干旱区生态环境知识资源中心(Arid): NHA1 is a cation/proton antiporter essential for the water-conserving functions of the rectal complex in Tribolium castaneum

Arid

DOI	10.1073/pnas.2217084120
	NHA1 is a cation/proton antiporter essential for the water-conserving functions of the rectal complex in Tribolium castaneum
	Naseem, Muhammad T.; Beaven, Robin; Koyama, Takashi; Naz, Sehrish; Su, Sheng-yuan; Leader, David P.; Klaerke, Dan A.; Calloe, Kirstine; Denholm, Barry; Halberg, Kenneth V.
通讯作者	Halberg, KV
来源期刊	PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
ISSN	0027-8424
EISSN	1091-6490
出版年	2023
卷号	120 期号:13
英文摘要	More than half of all extant metazoan species on earth are insects. The evolutionary success of insects is linked with their ability to osmoregulate, suggesting that they have evolved unique physiological mechanisms to maintain water balance. In beetles (Coleoptera)-the largest group of insects-a specialized rectal (cryptonephridial) complex has evolved that recovers water from the rectum destined for excretion and recycles it back to the body. However, the molecular mechanisms underpinning the remarkable water-conserving functions of this system are unknown. Here, we introduce a transcriptomic resource, BeetleAtlas.org, for the exceptionally desicca-tion-tolerant red flour beetle Tribolium castaneum, and demonstrate its utility by identifying a cation/H+ antiporter (NHA1) that is enriched and functionally signifi-cant in the Tribolium rectal complex. NHA1 localizes exclusively to a specialized cell type, the leptophragmata, in the distal region of the Malpighian tubules associated with the rectal complex. Computational modeling and electrophysiological characteri-zation in Xenopus oocytes show that NHA1 acts as an electroneutral K+/H+ antiporter. Furthermore, genetic silencing of Nha1 dramatically increases excretory water loss and reduces organismal survival during desiccation stress, implying that NHA1 activ-ity is essential for maintaining systemic water balance. Finally, we show that Tiptop, a conserved transcription factor, regulates NHA1 expression in leptophragmata and controls leptophragmata maturation, illuminating the developmental mechanism that establishes the functions of this cell. Together, our work provides insights into the molecular architecture underpinning the function of one of the most powerful water-conserving mechanisms in nature, the beetle rectal complex.SignificanceBeetles are the largest group of animals on earth. Unique adaptations in overcoming water stress is critical to their success in arid areas, yet the mechanisms underpinning this ability are unknown. Using genetics and electrophysiological studies, we show that a cation/H+ (NHA1) transporter is exclusively localized to specialized leptophragmata cells in the Malpighian tubules associated with the rectal complex. Ion transport by NHA1 in leptophragmata underpins the movement of water from the rectum to recycle it back to the body, and is essential for maintaining systemic water balance in beetles. This work provides insights into the molecular architecture of one of the most powerful water -conservation mechanisms in biology, and provides an important clue to the evolutionary success of the beetles.
英文关键词	rectal complex Tribolium castaneum cation H plus antiporter genetics secondary cell
类型	Article
语种	英语
开放获取类型	Green Submitted, Green Accepted, Green Published, hybrid
收录类别	SCI-E
WOS记录号	WOS:000964476900004
WOS关键词	MALPIGHIAN TUBULES ; VAPOR ABSORPTION ; TENEBRIO-MOLITOR ; RNA-SEQ ; EXPRESSION ; TRANSPORT ; MEALWORM ; LARVAE ; GENE ; DIFFERENTIATION
WOS类目	Multidisciplinary Sciences
WOS研究方向	Science & Technology - Other Topics
资源类型	期刊论文
条目标识符	http://119.78.100.177/qdio/handle/2XILL650/398164
推荐引用方式 GB/T 7714	Naseem, Muhammad T.,Beaven, Robin,Koyama, Takashi,et al. NHA1 is a cation/proton antiporter essential for the water-conserving functions of the rectal complex in Tribolium castaneum[J],2023,120(13).
APA	Naseem, Muhammad T..,Beaven, Robin.,Koyama, Takashi.,Naz, Sehrish.,Su, Sheng-yuan.,...&Halberg, Kenneth V..(2023).NHA1 is a cation/proton antiporter essential for the water-conserving functions of the rectal complex in Tribolium castaneum.PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA,120(13).
MLA	Naseem, Muhammad T.,et al."NHA1 is a cation/proton antiporter essential for the water-conserving functions of the rectal complex in Tribolium castaneum".PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 120.13(2023).