<i>ZmMs25</i> encoding a plastid-localized fatty acyl reductase is critical for anther and pollen development in maize

Zhang, Simiao; Shu, Wu; Niu, Canfang; Liu, Dongcheng; Yan, Tingwei; Tian, Youhui; Liu, Shuangshuang; Xie, Kui; Li, Ziwen; Li, Han; Zhao, Wei; Dong, Zhenying; Zhu, Taotao; Hou, Quancan; Ma, Biao; An, Xianghai; Li, Jinping; Wan, Xiangyuan

doi:10.1093/jxb/erab142

Cited by 35 publications

(33 citation statements)

References 71 publications

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“…In bread wheat ( Triticum aestivum L.), TaTAA1 encoded by Triticum aestivum anther 1 was the first reported alcohol-forming fatty acyl–CoA reductase responsible for male gametophyte development [ 39 ]. In maize, ZmMs6021/ZmMs25 [ 40 , 41 ] encoded a fatty acyl–ACP reductase and was directly activated and regulated by ZmMYB84, which is an MYB TF ortholog of AtMYB80 and OsMYB80 [ 41 ]. Even though the major catalytic steps of FARs in lipid biosynthesis have been revealed, our knowledge on the function and regulation of FAR family members involved in plant male reproduction is still limited.…”

Section: Introductionmentioning

confidence: 99%

ZmFAR1 and ZmABCG26 Regulated by microRNA Are Essential for Lipid Metabolism in Maize Anther

Jiang

Liu

et al. 2021

IJMS

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The function and regulation of lipid metabolic genes are essential for plant male reproduction. However, expression regulation of lipid metabolic genic male sterility (GMS) genes by noncoding RNAs is largely unclear. Here, we systematically predicted the microRNA regulators of 34 maize white brown complex members in ATP-binding cassette transporter G subfamily (WBC/ABCG) genes using transcriptome analysis. Results indicate that the ZmABCG26 transcript was predicted to be targeted by zma-miR164h-5p, and their expression levels were negatively correlated in maize B73 and Oh43 genetic backgrounds based on both transcriptome data and qRT-PCR experiments. CRISPR/Cas9-induced gene mutagenesis was performed on ZmABCG26 and another lipid metabolic gene, ZmFAR1. DNA sequencing, phenotypic, and cytological observations demonstrated that both ZmABCG26 and ZmFAR1 are GMS genes in maize. Notably, ZmABCG26 proteins are localized in the endoplasmic reticulum (ER), chloroplast/plastid, and plasma membrane. Furthermore, ZmFAR1 shows catalytic activities to three CoA substrates in vitro with the activity order of C12:0-CoA > C16:0-CoA > C18:0-CoA, and its four key amino acid sites were critical to its catalytic activities. Lipidomics analysis revealed decreased cutin amounts and increased wax contents in anthers of both zmabcg26 and zmfar1 GMS mutants. A more detailed analysis exhibited differential changes in 54 monomer contents between wild type and mutants, as well as between zmabcg26 and zmfar1. These findings will promote a deeper understanding of miRNA-regulated lipid metabolic genes and the functional diversity of lipid metabolic genes, contributing to lipid biosynthesis in maize anthers. Additionally, cosegregating molecular markers for ZmABCG26 and ZmFAR1 were developed to facilitate the breeding of male sterile lines.

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Section: Introductionmentioning

confidence: 99%

ZmFAR1 and ZmABCG26 Regulated by microRNA Are Essential for Lipid Metabolism in Maize Anther

Jiang

Liu

et al. 2021

IJMS

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“…GMS is generally due to a mutation in a nuclear gene; thus, the GMS mutant has obvious advantages, such as non-conditional, recessive, and strictly monogenic inheritance, and is useful for both hybrid breeding and seed production in crops [37]. Although GMS has long been a research focus for many plants, previous studies of the GMS genes have mainly focused on the single gene [25,[38][39][40]. The main reason is that it is relatively difficult to simultaneously obtain multi-gene mutations with traditional mutagenesis and map-based cloning methods.…”

Section: Discussionmentioning

confidence: 99%

Use of CRISPR/Cas9-Based Gene Editing to Simultaneously Mutate Multiple Homologous Genes Required for Pollen Development and Male Fertility in Maize

Liu

Zhang

Jiang

et al. 2022

Cells

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Male sterility represents an important trait for hybrid breeding and seed production in crops. Although the genes required for male fertility have been widely studied and characterized in many plant species, most of them are single genic male-sterility (GMS) genes. To investigate the role of multiple homologous genes in anther and pollen developments of maize, we established the CRISPR/Cas9-based gene editing method to simultaneously mutate the homologs in several putative GMS gene families. By using the integrated strategies of multi-gene editing vectors, maize genetic transformation, mutation-site analysis of T0 and F1 plants, and genotyping and phenotyping of F2 progenies, we further confirmed gene functions of every member in ZmTGA9-1/-2/-3 family, and identified the functions of ZmDFR1, ZmDFR2, ZmACOS5-1, and ZmACOS5-2 in controlling maize male fertility. Single and double homozygous gene mutants of ZmTGA9-1/-2/-3 did not affect anther and pollen development, while triple homozygous gene mutant resulted in complete male sterility. Two single-gene mutants of ZmDFR1/2 displayed partial male sterility, but the double-gene mutant showed complete male sterility. Additionally, only the ZmACOS5-2 single gene was required for anther and pollen development, while ZmACOS5-1 had no effect on male fertility. Our results show that the CRISPR/Cas9 gene editing system is a highly efficient and convenient tool for identifying multiple homologous GMS genes. These findings enrich GMS genes and mutant resources for breeding of maize GMS lines and promote deep understanding of the gene family underlying pollen development and male fertility in maize.

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“…9A ). Disruption of processes affecting plastid fatty acid synthesis and export have been previously demonstrated to cause male sterility in plants ( Li et al , 2015 ; T. Zhu et al , 2020 ; Zhang et al , 2021 ). A possible involvement of BnChimera in lipid biosynthesis was previously proposed after conducting cutin and wax measurements ( Xia et al , 2016 ).…”

Section: Discussionmentioning

confidence: 99%

Two wrongs make a right: heat stress reversion of a male-sterile Brassica napus line

Schuhmann

Engstler

Klöpfer

et al. 2022

Journal of Experimental Botany

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Male sterile lines play important roles in plant breeding to obtain hybrid vigour. The male sterility Lembke (MSL) system is a thermosensitive genic male sterility system of Brassica napus and is one of the main systems used in European rapeseed breeding. Interestingly the MSL system shows high similarity to the 9012AB breeding system from China including the ability to revert to fertile in high temperature conditions. Here we demonstrate that the MSL system is regulated by the same restorer of fertility gene BnaC9-Tic40 as the 9012AB system, which is related to the translocon at the inner envelope membrane of chloroplasts 40 (TIC40) from Arabidopsis. The male sterility gene of the MSL system was also identified to be a chloroplast localised protein which we call BnChimera, this gene shows high sequence similarity to the sterility gene previously described for the 9012AB system. For the first time a direct protein interaction between the BnaC9-Tic40 and the BnChimera could be demonstrated. In addition, the corresponding amino acids that mediate this interaction were identified and possibly determine how BnaC9-Tic40 acts as the restorer of fertility. Using an RNA-seq approach, the effects of heat treatment on the male fertility restoration of an MSL system line C545 were investigated. This data demonstrated that many pollen developmental pathways were affected by the higher temperatures. It is hypothesised that heat stress reverses the male sterility via a combination of slower production of cell wall precursors in plastids and a slower flower development, which ultimately results in fertile pollen. The potential breeding applications of these results are discussed regarding the capacity of using the MSL system in producing thermotolerant fertile plants.

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ZmMs25 encoding a plastid-localized fatty acyl reductase is critical for anther and pollen development in maize

Cited by 35 publications

References 71 publications

ZmFAR1 and ZmABCG26 Regulated by microRNA Are Essential for Lipid Metabolism in Maize Anther

ZmFAR1 and ZmABCG26 Regulated by microRNA Are Essential for Lipid Metabolism in Maize Anther

Use of CRISPR/Cas9-Based Gene Editing to Simultaneously Mutate Multiple Homologous Genes Required for Pollen Development and Male Fertility in Maize

Two wrongs make a right: heat stress reversion of a male-sterile Brassica napus line

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