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

Abstract

Summary Nuclear male‐sterile mutants with non‐conditional, recessive and strictly monogenic inheritance are useful for both hybrid and conventional breeding systems, and have long been a research focus for many crops. In allohexaploid wheat, however, genic redundancy results in rarity of such mutants, with the ethyl methanesulfonate‐induced mutant ms5 among the few reported to date. Here, we identify TaMs5 as a glycosylphosphatidylinositol‐anchored lipid transfer protein required for normal pollen exine development, and by transgenic complementation demonstrate that TaMs5‐A restores fertility to ms5. We show ms5 locates to a centromere‐proximal interval and has a sterility inheritance pattern modulated by TaMs5‐D but not TaMs5‐B. We describe two allelic forms of TaMs5‐D, one of which is non‐functional and confers mono‐factorial inheritance of sterility. The second form is functional but shows incomplete dominance. Consistent with reduced functionality, transcript abundance in developing anthers was found to be lower for TaMs5‐D than TaMs5‐A. At the 3B homoeolocus, we found only non‐functional alleles among 178 diverse hexaploid and tetraploid wheats that include landraces and Triticum dicoccoides. Apparent ubiquity of non‐functional TaMs5‐B alleles suggests loss‐of‐function arose early in wheat evolution and, therefore, at most knockout of two homoeoloci is required for sterility. This work provides genetic information, resources and tools required for successful implementation of ms5 sterility in breeding systems for bread and durum wheats.

Identification and genetic diversity analysis of a male-sterile gene (MS1) in Japanese cedar (Cryptomeria japonicaD. Don)

“…In terms of protein structure, CJt020762 contains the signal peptide, plant lipid transfer protein domain, transmembrane domain, and the GPI anchor domain modification sites ( Figure 1). This structure is similar to ms1 and ms5 in wheat [28][29][30] . Furthermore, while the plant lipid transfer protein domain and transmembrane domain of CJt020762 may be necessary for pollen production in C. japonica, an analysis of mutant wheat revealed that both the lipid transfer protein domain and transmembrane domain of wheat ms1 were necessary for pollen production 29 .…”

“…The fifth and final supporting evidence stems from the functional and structural similarity of CJt020762 with wheat male-sterility genes. In wheat male-sterility (Triticum aestivum), both ms1 and ms5 possess recessive inheritance and single locus control, hence male-sterility is caused by the failure of exine development during microspore formation [27][28][29][30] . MS1 in C. japonica and ms1 and ms5 in wheat have similar male-sterility phenotypes.…”

Male Fertility Genes in Bread Wheat (Triticum aestivum L.) and Their Utilization for Hybrid Seed Production

“…Genetic studies and subsequent cloning of genes for many of these mutants has revealed these as either dominant mutations or mutations in genes with a predominant functional homeolog ( Table 1 ). ms1 and ms5 are two such recessive mutants where one genome predominantly contributes to gene function [ 25 , 27 , 31 ]. ms1a mutant was the first male sterile mutant reported in wheat [ 48 ].…”

The Major Factors Causing the Microspore Abortion of Genic Male Sterile Mutant NWMS1 in Wheat (Triticum aestivum L.)

“…There are seven alleles on Ms1 locus: ms1a, ms1b, ms1c, ms1d, ms1e, ms1f, and ms1g [23,24]. Three genes-Ms1, Ms2, and Ms5-have been cloned; Ms1 and Ms5 encode a glycosylphosphatidylinositol (GPI)-anchored lipid transfer protein and Ms2 encodes an orphan protein [25][26][27][28]. The Ms1 is required for microgametogenesis in wheat.…”

“…Knockout of Ms1 generates male-sterile lines [29]. Wheat ms5 male sterility is induced by recessive homoeologous A and D genome non-specific lipid transfer proteins [28]. Only the Ms2 mutant is currently widely used in wheat breeding [27].…”