Abstract
Sex expression of dioecious buffalograss [Bouteloua dactyloides Columbus (syn. Buchloë dactyloides (Nutt.) Engelm.)] is known to be environmentally stable with approximate 1:1, male to female, sex ratios. Here we show that infection by the pistil smut fungus [Salmacisia buchloëana Huff & Chandra (syn. Tilletia buchloëana Kellerman and Swingle)] shifts sex ratios of buffalograss to be nearly 100% phenotypically hermaphroditic. In addition, pistil smut infection decreased vegetative reproductive allocation, increased most seed yield components, and increased pseudosexual reproductive allocation in both sex forms compared to uninfected clones. In female sex forms, pistil smut infection resulted in a 26 fold increase in ovary production and a 35 fold increase in potential harvest index. In male sex forms, pistil smut infection resulted in 2.37 fold increase in floret number and over 95% of these florets contained a well-developed pistil. Although all ovaries of infected plants are filled with fungal teliospores and hence reproductively sterile, an average male-female pair of infected plants exhibited an 87 fold increase in potential harvest index compared to their uninfected clones. Acquiring an ability to mimic the effects of pistil smut infection would enhance our understanding of the flowering process in grasses and our efforts to increase seed yield of buffalograss and perhaps other grasses.
Highlights
Sexual reproduction in perennial grasses is a complicated process requiring an orchestration of coordinated gene expression while adhering to a specific sequence of developmental events
The life cycle of pistil smut fungus begins as a germinating diploid teliospore in soil (Figure 1)
When the crown begins to differentiate from a vegetative meristem into a flowering apex, the pistil smut fungus interacts with the developmental process to induce female sex organs in its unisexual male hosts resulting in its namesake symptom of purple feathery pistillate stigmas exerting from “male” florets
Summary
Sexual reproduction in perennial grasses is a complicated process requiring an orchestration of coordinated gene expression while adhering to a specific sequence of developmental events. The buffalograss-pistil smut provides a non-threatening model system in which to explore the ability of smut infection to regulate its host sex expression, meristem determinacy, and resource allocation in order to enhance our understanding of the flowering process in grasses. We show that the parasitic pistil smut fungus demonstrates a remarkable ability to increase the overall sexual reproductive allocation of buffalograss by systematically enhancing various seed yield components of both male and female sex forms. If pistil smut’s ability to manipulate host pseudosexual reproductive allocation were better understood and capable of being realized without the fungus, it may benefit agriculture by improving the harvest index of grain crops in general and in perennial grain crops whose low seed yields have been problematic for commercialization [39]
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