Comparative phylogenomics and phylotranscriptomics provide insights into the genetic complexity of nitrogen-fixing root-nodule symbiosis

2024

Article référencé dans le Web of Science WOS:001159183500001

Zhang Y., Fu Y., Xian W. F., Li X. L., Feng Y., Bu F. J., Shi Y., Chen S. Y., van Velzen R., Battenberg K., Berry A. M., Salgado M. G., Liu H., Yi T. S., Fournier P., Alloisio N., Pujic P., Boubakri H., Schranz M. E., Delaux P. M., Wong G. K. S., Hocher Valérie, Svistoonoff Sergio, Gherbi Hassen, Wang E., Kohlen W., Wall L. G., Parniske M., Pawlowski K., Normand P., Doyle J. J., Cheng S. F.

Plant Communications, 2024, [Early access] (1), p. 100671 [18 p.] ISSN 2590-3462

Plant root-nodule symbiosis (RNS) with mutualistic nitrogen-fixing bacteria is restricted to a single clade of angiosperms, the Nitrogen-Fixing Nodulation Clade (NFNC), and is best understood in the legume family. Nodulating species share many commonalities, explained either by divergence from a common ancestor over 100 million years ago or by convergence following independent origins over that same time period. Regardless, comparative analyses of diverse nodulation syndromes can provide insights into constraints on nodulation-what must be acquired or cannot be lost for a functional symbiosis-and the latitude for variation in the symbiosis. However, much remains to be learned about nodulation, especially outside of legumes. Here, we employed a large-scale phylogenomic analysis across 88 species, complemented by 151 RNA-seq libraries, to elucidate the evolution of RNS. Our phylogenomic analyses further emphasize the uniqueness of the transcription factor NIN as a master regulator of nodulation and identify key mutations that affect its function across the NFNC. Comparative transcriptomic assessment revealed nodulespecific upregulated genes across diverse nodulating plants, while also identifying nodule-specific and nitrogen-response genes. Approximately 70% of symbiosis-related genes are highly conserved in the four representative species, whereas defense-related and host-range restriction genes tend to be lineage specific. Our study also identified over 900 000 conserved non-coding elements (CNEs), over 300 000 of which are unique to sampled NFNC species. NFNC-specific CNEs are enriched with the active H3K9ac mark and are correlated with accessible chromatin regions, thus representing a pool of candidate regulatory elements for genes involved in RNS. Collectively, our results provide novel insights into the evolution of nodulation and lay a foundation for engineering of RNS traits in agriculturally important crops.

Sciences du monde végétal [076] ; Biotechnologies [084]

Fonds IRD [F B010089548]

fdi:010089548