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Transcriptomic and proteomic analysis reveals mechanisms of low pollen-pistil compatibility during water lily cross breeding.

ABSTRACT: BACKGROUND:In water lily (Nymphaea) hybrid breeding, breeders often encounter non-viable seeds, which make it difficult to transfer desired or targeted genes of different Nymphaea germplasm. We found that pre-fertilization barriers were the main factor in the failure of the hybridization of Nymphaea. The mechanism of low compatibility between the pollen and stigma remains unclear; therefore, we studied the differences of stigma transcripts and proteomes at 0, 2, and 6?h after pollination (HAP). Moreover, some regulatory genes and functional proteins that may cause low pollen-pistil compatibility in Nymphaea were identified. RESULTS:RNA-seq was performed for three comparisons (2 vs 0 HAP, 6 vs 2 HAP, 6 vs 0 HAP), and the number of differentially expressed genes (DEGs) was 8789 (4680 were up-regulated), 6401 (3020 were up-regulated), and 11,284 (6148 were up-regulated), respectively. Using label-free analysis, 75 (2 vs 0 HAP) proteins (43 increased and 32 decreased), nine (6 vs 2 HAP) proteins (three increased and six decreased), and 90 (6 vs 0 HAP) proteins (52 increased and 38 decreased) were defined as differentially expressed proteins (DEPs). Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analyses revealed that the DEGs and DEPs were mainly involved in cell wall organization or biogenesis, S-adenosylmethionine (SAM) metabolism, hydrogen peroxide decomposition and metabolism, reactive oxygen species (ROS) metabolism, secondary metabolism, secondary metabolite biosynthesis, and phenylpropanoid biosynthesis. CONCLUSIONS:Our transcriptomic and proteomic analysis highlighted specific genes, incuding those in ROS metabolism, biosynthesis of flavonoids, SAM metabolism, cell wall organization or biogenesis and phenylpropanoid biosynthesis that warrant further study in investigations of the pollen-stigma interaction of water lily. This study strengthens our understanding of the mechanism of low pollen-pistil compatibility in Nymphaea at the molecular level, and provides a theoretical basis for overcoming the pre-fertilization barriers in Nymphaea in the future.

SUBMITTER: Sun CQ

PROVIDER: S-EPMC6896271 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Transcriptomic and proteomic analysis reveals mechanisms of low pollen-pistil compatibility during water lily cross breeding.

Sun Chun-Qing CQ Chen Fa-Di FD Teng Nian-Jun NJ Yao Yue-Mei YM Shan Xi X Dai Zhong-Liang ZL

BMC plant biology 20191205 1

<h4>Background</h4>In water lily (Nymphaea) hybrid breeding, breeders often encounter non-viable seeds, which make it difficult to transfer desired or targeted genes of different Nymphaea germplasm. We found that pre-fertilization barriers were the main factor in the failure of the hybridization of Nymphaea. The mechanism of low compatibility between the pollen and stigma remains unclear; therefore, we studied the differences of stigma transcripts and proteomes at 0, 2, and 6 h after pollination ...[more]

PMID: 31805858

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Project description:Water lilies (order Nymphaeales) are rich in both economic and cultural values. They grow into aquatic herbs, and are divided into two ecological types: tropical and hardy. Although tropical water lilies have more ornamental and medicinal values compared to the hardy water lily, the study and utilization of tropical water lilies in both landscaping and pharmaceutical use is greatly hindered due to their limited planting area. Tropical water lilies cannot survive the winter in areas beyond 24.3°N latitude. Here, the transgenic pipeline through the pollen-tube pathway was generated for water lily for the first time. To improve cold stress tolerance of tropical water lilies, a gene encoding choline oxidase (CodA) driven by a cold stress-inducible promoter was transformed into a tropical water lily through the pollen-tube transformation. Six independent transgenic lines were tested for survival rate during two winter seasons from 2015 to 2017 in Hangzhou (30.3°N latitude). PCR and southern blot detection revealed that the CodA gene had been integrated into the genome. Reverse transcription PCR showed that CodA gene was induced after cold stress treatment, and further quantitative real-time PCR revealed different expressions among six 4 lines and line 3 had the highest expression. Multiple physiological experiments showed that after cold stress treatment, both the conductivity and malondialdehyde (MDA) levels from transgenic plants were significantly lower than those of non-transgenic plants, whereas the content of betaine and the activity of superoxide dismutase, catalase, and peroxidase were higher than those from non-transgenic plants. These results suggest that expression of exogenous CodA gene significantly improved the cold stress tolerance of tropical water lilies through a wide range of physiological alterations. Our results currently expanded a six-latitude cultivating area of the tropical water lilies. These results not only illuminate the bright future for water lily breeding but will also facilitate the functional genomic studies.

Project description:BackgroundUnilateral incompatibility (UI) is an asymmetric reproductive barrier that unidirectionally prevents gene flow between species and/or populations. UI is characterized by a compatible interaction between partners in one direction, but in the reciprocal cross fertilization fails, generally due to pollen tube rejection by the pistil. Although UI has long been observed in crosses between different species, the underlying molecular mechanisms are only beginning to be characterized. The wild tomato relative Solanum habrochaites provides a unique study system to investigate the molecular basis of this reproductive barrier, as populations within the species exhibit both interspecific and interpopulation UI. Here we utilized a transcriptomic approach to identify genes in both pollen and pistil tissues that may be key players in UI.ResultsWe confirmed UI at the pollen-pistil level between a self-incompatible population and a self-compatible population of S. habrochaites. A comparison of gene expression between pollinated styles exhibiting the incompatibility response and unpollinated controls revealed only a small number of differentially expressed transcripts. Many more differences in transcript profiles were identified between UI-competent versus UI-compromised reproductive tissues. A number of intriguing candidate genes were highly differentially expressed, including a putative pollen arabinogalactan protein, a stylar Kunitz family protease inhibitor, and a stylar peptide hormone Rapid ALkalinization Factor. Our data also provide transcriptomic evidence that fundamental processes including reactive oxygen species (ROS) signaling are likely key in UI pollen-pistil interactions between both populations and species.ConclusionsGene expression analysis of reproductive tissues allowed us to better understand the molecular basis of interpopulation incompatibility at the level of pollen-pistil interactions. Our transcriptomic analysis highlighted specific genes, including those in ROS signaling pathways that warrant further study in investigations of UI. To our knowledge, this is the first report to identify candidate genes involved in unilateral barriers between populations within a species.

Project description:In plants, the cell fates of a vegetative cell (VC) and generative cell (GC) are determined after the asymmetric division of the haploid microspore. The VC exits the cell cycle and grows a pollen tube, while the GC undergoes further mitosis to produce two sperm cells for double fertilization. However, our understanding of the mechanisms underlying their fate differentiation remains limited. One major advantage of the nuclear proteome analysis is that it is the only method currently able to uncover the systemic differences between VC and GC due to GC being engulfed within the cytoplasm of VC, limiting the use of transcriptome. Here, we obtained pure preparations of the vegetative cell nuclei (VNs) and generative cell nuclei (GNs) from germinating lily pollens. Utilizing these high-purity VNs and GNs, we compared the differential nucleoproteins between them using state-of-the-art quantitative proteomic techniques. We identified 720 different amount proteins (DAPs) and grouped the results in 11 fate differentiation categories. Among them, we identified 29 transcription factors (TFs) and 10 cell fate determinants. Significant differences were found in the molecular activities of vegetative and reproductive nuclei. The TFs in VN mainly participate in pollen tube development. In comparison, the TFs in GN are mainly involved in cell differentiation and male gametogenesis. The identified novel TFs may play an important role in cell fate differentiation. Our data also indicate differences in nuclear pore complexes and epigenetic modifications: more nucleoporins synthesized in VN; more histone variants and chaperones; and structural maintenance of chromosome (SMC) proteins, chromatin remodelers, and DNA methylation-related proteins expressed in GN. The VC has active macromolecular metabolism and mRNA processing, while GC has active nucleic acid metabolism and translation. Moreover, the members of unfolded protein response (UPR) and programmed cell death accumulate in VN, and DNA damage repair is active in GN. Differences in the stress response of DAPs in VN vs. GN were also found. This study provides a further understanding of pollen cell differentiation mechanisms and also a sound basis for future studies of the molecular mechanisms behind cell fate differentiation.

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Transcriptomic and proteomic analysis reveals mechanisms of low pollen-pistil compatibility during water lily cross breeding.

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Transcriptomic and proteomic analysis reveals mechanisms of low pollen-pistil compatibility during water lily cross breeding.

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