Abstract

Rapeseed (Brassica napus L.) is an important oil crop worldwide and exhibits significant heterosis. Effective pollination control systems, which are closely linked to anther development, are a prerequisite for utilizing heterosis. The anther, which is the male organ in flowering plants, undergoes many metabolic processes during development. Although the gene expression patterns underlying pollen development are well studied in model plant Arabidopsis, the regulatory networks of genome-wide gene expression during rapeseed anther development is poorly understood, especially regarding metabolic regulations. In this study, we systematically analyzed metabolic processes occurring during anther development in rapeseed using ultrastructural observation and global transcriptome analysis. Anther ultrastructure exhibited that numerous cellular organelles abundant with metabolic materials, such as elaioplast, tapetosomes, plastids (containing starch deposits) etc. appeared, accompanied with anther structural alterations during anther development, suggesting many metabolic processes occurring. Global transcriptome analysis revealed dynamic changes in gene expression during anther development that corresponded to dynamic functional alterations between early and late anther developmental stages. The early stage anthers preferentially expressed genes involved in lipid metabolism that are related to pollen extine formation as well as elaioplast and tapetosome biosynthesis, whereas the late stage anthers expressed genes associated with carbohydrate metabolism to form pollen intine and to accumulate starch in mature pollen grains. Finally, a predictive gene regulatory module responsible for early pollen extine formation was generated. Taken together, this analysis provides a comprehensive understanding of dynamic gene expression programming of metabolic processes in the rapeseed anther, especially with respect to lipid and carbohydrate metabolism during pollen development.

Highlights

  • Rapeseed (Brassica napus L.) is animportant oil crop worldwide, providing both edible oil and industrial materials such as livestock meal, lubricants and biodiesel [1]

  • A similar anther developmental process to that found in Arabidopsis occurred in B. napus, containing a pollen mother cell stage, a tetrad stage, an early uninucleate microspore stage, a vacuolated microspore stage and a mature pollen stage

  • This study provides a comprehensive and systematic analysis of metabolic processes during rapeseed anther development using anatomy and genome-wide transcriptome analysis

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Summary

Introduction

Rapeseed (Brassica napus L.) is animportant oil crop worldwide, providing both edible oil and industrial materials such as livestock meal, lubricants and biodiesel [1]. As with many other crops, rapeseed shows significant heterosis, which is the superior performance of hybrids with respect to many agronomic traits relative to their parents This feature is commonly used to increase crop yields [2], but effective pollination control systems are required for its implementation. The study of anther development is foundational for the utilization of heterosis in selective crop breeding The anther contains both reproductive cells (pollen mother cells) and non-reproductive cell layers. The callose, which is composed of β-1,3-glucans, forms and is degraded in a process involving at least three cell wall enzymes, including β-1,3-glucanase [6,7], endocellulase [8,9], and polygalacturonase (PG) [10]. Since the anther development process is so complex, numerous genes must be dynamically expressed throughout the process, in large part to coordinate metabolism in both somatic and gametophytic cells [13]

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