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DMP8 and 9 regulate HAP2/GCS1 trafficking for the timely acquisition of sperm fusion competence

Wei Wang, Hanxian Xiong, Philipp Cyprys, Raphael Malka, María Flores‐Tornero, Peng Zhao, Xiongbo Peng, Stefanie Sprunck, Meng‐Xiang Sun

2022Proceedings of the National Academy of Sciences48 citationsDOIOpen Access PDF

Abstract

Sexual reproduction involves the fusion of two gametes of opposite sex. Although the sperm-expressed fusogen HAPLESS 2 (HAP2) or GENERATIVE CELL SPECIFIC 1 (GCS1) plays a vital role in this process in many eukaryotic organisms and an understanding of its regulation is emerging in unicellular systems [J. Zhang et al. , Nat. Commun. 12, 4380 (2021); J. F. Pinello et al. Dev. Cell 56, 3380–3392.e9 (2021)], neither HAP2/GCS1 interactors nor mechanisms for delivery and activation at the fusion site are known in multicellular plants. Here, we show that Arabidopsis thaliana HAP2/GCS1 interacts with two sperm DUF679 membrane proteins (DMP8 and DMP9), which are required for the EGG CELL 1 (EC1)-induced translocation of HAP2/GCS1 from internal storage vesicle to the sperm plasma membrane to ensure successful fertilization. Our studies in Arabidopsis and tobacco provide evidence for a conserved function of DMP8/9-like proteins as HAP2/GCS1 partner in seed plants. Our data suggest that seed plants evolved a DMP8/9-dependent fusogen translocation process to achieve timely acquisition of sperm fusion competence in response to egg cell–derived signals, revealing a previously unknown critical step for successful fertilization.

Topics & Concepts

BiologySpermEgg cellCell biologyLipid bilayer fusionFusion proteinArabidopsisGeneticsEvolutionary biologyGeneMembraneMutantRecombinant DNAPlant Reproductive BiologyPlant Molecular Biology ResearchPhotosynthetic Processes and Mechanisms