Horizontal gene transfer fuels metabolic innovation in the grass Zuloagaea bulbosa

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Abstract 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 statement Horizontal 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.

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