A single point mutation in Ms44 results in dominant male sterility and improves nitrogen use efficiency in maize

Abstract

SummaryApplication of nitrogen fertilizer in the past 50 years has resulted in significant increases in crop yields. However, loss of nitrogen from crop fields has been associated with negative impacts on the environment. Developing maize hybrids with improved nitrogen use efficiency is a cost‐effective strategy for increasing yield sustainably. We report that a dominant male‐sterile mutant Ms44 encodes a lipid transfer protein which is expressed specifically in the tapetum. A single amino acid change from alanine to threonine at the signal peptide cleavage site of the Ms44 protein abolished protein processing and impeded the secretion of protein from tapetal cells into the locule, resulting in dominant male sterility. While the total nitrogen (N) content in plants was not changed, Ms44 male‐sterile plants reduced tassel growth and improved ear growth by partitioning more nitrogen to the ear, resulting in a 9.6% increase in kernel number. Hybrids carrying the Ms44 allele demonstrated a 4%–8.5% yield advantage when N is limiting, 1.7% yield advantage under drought and 0.9% yield advantage under optimal growth conditions relative to the yield of wild type. Furthermore, we have developed an Ms44 maintainer line for fertility restoration, male‐sterile inbred seed increase and hybrid seed production. This study reveals that protein secretion from the tapetum into the locule is critical for pollen development and demonstrates that a reduction in competition between tassel and ear by male sterility improves grain yield under low‐nitrogen conditions in maize.

Genetic Male Sterility (Ms44) Increases Maize Grain Yield

“…However, it is difficult to explain how Ms44 could elicit a change in plant growth rate. Male sterility, caused by Ms44 , is the result of a single‐nucleotide polymorphism (SNP) causing an error in the splicing of the targeting peptide of a lipid transfer protein expressed exclusively in the tapetum for a short period of time after tetrad release (Fox et al, 2017). It is inconceivable how this gene function could be associated with an increase in whole‐plant growth rate or biomass.…”

“…Deployment of GMS hybrid technology through a blended hybrid is feasible through the use of a maintainer inbred line (Fox et al, 2017). This system provides an efficient, commercial process for seed production, reducing the labor input required for detasseling.…”

“…In contrast, the dominant GMS, Ms44 (Albertsen and Trimnell, 1992), makes testing GMS hybrids more feasible, since the source of male sterility must be incorporated into only one parent to obtain a 1:1 segregating male sterile hybrid. Combining the use of a dominant male sterile such as Ms44 with the development of a maintainer line similar to the maintainer described by Wu et al (2015) may be used to generate fully male sterile hybrids (Fox et al, 2017). In this report, we tested the hypothesis that GMS genes reduce competition between the developing tassel and ear, leading to improved ear development and ultimately to increased grain yield, especially under limited N or drought stress.…”

Wheat ms5 male‐sterility is induced by recessive homoeologous A and D genome non‐specific lipid transfer proteins

“…A key requirement for implementation of GMS hybrid production systems is a DNA sequence capable of fully restoring fertility to a line that is male-sterile due to a single locus that is either recessive in inheritance or which can be rendered recessive by inhibition (Fox et al, 2017). Fertile pollen is the result of a complex, conserved developmental process, and disturbance in any of the numerous responsible genes may result in male-sterility that is suitable for exploitation in breeding systems.…”

Construction of a multicontrol sterility system for a maize male‐sterile line and hybrid seed production based on the ZmMs7 gene encoding a PHD‐finger transcription factor

“…Since the first transgenic male sterility system was described (Mariani et al, 1990), many strategies to produce male-sterile plants have been reported,including chemical inducible male sterility systems (Feng et al, 2014;Singh et al, 2010;Venkatesh et al, 2014), transgenic maintainer systems (Chang et al, 2016;Fox et al, 2017;Perez-Prat and van Lookeren Campagne, 2002;Williams, 1995;Wu et al, 2016) and other biotechnology-based systems (Gils et al, 2008;Millwood et al, 2016;Mitsuda et al, 2006). Among them, the strategy of using transgenic maintainer lines to propagate nuclear male-sterile plants is more desirable and reliable.…”