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Programmed Cell Death in Grass Flower Development and Evolution Leveraging Basic Research into Rational Crop Design

Principal Investigator/Project Leader: 
Department of Project: 
Biology Dept.
Project Description: 

This proposal is about programmed cell death and sex determination in maize and the grass family. Programmed cell death is best defined as genetically encoded, actively controlled cellular suicide. Programmed cell death is of fundamental importance in plant development. For example, xylem cells undergo programmed cell death and create an interconnected network of hollow tubes essential for water transport. Despite its importance, developmentally regulated programmed cell death is far less understood than processes like cell division and differentiation (reviewed in Van Hautegem et al., 2015).

In the grasses, programmed cell death has a particular role to play in floral development. Maize flowers are initially hermaphroditic, but become either male or female through differential organ abortion. In male flowers, the female floral organs (the carpels) stop growing after they have formed, and eventually undergo programmed cell death. Programmed cell death in the carpels of the male maize floret is partially under the control of the transcription factor grassy tillers1. In gt1 mutants, the carpels in male flowers do not abort completely (Whipple et al.; Bartlett et al., 2015). However, gt1 mutant flowers are not fully hermaphroditic, indicating the existence of other genes that act with gt1 to regulate carpel abortion and programmed cell death. Which other genes are involved in carpel abortion? How do they interact with known sex determination genes in maize?

We have designed a series of genetic experiments geared at answering these questions. We will use mutant analysis to investigate whether gt1 is part of known sex determination pathways in maize. In addition, we have isolated four maize mutants where the gt1 mutant phenotype is strongly enhanced and programmed cell death in male flowers is disrupted. Using genetic and genomic tools, we will identify the genes that have been disrupted in these mutants, and work to determine their precise roles in mediating growth repression and programmed cell death. Surprisingly, gt1-like genes control growth repression and organ abortion not only in maize, but also in barley (a grass distantly related to maize) (Komatsuda et al., 2007), and even in persimmons (separated from grasses by more than 200 million years) (Akagi et al., 2014). In maize, barley, and persimmons, gt1- like genes are associated with the development of sterile or male flowers. However, sterile or male flowers have evolved separately in each lineage. Have gt1-like genes been repeatedly deployed throughout evolution to mediate floral sexuality? We will explore the expression of gt1-like genes in grass flowers from species spanning grass diversity. This sex determination project is uniquely suited for the Hatch program because it has the potential to considerably advance our knowledge of the fundamental mechanisms of grass development, while at the same time having transformative applications for crop design. Once we understand how growth repression is controlled in maize and other grasses, there is the potential for deactivating and activating growth repression at will, and drastically increasing cereal productivity. For example, rice flowers are hermaphroditic, which makes generating hybrid rice challenging. Targeted regulation of floral organ abortion has the potential to jump start hybrid rice breeding. Indeed, gt1-like genes were the targets of selection by ancient agronomists in both barley and maize [Komatsuda, 2007 #2179;Whipple, 2011 #2928;Wills, 2013 #3443]. As modern plant scientists, we can use our understanding of the genes and gene networks controlling plant development for rational crop design.