Abstract
BackgroundA major step in the higher plant life cycle is the decision to leave the mitotic cell cycle and begin the progression through the meiotic cell cycle that leads to the formation of gametes. The molecular mechanisms that regulate this transition and early meiosis remain largely unknown. To gain insight into gene expression features during the initiation of meiotic recombination, we profiled early prophase I meiocytes from maize (Zea mays) using capillary collection to isolate meiocytes, followed by RNA-seq.ResultsWe detected ~2,000 genes as preferentially expressed during early meiotic prophase, most of them uncharacterized. Functional analysis uncovered the importance of several cellular processes in early meiosis. Processes significantly enriched in isolated meiocytes included proteolysis, protein targeting, chromatin modification and the regulation of redox homeostasis. The most significantly up-regulated processes in meiocytes were processes involved in carbohydrate metabolism. Consistent with this, many mitochondrial genes were up-regulated in meiocytes, including nuclear- and mitochondrial-encoded genes. The data were validated with real-time PCR and in situ hybridization and also used to generate a candidate maize homologue list of known meiotic genes from Arabidopsis.ConclusionsTaken together, we present a high-resolution analysis of the transcriptome landscape in early meiosis of an important crop plant, providing support for choosing genes for detailed characterization of recombination initiation and regulation of early meiosis. Our data also reveal an important connection between meiotic processes and altered/increased energy production.
Highlights
A major step in the higher plant life cycle is the decision to leave the mitotic cell cycle and begin the progression through the meiotic cell cycle that leads to the formation of gametes
Note that anther samples contain meiocytes, which likely contributes to the small number of differentially expressed genes between anthers and meiocytes; substantially more differentially expressed genes were found between anthers or meiocytes vs. seedlings (Figure 2B, Additional file 2: Figure S1A-C; lists of up- and down-regulated genes generated with the DEseq package for R Statistical Analysis, using a threshold significance of P adj ≤ 0.01, Additional file 3: Table S2)
Detailed GO analysis of genes up-regulated in meiocytes To gain deeper insight into processes during early meiosis, we extended our functional analysis for genes up-regulated in meiocytes using AgriGO
Summary
A major step in the higher plant life cycle is the decision to leave the mitotic cell cycle and begin the progression through the meiotic cell cycle that leads to the formation of gametes. Obtaining early meiocytes from plants is possible by using CCM (Capillary Collection of Meiocytes), in which meiocytes are collected with a microcapillary [20] In these studies, mRNA of isolated Arabidopsis meiocytes at stages ranging from prophase I to tetrads was analyzed using expression microarrays [21] or next-generation sequencing [5,22]. Meiocytes showed substantial expression of transposable elements [5,22] as well as high levels of transcripts mapping to a mitochondrial genome insertion (MGI) in the nuclear genome [5] While these studies were based on pooled cells from all meiotic stages, no study has previously examined the early meiotic transcriptome within isolated meiocytes. Identifying genes and processes that are enriched is important for understanding the molecular mechanisms of regulation in early meiosis, recombination initiation, and gamete formation
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