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Genome-wide analysis of maize GPAT gene family and cytological characterization and breeding application of ZmMs33/ZmGPAT6 gene

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Abstract

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Genome-wide analysis of maize GPAT gene family, cytological characterization of ZmMs33/ZmGPAT6 gene encoding an ER-localized protein with four conserved motifs, and its molecular breeding application in maize.

Abstract

Glycerol-3-phosphate acyltransferase (GPAT) mediates the initial step of glycerolipid biosynthesis and plays pivotal roles in plant growth and development. Compared with GPAT genes in Arabidopsis, our understanding to maize GPAT gene family is very limited. Recently, ZmMs33 gene has been identified to encode a sn-2 GPAT protein and control maize male fertility in our laboratory (Xie et al. in Theor Appl Genet 131:1363–1378, 2018). However, the functional mechanism of ZmMs33 remains elusive. Here, we reported the genome-wide analysis of maize GPAT gene family and found that 20 maize GPAT genes (ZmGPAT1-20) could be classified into three distinct clades similar to those of ten GPAT genes in Arabidopsis. Expression analyses of these ZmGPAT genes in six tissues and in anther during six developmental stages suggested that some of ZmGPATs may play crucial roles in maize growth and anther development. Among them, ZmGPAT6 corresponds to the ZmMs33 gene. Systemic cytological observations indicated that loss function of ZmMs33/ZmGPAT6 led to defective anther cuticle, arrested degeneration of anther wall layers, abnormal formation of Ubisch bodies and exine and ultimately complete male sterility in maize. The endoplasmic reticulum-localized ZmMs33/ZmGPAT6 possessed four conserved amino acid motifs essential for acyltransferase activity, while ZmMs33/ZmGPAT6 locus and its surrounding genomic region have greatly diversified during evolution of gramineous species. Finally, a multi-control sterility system was developed to produce ms33 male-sterile lines by using a combination strategy of transgene and marker-assisted selection. This work will provide useful information for further deciphering functional mechanism of ZmGPAT genes and facilitate molecular breeding application of ZmMs33/ZmGPAT6 gene in maize.

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Abbreviations

ACP:

Acyl carrier protein

BLASTP:

Basic local alignment searching tool-protein to protein

CMS:

Cytoplasmic male sterility

CRISPR:

Clustered regularly interspersed short palindromic repeats

ER:

Endoplasmic reticulum

GPAT:

Glycerol-3-phosphate acyltransferase

LPA:

Lysophosphatidic acid

2-MAG:

sn-2 Monoacylglycerol

MAS:

Marker-assisted selection

MCS:

Multi-control sterility

MEGA:

Molecular evolutionary genetics analysis

qPCR:

Quantitative PCR

RT:

Reverse transcription

SEM:

Scanning electron microscopy

SPT:

Seed production technology

TEM:

Transmission electron microscopy

WT:

Wild type

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Acknowledgements

This work was supported by the National Transgenic Major Program of China (2018ZX0800922B, 2018ZX0801006B), the National Key R&D Program of China (2017YFD0102001, 2018YFD0100806, 2017YFD0101201), the National Natural Science Foundation of China (31771875, 31871702), the Fundamental Research Funds for the Central Universities of China (06500060, FRF-TP-18-013A1, FRF-TP-18-014A1), the “Ten Thousand Plan”-National High Level Talents Special Support Plan (for Xiangyuan Wan) and the Beijing Talents Foundation From Organization department of Beijing Municipal committee of CPC (For Xiangyuan Wan).

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  1. Taotao Zhu and Suowei Wu have contributed equally to this work.

Authors and Affiliations

  1. Biology and Agriculture Research Center, University of Science and Technology Beijing, Beijing, 100024, China

    Taotao Zhu, Suowei Wu, Ziwen Li, Ke Xie, Xueli An, Biao Ma, Quancan Hou, Zhenying Dong, Youhui Tian & Xiangyuan Wan

  2. Beijing Engineering Laboratory of Main Crop Bio-Tech Breeding, Beijing International Science and Technology Cooperation Base of Bio-Tech Breeding, Beijing Solidwill Sci-Tech Co. Ltd., Beijing, 100192, China

    Suowei Wu, Danfeng Zhang, Ziwen Li, Ke Xie, Xueli An, Biao Ma, Quancan Hou, Zhenying Dong, Jinping Li & Xiangyuan Wan

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  1. Taotao Zhu
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Zhu, T., Wu, S., Zhang, D. et al. Genome-wide analysis of maize GPAT gene family and cytological characterization and breeding application of ZmMs33/ZmGPAT6 gene. Theor Appl Genet 132, 2137–2154 (2019). https://doi.org/10.1007/s00122-019-03343-y

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