indicating that most XX pseudomales are not viable.  The phenotypes of transformer and transformer-2 suggest that they play a key role in regulating sex determination and are required for female sexual development of Zcucurbitae.  Our results will be beneficial to the understanding of sex determination in Zcucurbitae and can facilitate the development of genetic sexing strains for its biological control.



Keywords:  Zeugodacus cucurbitae        transformer        transformer-2        sex determination        RNA interference        biological control   
Received: 22 February 2023   Accepted: 04 May 2023
Fund: 

This work was supported by the Hainan Provincial Natural Science Foundation of China (321CXTD435), the National Natural Science Foundation of China (31860523, 31660339, 31702059, and 32260665), and the National Key R&D Program of China (2022YFC2601400).

About author:  #Correspondence Xianwu Lin, Tel: +86-898-66256215, E-mail: linxianw@hainanu.edu.cn; Rihui Yan, Tel: +86-898-66275675, E-mail: ryan1@hainanu.edu.cn * These authors contributed equally to this study.

Cite this article: 

Qin Ma, Zizhen Fan, Ping Wang, Siya Ma, Jian Wen, Fengqin Cao, Xianwu Lin, Rihui Yan. 2024.

Silencing transformer and transformer-2 in Zeugodacus cucurbitae causes defective sex determination with inviability of most pseudomales . Journal of Integrative Agriculture, 23(3): 938-947.

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