Tonoplast proton pumps regulate nuclear spacing of female gametophytes via mediating polar auxin transport in Arabidopsis

Front Plant Sci. 2022 Sep 13:13:1006735. doi: 10.3389/fpls.2022.1006735. eCollection 2022.

Abstract

The vacuole is an important organelle with multiple functions in plants, and the tonoplast that wraps the vacuole also plays essential roles in intracellular trafficking and ion homeostasis. Previous studies found that tonoplast proton pumps regulate embryo development and morphogenesis through their effects on vacuole biogenesis and distribution, as well as polar auxin transport and concomitant auxin gradient. However, the precise roles of the tonoplast proton pumps in gametophyte development remain unclear. Here we demonstrated that the lack of two types of tonoplast proton pumps or the absence of V-ATPase alone leads to abnormal development and nuclear localization of female gametophyte (FG), and slowed endosperm nuclei division after fertilization of the central cell. We further revealed that V-ATPase regulates auxin levels in ovules through coordinating the content and localization of PIN-FORMED 1 (PIN1) protein, hence influencing nuclear spacing between centra cell and egg cell, and subsequent endosperm development. Collectively, our findings revealed a crucial role of V-ATPase in auxin-mediated FG development in Arabidopsis and expanded our understanding of the functions of tonoplast proton pumps in seed plants reproductive development.

Keywords: V-ATPase; central cell; egg cell; endosperm; female gametophyte; plant vacuole.

Grants and funding

This research was supported by the National Natural Science Foundation of China (32070342 and 32000222), the National Basic Research Program of China (grant no. 2014CB943404), Shanghai Jiao Tong University JiRLMDS Joint Research Fund (Project MDS-JF-2020-8), the Agri-X Interdisciplinary Fund of Shanghai Jiao Tong University (Agri-X20200204 and Agri-X2017006), the Bio-X Interdisciplinary Fund of Shanghai Jiao Tong University (20CX-04), the Scientific and Technological Innovation Funds of Shanghai Jiao Tong University (19×160020009), Grant-in-Aid for Scientific Research (B) (JP16H04803), and Grant-in-Aid for Scientific Research on Innovative Areas (JP25113002 and JP18H05487).