Three 1-Aminocyclopropane-1-Carboxylate Synthase Genes Regulated by Primary and Secondary Pollination Signals in Orchid Flowers1

Abstract

The temporal and spatial expression patterns of three 1-aminocyclopropane-1-carboxylate (ACC) synthase genes were investigated in pollinated orchid (Phalaenopsis spp.) flowers. Pollination signals initiate a cascade of development events in multiple floral organs, including the induction of ethylene biosynthesis, which coordinates several postpollination developmental responses. The initiation and propagation of ethylene biosynthesis is regulated by the coordinated expression of three distinct ACC synthase genes in orchid flowers. One ACC synthase gene (Phal-ACS1) is regulated by ethylene and participates in amplification and interorgan transmission of the pollination signal, as we have previously described in a related orchid genus. Two additional ACC synthase genes (Phal-ACS2 and Phal-ACS3) are expressed primarily in the stigma and ovary of pollinated orchid flowers. Phal-ACS2 mRNA accumulated in the stigma within 1 h after pollination, whereas Phal-ACS1 mRNA was not detected until 6 h after pollination. Similar to the expression of Phal-ACS2, the Phal-ACS3 gene was expressed within 2 h after pollination in the ovary. Exogenous application of auxin, but not ACC, mimicked pollination by stimulating a rapid increase in ACC synthase activity in the stigma and ovary and inducing Phal-ACS2 and Phal-ACS3 mRNA accumulation in the stigma and ovary, respectively. These results provide the basis for an expanded model of interorgan regulation of three ACC synthase genes that respond to both primary (Phal-ACS2 and Phal-ACS3) and secondary (Phal-ACS1) pollination signals.Pollination of flowers is a key regulatory event in plant reproduction. In many flowers pollination causes an initial, dramatic increase in ethylene production in the stigma and style and a subsequent increase in ethylene production by other floral organs. Moreover, ethylene has been shown to play a regulatory role in postpollination developmental events (Larsen et al

Whole Genome Analysis of Gene Expression Reveals Coordinated Activation of Signaling and Metabolic Pathways during Pollen-Pistil Interactions in Arabidopsis

“…A comparison between tissue and time-course expression allowed us to determine that 78% (1,066) of the regulated transcripts were first expressed before pollination in UP or unfertilized ovules, 7% (96) were exclusively induced by pollination (absent in any other tissue directly involved in the reproductive process), 12% (170) represent transcripts identified initially as preferentially expressed in our pollen data set (absent from UP or ovules), and 3% (36) were enriched (Supplemental File S2). Despite the predominant expression of genes in the pistil at receptivity, only a few proteins expressed in the sporophytic female tissues were identified with functions in pollen-pistil interactions (Wu et al, 2000;de Graaf et al, 2003;Palanivelu et al, 2003;Park and Lord, 2003), and only one gene was identified to be strictly induced by pollination (Bui and O'Neill, 1998). The comparison of our time-course data set with recently reported transcriptomes of in vitro (Wang et al, 2008) and semi-in vitro pollen tube growth (Qin et al, 2009) confirmed an expected overlap of multiple genes "de novo" transcribed during pollen tube growth and possibly induced due to interactions with the female tissues.…”

Differential Expression of Three Members of the 1-Aminocyclopropane-1-Carboxylate Synthase Gene Family in Carnation1

“…Four of the ACC synthase genes in tomato have been shown to be differentially regulated in fruit and hypocotyls during ripening by wounding and auxin treatment . ACC synthase mRNAs are also induced during flower senescence and following pollination in carnation and orchid Woodson et al, 1992;O'Neill et al, 1993;Jones and Woodson, 1997;Bui and O'Neill, 1998). Few studies of other species have included the investigation of ACC synthase expression in floral tissue.…”

“…Highly divergent ACC synthase multigene families have been identified and characterized in Arabidopsis (Liang et al, 1992(Liang et al, , 1996; Van der Straeten et al, 1992), tomato (Olson et al, 1991;Rottmann et al, 1991;Yip et al, 1992;Lincoln et al, 1993;Oetiker et al, 1997), mung bean (Botella et al, 1992a(Botella et al, , 1992b(Botella et al, , 1993Kim et al, 1992Kim et al, , 1997, zucchini (Huang et al, 1991), rice (Zarembinski and Theologis, 1993), potato (Destefano-Beltran et al, 1995;Schlagnhaufer et al, 1995), and orchid (Bui and O'Neill, 1998). The Arabidopsis gene family includes at least five members whose expression is differentially induced by hormones, developmental cues, Li ϩ , and the protein-synthesis inhibitor CHX (Liang et al, 1996).…”

Role of Auxin in Orchid Development

“…13,14 Moreover, auxin up-regulated the ethylene biosythethic genes in Phalaenopsis, Phal-ACS2 and Phal-ACS3, and auxin-induced ethylene production was secondarily enhanced through ethylene-stimulated Phal-ACS1 expression. 30 Independent of ethylene, auxin treatment depressed transcript levels of the Phalaenopsis gene, PeMADS6, whose function is to sustain the life of the floral parts while inhibiting the completion of ovary and ovule maturation after pollination. 32 However, both auxin and ethylene response elements have been identified in the promoter region of PeMADS6, implicating both hormones in this pollination-induced shift in gene expression.…”

“…13,14,29 Most of these changes are mediated through auxin-stimulated ethylene production. [29][30][31] In fact, a combination of auxin and ethylene are needed for optimal ovary/ovule development. The addition of ethylene antagonists to pollinated or unpollinated, NAA-treated stigmas resulted in partial stigmatal closure and moderate ovary swelling, and only a small amount of perianth senescence, while ethylene alone promoted death of the perianth without ovary enlargement or closure of the stigma.…”