Maize domestication phenotypes reveal strigolactone networks coordinating grain size evolution with kernel-bearing cupule architecture

Authors: GUAN, JIAHN-CHOU - University Of Florida; LI, CHANGSHENG - University Of Amsterdam; Flint-Garcia, Sherry; SUZUKI, MASAHARU - University Of Florida; WU, SHAN - University Of Florida; SAUNDERS, JONATHAN - University Of Florida; DONG, LEMENG - University Of Amsterdam; BOUWMEESTER, HARRO - University Of Amsterdam; MCCARTY, DONALD - University Of Florida; KOCH, KAREN - University Of Florida

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/15/2022
Publication Date: 2/2/2023
Citation: Guan, J., Li, C., Flint Garcia, S.A., Suzuki, M., Wu, S., Saunders, J., Dong, L., Bouwmeester, H., Mccarty, D., Koch, K. 2023. Maize domestication phenotypes reveal strigolactone networks coordinating grain size evolution with kernel-bearing cupule architecture. The Plant Cell. 35(3):1013-1037. https://doi.org/10.1093/plcell/koac370.
DOI: https://doi.org/10.1093/plcell/koac370

Interpretive Summary: Maize (corn) was domesticated from the wild ancestor, teosinte, approximately 9,000 years ago in southern Mexico. The gradual transition from teosinte to maize involved major changes in plant, ear, and kernel morphology. For example, modern corn seeds are nearly ten times heavier and the hard fruitcase that encases the teosinte seed was evolutionarily repurposed to form the corn cob. Only a handful of genes have been identified over the past four decades that control these major changes in morphology. A mutation in one of these key domestication genes, called teosinte glume architecture, opened the hard fruitcase early in the domestication process, thus exposing the seed for easier harvest and consumption and allowed the seed to expand in size. In this study, we investigated the role of a class of plant hormones called strigolactones in seed size and restructuring of the cob and kernels. Maize plants with mutations in the strigolactone biochemical pathway share the striking, teosinte-like ear appearance that is controlled by teosinte glume architecture. Additional lines of evidence show that teosinte glume architecture and strigolactones regulate a similar suite of downstream genes and result in similar changes in ear morphology. Our results suggest that teosinte glume architecture and strigolactone biosynthetic genes operated in tandem during domestication, resulting in larger exposed seeds typical of maize. These findings will be useful to researchers studying domestication in maize and other crop plants, and also researchers and breeders who are working to domesticate new crop species.

Technical Abstract: The maize (Zea mays) ear represents one of the most striking domestication phenotypes in any crop species, with the cob conferring an exceptional yield advantage over the ancestral form of teosinte. Remodeling of the grain-bearing surface required profound developmental changes. However, the underlying mechanisms remain unclear and can only be partly attributed to the known domestication gene Teosinte glume architecture 1 (Tga1). Here we show that a more complete conversion involves strigolactones (SLs), and that these are prominent players not only in the Tga1 phenotype but also other domestication features of the ear and kernel. Genetic combinations of a teosinte tga1 allele with three SL-related mutants progressively enhanced ancestral morphologies. The SL mutants, in addition to modulating the tga1 phenotype, also reshaped kernel-bearing pedicels and cupules in a teosinte-like manner. Genetic and molecular evidence are consistent with SL regulation of TGA1, including direct interaction of TGA1 with components of the SL-signaling system shown here to mediate TGA1 availability by sequestration. Roles of the SL network extend to enhancing maize seed size and, importantly, coordinating increased kernel growth with remodeling of protective maternal tissues. Collectively, our data show that SLs have central roles in releasing kernels from restrictive maternal encasement and coordinating other factors that increase kernel size, physical support, and their exposure on the grain-bearing surface.