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Adaptive reduction of male gamete number in the selfing plant Arabidopsis thaliana

Takashi Tsuchimatsu, Hiroyuki Kakui, Misako Yamazaki, Cindy Marona, Hiroki Tsutsui, Afif Hedhly, Dazhe Meng, Yutaka Sato, Thomas Städler, Ueli Grossniklaus, Masahiro M. Kanaoka, Michael Lenhard, Magnus Nordborg, Kentaro K. Shimizu

2020Nature Communications53 citationsDOIOpen Access PDF

Abstract

The number of male gametes is critical for reproductive success and varies between and within species. The evolutionary reduction of the number of pollen grains encompassing the male gametes is widespread in selfing plants. Here, we employ genome-wide association study (GWAS) to identify underlying loci and to assess the molecular signatures of selection on pollen number-associated loci in the predominantly selfing plant Arabidopsis thaliana. Regions of strong association with pollen number are enriched for signatures of selection, indicating polygenic selection. We isolate the gene REDUCED POLLEN NUMBER1 (RDP1) at the locus with the strongest association. We validate its effect using a quantitative complementation test with CRISPR/Cas9-generated null mutants in nonstandard wild accessions. In contrast to pleiotropic null mutants, only pollen numbers are significantly affected by natural allelic variants. These data support theoretical predictions that reduced investment in male gametes is advantageous in predominantly selfing species.

Topics & Concepts

SelfingBiologyPollenGameteGeneticsArabidopsis thalianaAlleleLocus (genetics)Evolutionary biologyGeneMutantBotanyPopulationSociologyDemographySpermPlant Reproductive BiologyPlant and animal studiesInsect and Arachnid Ecology and Behavior
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