Stemona genomes illuminate fatty acid partitioning between seeds and elaiosomes mediating wasp dispersal

Abstract

O_LISeed dispersal by wasps (vespicochory) is documented in five angiosperm families, with phylogenies suggesting that most vespicochorous lineages evolved from ant-dispersed (myrmecochorous) ancestors. While recent work has identified cues attracting wasp dispersers, the molecular basis remains unclear. C_LIO_LITo shed light on the molecular basis of vespicochory, we generated chromosome-level genomes for the wasp-dispersed Stemona tuberosa, and its close ant-dispersed relative S. mairei. Combining comparative genomic, transcriptomic, lipidomic, and functional analyses, we ask (i) how chemical elaiosome differentiation occurs during seed development, and (ii) how key mutualism-associated genes evolved in Stemona. C_LIO_LIWe show that elaiosomes up-regulate stearoyl-ACP {Delta}9 desaturases (SAD) and accumulate oleic acid and 1,2-diolein, which serve both as food rewards and as precursors for CER1/3-mediated biosynthesis of (Z)-9-tricosene, the key wasp attractant. By contrast, high expression of FatB and DGAT1 in seeds is associated with medium-chain fatty acids (MCFAs) production. Comparative genomics indicates conservation of these genes across Stemona, with S. tuberosa-specific FatB expansion and SAD/CER1/3 repertoire divergence. C_LIO_LIOur work supports a model for elaiosome-seed fatty-acid differentiation linking recruitment and nourishment in vespicochory. Given that oleic acid and 1,2-diolein are also key cues in myrmecochory, this shared biochemical basis may help explain how vespicochory evolves from ant-dispersed ancestors. C_LI