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Integrated metabolite profiling and transcriptome analysis reveals a dynamic metabolic exchange between pollen tubes and the style during fertilization of Brassica napus

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Abstract

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In this study, we analyzed the transcriptome and metabolite profile of the style to explore the essential metabolites and specific genes for pollen tube growth of B. napus in vivo.

Abstract

For sexual reproduction of flowering plants, pollen must germinate on the stigma and the pollen tube must grow through the style to deliver the sperm nuclei to the female gametophyte cells. During this process, the rapidly growing pollen tube can cover substantial distances. Despite the clear requirements for energy and cellular building blocks in this process, few studies have examined the role of metabolism in the style for pollen tube elongation. In this study, we comprehensively analyzed the transcriptome and metabolite profiles during pollen germination and pollen tube growth in the style in Brassica napus. We profiled the transcripts and metabolites stored in pollen and identified many transcripts related to metabolic pathways. Mature pollen contained low levels of nutrients, whereas the styles contained high levels of diverse nutrients. The levels of most nutrients in the style, especially metabolites for cell wall synthesis and energy metabolism, rapidly decreased at 2 h after pollination, along with pollen germination and pollen tube elongation through the style. A subset of genes involved in cell wall synthesis and nutrient transport were expressed specifically in styles at 1 h after pollination. These results demonstrated that successful fertilization involves the transcripts and nutrients stored in mature pollen, and specific gene expression and stored nutrients in the style. Therefore, these findings enhance our understanding of fertilization in B. napus.

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Acknowledgements

This work was supported by the NSFC project (31671730), the National Key R&D Program of China (2016YFD0100506), and the Fundamental Research Funds for the Central Universities (KYZ201301 and KJSY201510).

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Author notes

  1. Helin Tan and Jiahuan Zhang have contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, 210095, China

    Helin Tan & Wenxue Ye

  2. Plant Sciences Division, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, LE12 5RD, UK

    Jiahuan Zhang

  3. College of Life Sciences, Shanxi Agricultural University, Taigu, 030801, China

    Xiao Qi & Xingchun Wang

  4. Animal Sciences National Teaching Demonstration Center, Nanjing Agricultural University, Nanjing, 210095, China

    Xiaoe Xiang

Authors
  1. Helin Tan
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  2. Jiahuan Zhang
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  3. Xiao Qi
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  4. Wenxue Ye
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  5. Xingchun Wang
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  6. Xiaoe Xiang
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Contributions

J. Z. and X. Q. performed most of the research, X. X. and W. Y. completed the metabolite detection, H. T. and X. W. drafted the manuscript. H. T. designed the experiment, supervised the study, and revised the manuscript.

Corresponding authors

Correspondence to Helin Tan or Xiaoe Xiang.

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The authors declare that there are no conflicts of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11103_2018_740_MOESM1_ESM.tif

Supplemental figure 1: The pistil of B. napus. The arrows show the tissue, and the dotted line shows the cut site for collecting samples. (TIF 753 KB)

11103_2018_740_MOESM2_ESM.tif

Supplemental figure 2: Pollen stained with I2-KI. A: Normal, non-stained pollen, B: pollen stained with 1% I2-KI. (TIF 179 KB)

11103_2018_740_MOESM3_ESM.tif

Supplemental figure 3: Pollen tubes examined by ultraviolet fluorescence microscopy. A: non-pollinated stigma and style; B: pollen germinated on the stigma at 1 hour after pollination; C: pollen germinated on the stigma at 2 hours after pollination; D: pollen germinated on the stigma at 3 hours after pollination; E: pollen germinated on the stigma at 6 hours after pollination. The scale bar = 100 μm. (TIF 1466 KB)

Supplemental table 1 The metabolites detected in mature pollen grain. (XLS 52 KB)

11103_2018_740_MOESM5_ESM.xls

Supplemental table 2 The metabolites detected in style at different stage during pollen germination and pollen tube growth. (XLS 100 KB)

11103_2018_740_MOESM6_ESM.xls

Supplemental table 3 A list of genes encoding enzymes of precursor synthesis for cell wall activated specifically in style. (XLS 33 KB)

11103_2018_740_MOESM7_ESM.xls

Supplemental table 4 The genes encoding enzymes of precursor synthesis for cell wall activated specifically in style. (XLS 33 KB)

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Tan, H., Zhang, J., Qi, X. et al. Integrated metabolite profiling and transcriptome analysis reveals a dynamic metabolic exchange between pollen tubes and the style during fertilization of Brassica napus. Plant Mol Biol 97, 325–335 (2018). https://doi.org/10.1007/s11103-018-0740-y

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  • DOI: https://doi.org/10.1007/s11103-018-0740-y

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