Functional Dioecy in Echinocereus: Ontogenetic Patterns, Programmed Cell Death, and Evolutionary Significance

Abstract

Premise of research. Dioecy has evolved numerous times among unrelated Cactaceae taxa. Changes in ontogenetic patterns determine final floral morphology and breeding system. It has not been established whether these changes share a common pattern in the cactus family, which would allow inferences to be made in the evolutionary process that underlies the development of unisexual flowers. Echinocereus has related hermaphroditic and dioecious taxa, which makes it a useful system to determine how transitions from hermaphroditic to unisexual flowers occur.Methodology. Sexual systems in five Echinocereus taxa were determined using controlled pollinations and field observations of floral morphology and fruit-set patterns. Floral and seed development were analyzed using histological observations and scanning electron microscopy; a TUNEL assay was used as an indicator of DNA fragmentation to corroborate programmed cell death during floral and seed development.Pivotal results. Changes in ontogenetic patterns result in unisexual flower development in four species of Echinocereus section Triglochidiati (Cactaceae). Populations of E. coccineus, E. polyacanthus, E. pacificus, and E. mombergerianus are functionally dioecious, whereas E. triglochidiatus is hermaphroditic. At anthesis, the male (female-sterile) flowers of dioecious species exhibit a fully developed gynoecium with ovules where, after fertilization, seeds are aborted at early stages of postzygotic development. Flowers on female (male-sterile) plants do not form pollen grains in any of the dioecious species. Programmed cell death mediates both seed and pollen abortion. We propose that heterochrony controls male sterility by accelerating the process of programmed cell death in tapetal cells during anther development in female flowers.Conclusions. Dioecious taxa of Echinocereus share the ontogenetic pattern of male and female sterility. We provide groundwork for future research on developmental pathways of unisexual flowers in closely related taxa in Cactaceae, as well as the embryological framework to elucidate the molecular/genetic mechanisms involved in the development of unisexuality.