High expression in maize pollen correlates with genetic contributions to pollen fitness as well as with coordinated transcription from neighboring transposable elements


Autoři: Cedar Warman aff001;  Kaushik Panda aff002;  Zuzana Vejlupkova aff001;  Sam Hokin aff003;  Erica Unger-Wallace aff004;  Rex A. Cole aff001;  Antony M. Chettoor aff003;  Duo Jiang aff005;  Erik Vollbrecht aff004;  Matthew M. S. Evans aff003;  R. Keith Slotkin aff002;  John E. Fowler aff001
Působiště autorů: Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, United States of America aff001;  Donald Danforth Plant Science Center, St. Louis, Missouri, United States of America aff002;  Department of Plant Biology, Carnegie Institution for Science, Stanford, California, United States of America aff003;  Department of Genetics Development and Cell Biology, Iowa State University, Ames, Iowa, United States of America aff004;  Department of Statistics, Oregon State University, Corvallis, Oregon, United States of America aff005;  Bioinformatics and Computational Biology, Iowa State University, Ames, Iowa, United States of America aff006;  Interdepartmental Genetics, Iowa State University, Ames, Iowa, United States of America aff007;  Center for Genome Research and Biocomputing, Oregon State University, Corvallis, Oregon, United States of America aff008
Vyšlo v časopise: High expression in maize pollen correlates with genetic contributions to pollen fitness as well as with coordinated transcription from neighboring transposable elements. PLoS Genet 16(4): e1008462. doi:10.1371/journal.pgen.1008462
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008462

Souhrn

In flowering plants, gene expression in the haploid male gametophyte (pollen) is essential for sperm delivery and double fertilization. Pollen also undergoes dynamic epigenetic regulation of expression from transposable elements (TEs), but how this process interacts with gene expression is not clearly understood. To explore relationships among these processes, we quantified transcript levels in four male reproductive stages of maize (tassel primordia, microspores, mature pollen, and sperm cells) via RNA-seq. We found that, in contrast with vegetative cell-limited TE expression in Arabidopsis pollen, TE transcripts in maize accumulate as early as the microspore stage and are also present in sperm cells. Intriguingly, coordinate expression was observed between highly expressed protein-coding genes and their neighboring TEs, specifically in mature pollen and sperm cells. To investigate a potential relationship between elevated gene transcript level and pollen function, we measured the fitness cost (male-specific transmission defect) of GFP-tagged coding sequence insertion mutations in over 50 genes identified as highly expressed in the pollen vegetative cell, sperm cell, or seedling (as a sporophytic control). Insertions in seedling genes or sperm cell genes (with one exception) exhibited no difference from the expected 1:1 transmission ratio. In contrast, insertions in over 20% of vegetative cell genes were associated with significant reductions in fitness, showing a positive correlation of transcript level with non-Mendelian segregation when mutant. Insertions in maize gamete expressed2 (Zm gex2), the sole sperm cell gene with measured contributions to fitness, also triggered seed defects when crossed as a male, indicating a conserved role in double fertilization, given the similar phenotype previously demonstrated for the Arabidopsis ortholog GEX2. Overall, our study demonstrates a developmentally programmed and coordinated transcriptional activation of TEs and genes in pollen, and further identifies maize pollen as a model in which transcriptomic data have predictive value for quantitative phenotypes.

Klíčová slova:

Arabidopsis thaliana – Fertilization – Gene expression – Maize – Pollen – Seedlings – Seeds – Sperm


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