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Cellular and molecular characteristics of pollen abortion in chrysanthemum cv. Kingfisher

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Abstract

Key message

Microspore degeneration at the tetrad stage is associated with tapetum degeneration retardation. Some genes and proteins related to cell senescence and death are the key factors for pollen abortion.

Abstract

Chrysanthemum (Chrysanthemum morifolium) is a major floriculture crop in the world, but pollen contamination is an urgent problem to be solved in chrysanthemum production. C. morifolium ‘Kingfisher’ is a chrysanthemum cultivar that does not contain any pollen in mature anthers, thus it is a very important material for developing chrysanthemum without pollen contamination. However, the mechanism of its pollen abortion remains unclear. In this study, the cellular and molecular mechanisms of ‘Kingfisher’ pollen abortion were investigated using transmission electron microscopy, RNA sequencing, isobaric tags for relative and absolute quantitation, and bioinformatics. It was found that the meiosis of microspore mother cells was normal before the tetrad stage, the microspores began to degenerate at the tetrad stage, and no microspores were observed in the anthers after the tetrad stage. In addition, transcriptomic and proteomic analyses showed that some genes and proteins related to cell senescence and death were identified to be implicated in chrysanthemum pollen abortion. These results indicated that the tetrad stage was the main period of pollen abortion, and the genes and proteins related to cell senescence and death contributed to pollen abortion. These add to our understanding of chrysanthemum pollen abortion and will be helpful for development of flowers without pollen contamination in the future.

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Abbreviations

iTRAQ:

Isobaric tags for relative and absolute quantitation

TEM:

Transmission electron microscopy

FPKM:

Clean reads per kilo base per million

KEGG:

Kyoto encyclopedia of genes and genomes

COG:

Cluster of orthologous groups

DEG:

Differentially expressed gene

DEP:

Differentially expressed proteins

PCD:

Programmed cell death

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (31471901), the earmarked fund for Jiangsu Agricultural Industry Technology System (JATS[2018]006), the Natural Science Foundation of Jiangsu Province (BK20161449), and the Fundamental Research Funds for the Central Universities (KYTZ201602).

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Authors and Affiliations

  1. College of Horticulture, Nanjing Agricultural University, Nanjing, 210095, China

    Fan Wang, Xinghua Zhong, Lulu Huang, Weimin Fang, Fadi Chen & Nianjun Teng

  2. Key Laboratory of Landscaping Agriculture, Ministry of Agriculture, Nanjing, 210095, China

    Fan Wang, Xinghua Zhong, Lulu Huang, Weimin Fang, Fadi Chen & Nianjun Teng

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  1. Fan Wang
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  2. Xinghua Zhong
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  3. Lulu Huang
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  4. Weimin Fang
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  6. Nianjun Teng
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Contributions

NJT conceived and designed the experiments; WMF and FDC contributed to the research idea; FW, XHZ and LLH performed the experiments and analyzed the data; FW and XHZ wrote the paper; all authors read and approved the final manuscript.

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Correspondence to Nianjun Teng.

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Electronic supplementary material

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Supplementary Figure S1 Distribution of annotated species (TIF 441 KB)

11103_2018_777_MOESM2_ESM.tif

Supplementary Figure S2 Functional distribution of COG annotation. X axis represents the numbers of unigenes, Y axis represents the COG functional categories (TIF 9713 KB)

11103_2018_777_MOESM3_ESM.tif

Supplementary Figure S3 Functional distribution of GO annotation. X axis represents the numbers of unigenes, Y axis represents the GO functional categories (TIF 11127 KB)

11103_2018_777_MOESM4_ESM.tif

Supplementary Figure S4 CDS length distribution. X axis represents the lengths of CDS, Y axis represents the numbers of CDS (TIF 10602 KB)

11103_2018_777_MOESM5_ESM.tif

Supplementary Figure S5 Number statistics and MA plot of DEGs. a Number statistics of DEGs. X axis represents the expression patterns of DEGs, Y axis represents the numbers of DEGs. b MA plot of DEGs. X axis represents value A (log2 transformed mean expression level), Y axis represents value M (log2 transformed fold change). ‘Kingfisher-1’ represents pollen aborting stage, ‘Kingfisher-2’ represents pollen aborted stage (TIF 32893 KB)

11103_2018_777_MOESM6_ESM.tif

Supplementary Figure S6 Pathway functional enrichment of DEGs. X axis represents rich factors (rich factor = the number of DEGs in one pathway/the number of unigenes in this pathway), Y axis represents pathway names. Colorings indicate q-values (blue: high, black: low), the lower q-value indicates the more significant enrichment. Point sizes indicate the numbers of DEGs (big: more, small: less) (TIF 5951 KB)

11103_2018_777_MOESM7_ESM.tif

Supplementary Figure S7 Validation of RNA-Seq results by qRT-PCR. FPKM represents the expression level of the genes in the sequencing data (TIF 3336 KB)

Supplementary Table S1 (DOCX 13 KB)

Supplementary Table S2 KEGG annotation results of unigenes (XLS 1077 KB)

Supplementary Table S3 (DOCX 13 KB)

Supplementary Table S4 The different expression of unigenes (XLS 2874 KB)

Supplementary Table S5 KEGG annotation results of DEGs (XLS 510 KB)

Supplementary Table S6 131 DEGs classified into 7 categories (XLS 37 KB)

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Wang, F., Zhong, X., Huang, L. et al. Cellular and molecular characteristics of pollen abortion in chrysanthemum cv. Kingfisher. Plant Mol Biol 98, 233–247 (2018). https://doi.org/10.1007/s11103-018-0777-y

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