Collins, C. F. | bioRxiv Science

bioRxiv2026

Horizontal gene transfer fuels metabolic innovation in the grass Zuloagaea bulbosa

Horizontal gene transfer (HGT) allows the movement of DNA across broad evolutionary distances without sexual reproduction. In grasses, HGT is widespread and although a few horizontally transferred genes (HTG) are adaptive, most are purged over time. Within the adaptive HTG, biosynthetic genes encoding enzymes that act together in the same pathway and physically co-localise in clusters have been reported multiple times. The aims of this study are to test whether HGT is bidirectional in a pair of grass species, maize and Zuloagaea bulbosa, and if HTGs are found more than expected by chance in biosynthetic genes organised in clusters. To achieve this, we firstly generated a phased reference genome for Z. bulbosa. Then we identified 56 candidate horizontally transferred genes, of which 45% were from Andropogoneae, including two likely to be of maize origin. Since transfers from Z. bulbosa to maize were previously described, our results show that HGT is bidirectional, although the balance might not be even. After predicting all biosynthetic gene clusters in the Z. bulbosa genome, we found that HTGs are enriched in biosynthetic genes organised in clusters. This correlation between HGT and gene clustering is likely to be a consequence of selection due to the immediate adaptive benefit a whole pathway can provide. Two of the HTGs from Andropogoneae belong to the benzoxazinoid BGC, which previously underwent an ancestral transfer from Panicoideae into Pooideae. The dynamism of biosynthetic gene clusters, including recurrent horizontal gene transfers, contributes to the extraordinary metabolic diversity present in plants. Significance statementHorizontal gene transfer (HGT) is a significant driver of evolution that is widespread in grasses. In this study, we show for the first time reciprocal transfer of DNA between maize and another Mexican grass, Zuloagaea bulbosa. This result represents a proof of concept of bidirectional HGT which allows for limited, recurrent gene flow among distant species. Furthermore, we show that horizontally transferred genes are enriched for biosynthetic genes organised in biosynthetic gene clusters, regions of the genome that encode for multiple enzymes that act in the same biosynthetic pathway. We hypothesise that the transfer of a complete multi-genic pathway, ready to be used and potentially offering an evolutionary advantage, might promote a predominant retention of gene clusters in comparison with background HGT.

genomics↗

bioRxiv2025

Regulatory features determine the evolutionary fate of laterally acquired genes in plants

Lateral gene transfer (LGT) is widespread in eukaryotes, including in animals and plants where it can fuel adaptive evolution and innovation. However, the factors that influence the integration and long-term retention of transferred genes remain poorly understood. The pangenome of the grass Alloteropsis has a high turnover of laterally acquired genes, and here we combine expression, methylation and genomic data to identify factors promoting their long-term persistence. Most transferred genes appear to be degenerating, showing lower expression levels and/or greater sequence truncation compared to their vertically inherited homologs. These degenerating genes also show significantly higher levels of DNA methylation, potentially indicating transcriptional silencing. The likelihood of a transferred gene being retained will be influenced by how easily it can be expressed in the recipient genome. In Alloteropsis, putatively functional laterally acquired genes had expression levels significantly more similar to their donor xenolog than to their vertically inherited homolog. This pattern suggests that transferred genes may carry cis-regulatory elements encoded on the fragment of DNA that moves between species, facilitating their expression in the new genomic context. Evolutionary novelty may also increase the likelihood that selection retains a transferred gene. However, only a significant difference in expression level, not sequence divergence, between donor and recipient orthologs is associated with successful lateral gene transfer. Overall, our results show that most transferred genes degrade over time. However, those capable of regulating their own expression are more likely to persist and contribute to long-term evolutionary innovation. Significance StatementLateral gene transfer (LGT) can introduce novel traits into plant genomes, yet most transferred genes are only transient residents and are degenerating, with reduced expression, truncation, and elevated DNA methylation. However, a minority persist and are more likely to resemble their donor counterparts in expression, suggesting co-transfer of cis-regulatory elements. These findings indicate that regulatory compatibility is key to their long-term survival.

evolutionary biology↗