Genomes of Poaceae sisters reveal key metabolic innovations preceding the emergence of grasses

Authors: TAKEDA-KIMURA, YURI - University Of Wisconsin; MOORE, BETHANY - University Of Wisconsin; HOLDEN, SAMUEL - Sainsbury Laboratory; DEB, SONTOSH - University Of Alabama; BARRETT, MATT - James Cook University; LORENCE, DAVID - National Tropical Botanical Garden (NTBG); DE OLIVEIRA, MARCOS - University Of Wisconsin; GRIMWOOD, JANE - Hudsonalpha Institute For Biotechnology; WILLIAMS, MELISSA - Hudsonalpha Institute For Biotechnology; BOSTON, LORI BETH - Hudsonalpha Institute For Biotechnology; JENKINS, JERRY - Hudsonalpha Institute For Biotechnology; PLOTT, CHRISTOPHER - Hudsonalpha Institute For Biotechnology; SHU, SHENGQIANG - Department Of Energy Joint Genome; BARRY, KERRIE - Department Of Energy Joint Genome; GOODSTEIN, DAVID - Department Of Energy Joint Genome; SCHMUTZ, JEREMY - Department Of Energy Joint Genome; Moscou, Matthew; MCKAIN, MICHAEL - University Of Alabama; LEEBENS-MACK, JAMES - University Of Georgia; MAEDA, HIROSHI - University Of Wisconsin

Submitted to: bioRxiv
Publication Type: Pre-print Publication
Publication Acceptance Date: 11/7/2024
Publication Date: 11/7/2024
Citation: Takeda-Kimura, Y., Moore, B., Holden, S., Deb, S.K., Barrett, M., Lorence, D., De Oliveira, M.V., Grimwood, J., Williams, M., Boston, L., Jenkins, J., Plott, C., Shu, S., Barry, K., Goodstein, D.M., Schmutz, J., Moscou, M.J., Mckain, M.R., Leebens-Mack, J.H., Maeda, H.A. 2024. Genomes of Poaceae sisters reveal key metabolic innovations preceding the emergence of grasses. bioRxiv. https://doi.org/10.1101/2024.11.06.622220.
DOI: https://doi.org/10.1101/2024.11.06.622220

Interpretive Summary: The grass family (Poaceae, Poales) holds immense economic and ecological significance, exhibiting unique metabolic traits, including dual starch and lignin biosynthetic pathways. To investigate when and how the metabolic innovations known in grasses evolved, we sequenced the genomes of a non-core grass, Pharus latifolius, the non-grass graminids, Joinvillea ascendens and Ecdeiocolea monostachya, representing the sister clade to Poaceae, and Typha latifolia, representing the sister clade to the remaining Poales. The rho whole genome duplication ('WGD) in the ancestral lineage for all grasses contributed to the gene family expansions underlying cytosolic starch biosynthesis, whereas an earlier tandem duplication of phenylalanine ammonia lyase (PAL) gave rise to phenylalanine/tyrosine ammonia lyase (PTAL) responsible for the dual lignin biosynthesis. Two mutations were sufficient to expand ancestral PAL function into PTAL. The integrated genomic and biochemical analyses of grass relatives in Poales revealed the evolutionary and molecular basis of key metabolic innovations of grasses.

Technical Abstract: The cereal crops corn, rice, wheat, barley, rye, oats, millet, and tef are all grasses. Grasses emerged over a 100 million year period, adapting to diverse environments and potentially gaining unique biological pathways. In this work, we set out to sequence the genomes of several ancient relatives of grasses in order to identify and understand key pathways that emerged in the grasses. We discovered that the enzymes producing starch were duplicated during an event that impacted all grasses, whereas duplication of enzymes producing lignin (PAL and PTAL) occurred independently. We show that two differences in the lignin producing enzymes PAL and PTAL are sufficient to swap their specificity. By understanding the key mutations that underlie their specificity change, we can use this knowledge to engineer lignin biosynthetic pathways in diverse plants to improve the production of food, fiber, and fuel crops.