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Postmeiotic development of pollen surface layers requires two Arabidopsis ABCG-type transporters

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Abstract

Key message

Two Arabidopsis ABC transporters, ABCG1 and ABCG16, are expressed in the tapetal layer, specifically after postmeiotic microspore release, and play important roles in pollen surface development.

Abstract

The male gametophytic cells of terrestrial plants, the pollen grains, travel far before fertilization, and thus require strong protective layers, which take the form of a pollen coat and a pollen wall. The protective surface structures are generated by the tapetum, the tissue surrounding the developing gametophytes. Many ABC transporters, including Arabidopsis thaliana ABCG1 and ABCG16, have been shown to play essential roles in the development of such protective layers. However, the details of the mechanism of their function remain to be clarified. In this study, we show that ABCG1 and ABCG16 are localized at the plasma membrane of tapetal cells, specifically after postmeiotic microspore release, and play critical roles in the postmeiotic stages of male gametophyte development. Consistent with this stage-specific expression, the abcg1 abcg16 double knockout mutant exhibited defects in pollen development after postmeiotic microspore release; their microspores lacked intact nexine and intine layers, exhibited defects in pollen mitosis I, displayed ectopic deposits of arabinogalactan proteins, failed to complete cytokinesis, and lacked sperm cells. Interestingly, the double mutant exhibited abnormalities in the internal structures of tapetal cells, too; the storage organelles of tapetal cells, tapetosomes and elaioplasts, were morphologically altered. Thus, this work reveals that the lack of ABCG1 and ABCG16 at the tapetal cell membrane causes a broad range of defects in pollen, as well as in tapetal cells themselves. Furthermore, these results suggest that normal pollen surface development is necessary for normal development of the pollen cytoplasm.

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Abbreviations

ABC transporter:

ATP-binding cassette transporter

AMS:

Aborted microspores

TEK:

Transposable element silencing via AT-hook

AGP:

Arabinogalactan protein

TEM:

Transmission electron microscopy

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Acknowledgments

This work was supported by the National Research Foundation (NRF) of Korea Grant funded by the Ministry of Science, Information and Communication Technology, and Future Planning, Korea awarded to Y.L. (NRF-2015R1A2A1A01004294), Grants from the National Key Basic Research Developments Program, Ministry of Science and Technology, China (2013CB126902); National Transgenic Major Program (2016ZX08009003-003-007) awarded to D. Zhang, and by the Direct Grant for Research from the Chinese University of Hong Kong (4053089 and 3132797) to B. Kang.

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Authors and Affiliations

  1. Department of Life Sciences, Pohang University of Science and Technology (POSTECH), Pohang, 37673, Korea

    Sojeong Yim, Deepa Khare, Joohyun Kang, Jae-Ung Hwang & Youngsook Lee

  2. Division of Integrative Biosciences and Biotechnology, POSTECH, Pohang, 37673, Korea

    Youngsook Lee

  3. Joint International Research Laboratory of Metabolic and Developmental Sciences, Shanghai Jiao Tong University-University of Adelaide Joint Center for Agriculture and Health, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China

    Wanqi Liang & Dabing Zhang

  4. Department of Plant and Microbial Biology, University Zurich, 8008, Zurich, Switzerland

    Enrico Martinoia

  5. School of Life Sciences, Centre for Cell and Developmental Biology and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Hong Kong, China

    Byungho Kang

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  1. Sojeong Yim
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  2. Deepa Khare
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Correspondence to Youngsook Lee.

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Communicated by Y.-Il Park.

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Yim, S., Khare, D., Kang, J. et al. Postmeiotic development of pollen surface layers requires two Arabidopsis ABCG-type transporters. Plant Cell Rep 35, 1863–1873 (2016). https://doi.org/10.1007/s00299-016-2001-3

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