Interorgan regulation of ethylene biosynthetic genes by pollination.

Abstract

Pollination initiates a syndrome of developmental events that contribute to successful reproduction, including perianth senescence, changes in pigmentation, and ovule differentiation in preparation for impending fertilization. In orchid flowers, initiation of each of these processes in distinct floral organs is strictly and coordinately controlled by pollination, thus providing a unique opportunity to study the signals that coordinate interorgan postpollination development. Because ethylene has been implicated in contributing to regulation of severa1 aspects of postpollination development, we focused on determining the expression of its biosynthetic genes and their possible role in regulation. The abundance of mRNA encoding both 1-aminocyclopropane-l-carboxylic acid (ACC) synthase and ACC oxidase in the stigma, ovary, and labellum was found to be coordinately regulated by emasculation, auxin, and ethylene. Although petals contribute up to 26% of total flower ethylene and accumulate high levels of ACC oxidase mRNA and activity following pollination, no ACC synthase mRNA or activity was detected in this tissue. Together, these results support a model of interorgan regulation of postpollination development that depends on pollination-stimulated accumulation of mRNA encoding ethylene biosynthetic enzymes in a developmentally regulated and tissue-specific manner. This model relies on the translocation of a soluble hormone precursor, ACC, rather than on the translocation of the hormone itself. In this way, ACC serves to actuate the response already initiated by ethylene perceived by other parts of the flower. Thus, ACC may function as a secondary transmissible signal that coordinates postpollination development in diverse floral organs.

Ovary and Gametophyte Development Are Coordinately Regulated by Auxin and Ethylene following Pollination.

“…A parallel study has demonstrated that the postpollination syndrome of development in orchids, including ovary development, involves coordinated interorgan regulation of expression of ethylene biosynthetic genes (ONeill et al, 1993). Together, these results present the foundation of a molecular model for the regulation of ovary, ovule, and gametophyte development by pollination.…”

“…Indeed, a model of auxin as the pollination signal was proposed by Burg and Dijkman (1967) whereby auxin from the pollen diffuses through the column where it stimulates ethylene production that in turn triggers senescence of the perianth. We have shown that pollination and auxin induce the expression of genes encoding ACC synthase and ACC oxidase in the gynoecium (ONeill et al, 1993). The pattern of expression is similar for both genes with either of these two stimuli.…”

“…Ethylene production was determined as previously described (ONeill et al, 1993). Briefly, detached whole flowers were sealed in gas-tight containers equipped with septa for 2 hr.…”

Programmed senescence of plant organs

“…Other flowers, such as petunia, gradually senesce over a period of days after flower opening, but this process is accelerated by pollination. In still other flowers perianth senescence is absolutely dependent on pollination and in these cases the external stimuli and endogenous signals that regulate programmed senescence have been examined in detail (O'Neill et al, 1993;O'Neill and Nadeau, 1997;O'Neill, 1997).…”

Mycotoxins reveal connections between plants and animals in apoptosis and ceramide signaling

“…Programmed cell death in plants: occurrence in development, disease and genetic lesions Programmed cell death regimes in plants are recognized to occur at specific points during development including senescence (Woodson et al, 1992;Smart, 1994), pollination (O'Neill et al, 1993;Zhang and O'Neil, 1993); tracheary element development (Chasan, 1994;Demura and Fukuda, 1994;Fukuda, 1994) and in the formation of aleurone cells in barley and wheat (Wang et al, 1996;Kuo et al, 1996). Analogous to apoptosis in animals, cell death may be triggered in response to pathogens (see reviews by Dangl, 1995;Keen, 1990;Lamb, 1994;Jones and Dangl, 1996;Morel and Dangl, 1997).…”