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.