Tools for de novo domestication: GRASSY TILLERS1 (GT1) and SIX-ROWED SPIKE1 (VRS1) homologs are conserved growth repression regulators

Authors: Gallagher, Joseph - Joe; MAN, JARRETT - University Of Massachusetts, Amherst; CHIARAMIDA, ADRIANA - University Of Massachusetts, Amherst; ROZZA, ISABELLA - University Of Massachusetts, Amherst; PATTERSON, ERIN - University Of Massachusetts, Amherst; POWELL, MORGAN - University Of Massachusetts, Amherst; SCHRAGER-LAVELLE, AMANDA - University Of Massachusetts, Amherst; MULTANI, DILBAG - Corteva Agriscience; MEELEY, ROBERT - Corteva Agriscience; BARTLETT, MADELAINE - University Of Massachusetts, Amherst

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/31/2023
Publication Date: 12/14/2023
Citation: Gallagher, J.P., Man, J., Chiaramida, A., Rozza, I.K., Patterson, E.L., Powell, M.M., Schrager-Lavelle, A., Multani, D.S., Meeley, R., Bartlett, M.E. 2023. Tools for de novo domestication: GRASSY TILLERS1 (GT1) and SIX-ROWED SPIKE1 (VRS1) homologs are conserved growth repression regulators. Proceedings of the National Academy of Sciences (PNAS). Vol. 120. https://doi.org/10.1073/pnas.2311961120.
DOI: https://doi.org/10.1073/pnas.2311961120

Interpretive Summary: Plant yield can be impacted by the fertility of reproductive structures. In grasses, this fertility is regulated in part by genes that regulate growth repression. Genes GRASSY TILLERS1 (GT1) and SIX-ROWED SPIKE1 (VRS1) both regulate growth repression and have been identified as playing a role in regulating floral development in maize and barley, respectively. In this study, the roles of GT1-like and VRS1-like genes in maize and brachypodium were examined. CRISPR-Cas9 gene editing was used to develop mutants in these genes. Double mutants in gt1 and vrs1-like1 (vrl1) developed more branching and flowering structures in maize and brachypodium. Repression of floral tissues caused by transgenic expression of GT1 in the model plant Arabidopsis thaliana confirmed that these genes can regulate growth repression across long divergence times. Thus, these genes display a highly conserved role in regulating grass reproduction via growth repression, and may be useful for improving productivity through crop engineering.

Technical Abstract: Crop engineering and de novo domestication using genome editing are new frontiers in agriculture. However, outside of well-studied crops and model systems, prioritizing engineering targets remains challenging. Evolution can guide us, revealing genes with deeply conserved roles that have repeatedly been selected in the evolution of plant form. Homologs of the transcription factor genes GRASSY TILLERS1 (GT1) and SIX-ROWED SPIKE1 (VRS1) have repeatedly been targets of selection in domestication and evolution, where they repress growth in many developmental contexts. This suggests a conserved role for these genes in regulating growth repression. To test this, we determined the roles of GT1 and VRS1 homologs in Zea mays (maize) and the distantly related grass Brachypodium distachyon (brachypodium) using gene editing and mutant analysis. In maize, gt1; vrs1-like1 (vrl1) mutants have derepressed growth of floral organs. In addition, gt1; vrl1 mutants bore more ears and more branches, indicating broad roles in growth repression. In brachypodium, bdgt1; bdvrl1 mutants have more branches, spikelets, and flowers than wild-type plants, indicating conserved roles for GT1 and VRS1 homologs in growth suppression over ca. 59 million years of grass evolution. Importantly, many of these traits influence crop productivity. Notably, maize GT1 can suppress growth in Arabidopsis thaliana (arabidopsis) floral organs, despite ca. 160 million years of evolution separating the grasses and arabidopsis. Thus, GT1 and VRS1 maintain their potency as growth regulators across vast timescales and in distinct developmental contexts. This work highlights the power of evolution to inform genome editing in crop improvement.