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The MYB transcription factor Baymax1 plays a critical role in rice male fertility

Theoretical and Applied Genetics volume 134, pages 453–471 (2021)Cite this article

Abstract

Key message Rice male fertility gene Baymax1 , isolated through map-based cloning, encodes a MYB transcription factor and is essential for rice tapetum and microspore development.

Abstract The mining and characterization of male fertility gene will provide theoretical and material basis for future rice production. In Arabidopsis, the development of male organ (namely anther), usually involves the coordination between MYB (v-myb avian myeloblastosis viral oncogene homolog) and bHLH (basic helix-loop-helix) members. However, the role of MYB proteins in rice anther development remains poorly understood. In this study, we isolated and characterized a male sterile mutant (with normal vegetative growth) of Baymax1 (BM1), which encodes a MYB protein. The bm1 mutant exhibited slightly lagging meiosis, aborted transition of the tapetum to a secretory type, premature tapetal degeneration, and abnormal pollen exine formation, leading to ultimately lacks of visible pollens in the mature white anthers. Map-based cloning, complementation and targeted mutagenesis using CRISPR/Cas9 technology demonstrated that the mutated LOC_Os04g39470 is the causal gene in bm1. BM1 is preferentially expressed in rice anthers from stage 5 to stage 10. Phylogenetic analysis indicated that rice BM1 and its homologs in millet, maize, rape, cabbage, and pigeonpea are evolutionarily conserved. BM1 can physically interacts with bHLH protein TIP2, EAT1, and PHD (plant homeodomain)-finger member TIP3, respectively. Moreover, BM1 affects the expression of several known genes related to tapetum and microspore development. Collectively, our results suggest that BM1 is one of key regulators for rice male fertility and may serve as a potential target for rice male-sterile line breeding and hybrid seed production.

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Abbreviations

AD:

Activation domain

BD:

Binding domain

bHLH:

Basic helix-loop-helix

BiFC:

Bimolecular fluorescence complementation

BSA:

Bulked segregant analysis

CDS:

Coding sequence

CMS:

Cytoplasmic genetic male sterility

DAPI:

4′,6-Diamidine-2-phenylindole Dihydrodihydrochloride

FAA:

Formalin-aceto-alcohol

GUS:

β-Glucuronidase

InDel:

Insertion-deletion

MCs:

Meiotic cells

MMCs:

Microsporocytes

MYB:

V-myb avian myeloblastosis viral oncogene homolog

ORF:

Open reading frame

PCD:

Programmed cell death

PHD:

Plant homeodomain

PTGMS:

Photoperiod-thermo-sensitive genic male sterility

SEM:

Scanning electron microscopy

SPT:

Seed production technology

SSR:

Simple sequence repeat

TEM:

Transmission electron microscopy

TFs:

Transcription factors

TUNEL:

Terminal deoxynucleotidyl transferase-mediated dUTP nick-end labeling

Y2H:

Yeast two-hybrid

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Acknowledgements

We thank Bio-ultrastructure analysis Lab. of Analysis center of Agrobiology and environmental sciences, Zhejiang Univ. for TEM and SEM observation. This work was supported by grants from the National Natural Science Foundation of China (#31801440, #31871236, and #31521064), the National Key Transform Program (#2016ZX08001-002), the Chinese Academy of Agricultural Sciences Innovation Project (CAAS-ASTIP-2013-CNRRI).

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  1. Xiao-Jiao Xiang and Lian-Ping Sun contributed equally to this work.

Affiliations

  1. Key Laboratory for Zhejiang Super Rice Research and State Key Laboratory of Rice Biology, China National Rice Research Institute, Hangzhou, 311400, China

    Xiao-Jiao Xiang, Lian-Ping Sun, Ping Yu, Zheng-Fu Yang, Pei-Pei Zhang, Ying-Xin Zhang, Wei-Xun Wu, Dai-Bo Chen, Xiao-Deng Zhan, Riaz-Muhammad Khan, Adil Abbas, Shi-Hua Cheng & Li-Yong Cao

  2. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China

    Xiao-Jiao Xiang & Zheng-Fu Yang

  3. State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Taian, 271018, China

    Xiao-Jiao Xiang

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  1. Xiao-Jiao Xiang
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Contributions

XJX, LPS, LYC, and SHC designed the study. XJX and LPS contributed to data acquisition, analysis and the original draft. PY, and ZFY provided methodology. PPZ, YXZ, WXW, DBC, XDZ, RMK, and AA offered assistance in data collection and draft revision. All authors reviewed the results and approved to submit the manuscript to your journal.

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Correspondence to Shi-Hua Cheng or Li-Yong Cao.

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Xiang, XJ., Sun, LP., Yu, P. et al. The MYB transcription factor Baymax1 plays a critical role in rice male fertility. Theor Appl Genet 134, 453–471 (2021). https://doi.org/10.1007/s00122-020-03706-w

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