Abstract
BackgroundThe fragrant flower plant Osmanthus fragrans has an extremely rare androdioecious breeding system displaying the occurrence of males and hermaphrodites in a single population, which occupies a crucial intermediate stage in the evolutionary transition between hermaphroditism and dioecy. However, the molecular mechanism of androdioecy plant is very limited and still largely unknown.ResultsHere, we used SWATH-MS-based quantitative approach to study the proteome changes between male and hermaphroditic O. fragrans pistils. A total of 428 proteins of diverse functions were determined to show significant abundance changes including 210 up-regulated and 218 down-regulated proteins in male compared to hermaphroditic pistils. Functional categorization revealed that the differentially expressed proteins (DEPs) primarily distributed in the carbohydrate metabolism, secondary metabolism as well as signaling cascades. Further experimental analysis showed the substantial carbohydrates accumulation associated with promoted net photosynthetic rate and water use efficiency were observed in purplish red pedicel of hermaphroditic flower compared with green pedicel of male flower, implicating glucose metabolism serves as nutritional modulator for the differentiation of male and hermaphroditic flower. Meanwhile, the entire upregulation of secondary metabolism including flavonoids, isoprenoids and lignins seem to protect and maintain the male function in male flowers, well explaining important feature of androdioecy that aborted pistil of a male flower still has a male function. Furthermore, nine selected DEPs were validated via gene expression analysis, suggesting an extra layer of post-transcriptional regulation occurs during O. fragrans floral development.ConclusionTaken together, our findings represent the first SWATH-MS-based proteomic report in androdioecy plant O. fragrans, which reveal carbohydrate metabolism, secondary metabolism and post-transcriptional regulation contributing to the androdioecy breeding system and ultimately extend our understanding on genetic basis as well as the industrialization development of O. fragrans.
Highlights
The fragrant flower plant Osmanthus fragrans has an extremely rare androdioecious breeding system displaying the occurrence of males and hermaphrodites in a single population, which occupies a crucial intermediate stage in the evolutionary transition between hermaphroditism and dioecy
Phenotype characterization for appropriate sampling and following SWATH‐MS analysis To perform a comprehensive proteomes analyses on androdioecy breeding system in Osmanthus fragrans, we used innovative SWATH-MS-based quantitative proteomic strategy to compare the proteomes of male and hermaphroditic flowers as outlined in Fig. 1, which employs a high specificity data-independent acquisition (DIA) method coupled with a novel targeted data extraction. Both male and hermaphroditic flowers of O. fragrans were sampled at the full bloom stage, and other floral organs were removed manually, leaving only the pistils
Carbohydrate metabolism and TCA cycle in pistils Fertilization of higher plants depend on the pollen tube elongation of the style toward the ovary, which was considered to be the fastest growing plant cell requiring a huge consumption of nutrient and energy [39, 40]
Summary
The fragrant flower plant Osmanthus fragrans has an extremely rare androdioecious breeding system displaying the occurrence of males and hermaphrodites in a single population, which occupies a crucial intermediate stage in the evolutionary transition between hermaphroditism and dioecy. Androdioecious plants are extremely rare in nature, less than 50 plants have been reported worldwide such as Datisca glomerata [2], Mercurialis annua [3], Pseudoxandra spiritus-sancti [4] and Tapiscia sinensis [5, 6], drawing widespread interests by scientists Such an unusual breeding system prefers to be distributed in the Oleaceae species including Phillyrea latifolia [7], Phillyrea angustifolia [8], Fraxinus lanuginose [9], Chionanthus retusus [10], Osmanthus serrulatus [11], O. delavayi [12] etc., accompanied by higher frequencies of males compared to other androdioecious species [13]. The molecular mechanism of reproductive development and sex differentiation in androdioecy plants is still largely unknown and requires more detailed investigations
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