Plasma membrane H+-ATPase overexpression increases rice yield via simultaneous enhancement of nutrient uptake and photosynthesis

Maoxing Zhang,Yosuke Toda,Yin Wang,Shiwei Guo,Ming Ding,Liang Xiao,Xin Xiao,Yuya Kawai,Guohua Xu,Qirong Shen,Toshinori Kinoshita,Takamasa Suzuki,Houqing Zeng,Yuji Hayashi ,Xi Chen,Feng Yan,Wenxiu Ye,Jin Xu,Feiyun Xu,Yiyong Zhu

doi:10.1038/s41467-021-20964-4

Abstract

Nitrogen (N) and carbon (C) are essential elements for plant growth and crop yield. Thus, improved N and C utilisation contributes to agricultural productivity and reduces the need for fertilisation. In the present study, we find that overexpression of a single rice gene, Oryza sativa plasma membrane (PM) H+-ATPase 1 (OSA1), facilitates ammonium absorption and assimilation in roots and enhanced light-induced stomatal opening with higher photosynthesis rate in leaves. As a result, OSA1 overexpression in rice plants causes a 33% increase in grain yield and a 46% increase in N use efficiency overall. As PM H+-ATPase is highly conserved in plants, these findings indicate that the manipulation of PM H+-ATPase could cooperatively improve N and C utilisation, potentially providing a vital tool for food security and sustainable agriculture.

Highlights

Nitrogen (N) and carbon (C) are essential elements for plant growth and crop yield
Increasing crop yield by improving N use efficiency (NUE) and C fixation is important for sustainable agriculture and environment performance
We demonstrated the critical role of the plasma membrane (PM) H+-ATPase gene OSA1 in controlling both NUE and photosynthesis in paddy rice production

Summary

Introduction

Nitrogen (N) and carbon (C) are essential elements for plant growth and crop yield. improved N and C utilisation contributes to agricultural productivity and reduces the need for fertilisation. We find that overexpression of a single rice gene, Oryza sativa plasma membrane (PM) H+-ATPase 1 (OSA1), facilitates ammonium absorption and assimilation in roots and enhanced light-induced stomatal opening with higher photosynthesis rate in leaves. Overexpression of the PM H+-ATPase in guard cells significantly enhances stomatal opening, photosynthesis and, subsequently, growth in Arabidopsis thaliana, a model plant[11] It remains unknown if this manipulation would be efficient in crops, such as rice, which is the staple food for three billion people worldwide[12]. We examined the involvement of PM H+-ATPase in NH4+ uptake by rice roots and stomatal opening for CO2 uptake and photosynthesis in rice leaves, with the aim of developing a new strategy to improve rice yield and N use efficiency (NUE) via the overexpression of a single gene, Oryza sativa PM H+-ATPase 1 (OSA1)

Methods

Results

Conclusion