For decades, it was known that plants trade carbohydrates for phosphate with their fungal symbionts. However, recent studies show that plant-derived lipids probably represent the most essential currency of exchange. Understanding the regulation of plant genes involved in the currency of exchange is crucial to understanding stability of this mutualism. Plants encounter many different AMF genotypes that vary greatly in the benefit they confer to plants. Yet the role that fungal genetic variation plays in the regulation of this currency has not received much attention. We used a high-resolution phylogeny of one AMF species (Rhizophagus irregularis) to show that fungal genetic variation drives the regulation of the plant fatty acid pathway in cassava (Manihot esculenta); a pathway regulating one of the essential currencies of trade in the symbiosis. The regulation of this pathway was explained by clearly defined patterns of fungal genome-wide variation representing the precise fungal evolutionary history. This represents the first demonstrated link between the genetics of AMF and reprogramming of an essential plant pathway regulating the currency of exchange in the symbiosis. The transcription factor RAM1 was also revealed as the dominant gene in the fatty acid plant gene co-expression network. Our study highlights the crucial role of variation in fungal genomes in the trade of resources in this important symbiosis and also opens the door to discovering characteristics of AMF genomes responsible for interactions between AMF and cassava that will lead to optimal cassava growth.
Phylogenetic signals of cassava fatty acid gene transcription significantly associated with the R. irregularis phylogeny and the cassava fatty acid pathway co-expression network.
a Histograms showing the transcriptional responses of cassava genes in the different fungal treatments and represented as the difference of each treatment to the mean transcriptional response across all treatments. Bars represent ±S.E. Phylogenetic signal indicators and their significance are shown below in each histogram. Only genes that showed at least one significant indicator are displayed. Other fatty acid-related genes are shown in Fig. S5B. b The plant co-expression network based on one gene module comprising the largest number of genes from the fatty acid pathway. The network shows the strong co-transcription of RAM1 with several other transcription factors (WRI5c and RAD1) and fatty acid synthesis genes (DLD, KASIII, MAT, and EAR), which are also hub genes in this module (in bold). In this module, 45 were hub genes out of 476, but only the hub fatty acid-related genes are shown in bold. Edges (connections between nodes/genes) of the network are represented as a function of their weight, a measure of connection strength. Only the 5% strongest edges are represented with increase thickness and decrease transparency with connection intensity. Node size reflects the degree of connectivity, i.e., the number of connections with other nodes. More information on the network is available in Data S5a.