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 several aspects of postpollination development (Zhang and O'Neill, accompanying paper), we focused on understanding regulation of its biosynthetic genes in response to pollination-associated factors and in different floral organs. The abundance of mRNA encoding both ACC synthase and ACC oxidase was found to be coordinately regulated by emasculation, auxin and ethylene in the stigma, ovary and labellum. In petals, however, ACC synthase mRNA and activity were not detected in spite of high levels of ACC oxidase mRNA and activity following pollination and in spite of the observation that petals contribute approximately 25% of the total ethylene produced by orchid flowers at the climacteric peak. Together, the 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. Pollination provides the primary signal that induces the accumulation of ACC synthase mRNA and enzyme activity in the stigma. This activity leads to the accumulation of the ethylene hormone precursor, 1-aminocyclopropane-1-carboxylic acid (ACC) which is converted to ethylene by a low basal level of ACC oxidase present in stigma tissue. This ethylene acts autocatalytically to further stimulate ACC synthase and ACC oxidase mRNA accumulation in the gynoecium. Since ACC synthase mRNA does not accumulate to detectable levels in the perianth, excluding the labellum, but substantial ethylene is produced by this tissue, ethylene production must be supported by ACC translocation from its site of synthesis in the stigma, ovary and/or labellum to the rest of the perianth. This mechanism relies on the translocation of a soluble hormone precursor rather than on the translocation of the hormone itself. However, the translocated precursor, ACC, serves to actuate the response already initiated by ethylene perceived by other parts of the flower. Thus, ACC functions as a secondary transmissible signal that communicates to other parts of the flower that pollination has occurred, but the primary signal is ethylene produced by the column.