Animal-mediated pollination is essential in plant reproductive biology and is often associated with pollination syndromes, sets of floral traits, such as color, scent, shape, or nectar content. Selection by pollinators is often considered a key factor in floral evolution and plant speciation. Our aim is the identification and characterization of the genetic changes that caused the evolution of divergent pollination syndromes in closely related plant species. We focus on ANTHOCYANIN2 (AN2), a welldefined myb-type transcription factor that is a major determinant of flower color variation between Petunia integrifolia and Petunia axillaris. Analysis of sequence variation in AN2 in wild P. axillaris accessions showed that loss-of-function alleles arose at least five times independently. DNA sequence analysis was complemented by functional assays for pollinator preference using genetic introgressions and transgenics. These results show that AN2 is a major determinant of pollinator attraction. Therefore, changes in a single gene cause a major shift in pollination biology and support the notion that the adaptation of a flowering plant to a new pollinator type may involve a limited number of genes of large effect. Gene identification and analysis of molecular evolution in combination with behavioral and ecological studies can ultimately unravel the evolutionary genetics of pollination syndromes.
Plant shoot development depends on the perpetuation of a group of undifferentiated cells in the shoot apical meristem (SAM). In the Petunia mutant hairy meristem (ham), shoot meristems differentiate postembryonically as continuations of the subtending stem. HAM encodes a putative transcription factor of the GRAS family, which acts non-cell-autonomously from L3-derived tissue of lateral organ primordia and stem provasculature. HAM acts in parallel with TERMINATOR (PhWUSCHEL) and is required for continued cellular response to TERMINATOR and SHOOTMERISTEMLESS (PhSTM). This reveals a novel mechanism by which signals from differentiating tissues extrinsically control stem cell fate in the shoot apex. Received March 11, 2002; revised version accepted June 18, 2002. Plants differ from animals in that they continuously form new organs (stems, leaves, or flowers) during postembryonic shoot development. This depends on the perpetuation of a shoot apical meristem (SAM) at the very summit of the growth axis. Within the SAM, a few stem cells are specified whose daughters give rise to the entire aerial plant body (for review, see Weigel and Jürgens 2002). A primary question in plant development is how the SAM is maintained and how stem cells are specified.A major signaling pathway that controls stem cell identity is mediated by the homeobox gene WUSCHEL (WUS). WUS is critical for SAM maintenance as judged by mutation (Laux et al. 1996) or by genetically programmed elimination during flower development (Lenhard et al. 2001;Lohmann et al. 2001). WUS expression is under negative feedback control of one of its target genes, CLAVATA3 (CLV3), which keeps stem cell maintenance and differentiation in dynamic equilibrium (Brand et al. 2000;Schoof et al. 2000). Other major factors that control SAM maintenance are the homeobox genes of the KNOTTED (KNOX) family. One of these, SHOOTMERISTEMLESS (STM), is thought to distinguish the SAM from lateral organs (Byrne et al. 2000). Ectopic KNOX expression can induce adventitious SAMs at sites that normally are fully differentiated (e.g., see Sinha et al. 1993).Factors like WUS, STM, and CLV are all expressed within undifferentiated cells of the SAM and are meristem intrinsic. There is evidence, however, that SAM development depends on extrinsic activities present in differentiating tissues. For example, SAM function can be affected by failures in lateral organ development or in the establishment of their ad-abaxial polarities (Waites et al. 1998;Lynn et al. 1999). Clearly, the SAM is intricately linked to its differentiating environment by noncell-autonomous control systems, the extent and molecular mechanisms of which are important issues.Here, we describe the GRAS gene HAIRY MERISTEM (HAM) of Petunia. HAM mediates a signal from lateral organ primordia and stem provasculature that is essential and specific for maintaining the SAM. This defines a novel pathway that links stem cell perpetuation to differentiation. Results and discussion HAIRY MERISTEM is required for meristem maintenanceThe ...
Animal-mediated pollination is essential in the reproductive biology of many flowering plants and tends to be associated with pollination syndromes, sets of floral traits that are adapted to particular groups of pollinators. The complexity and functional convergence of various traits within pollination syndromes are outstanding examples of biological adaptation, raising questions about their mechanisms and origins. In the genus Petunia, complex pollination syndromes are found for nocturnal hawkmoths (P. axillaris) and diurnal bees (P. integrifolia), with characteristic differences in petal color, corolla shape, reproductive organ morphology, nectar quantity, nectar quality, and fragrance. We dissected the Petunia syndromes into their most important phenotypic and genetic components. They appear to include several distinct differences, such as cell-growth and cell-division patterns in the basal third of the petals, elongation of the ventral stamens, nectar secretion and nectar sugar metabolism, and enzymatic differentiation in the phenylpropanoid pathway. In backcross-inbred lines of species-derived chromosome segments in a transposon tagging strain of P. hybrida, one to five quantitative trait loci were identified for each syndrome component. Two loci for stamen elongation and nectar volume were confirmed in introgression lines and showed large allelic differences. The combined data provide a framework for a detailed understanding of floral syndromes from their developmental and molecular basis to their impact on animal behavior. With its molecular genetic tools, this Petunia system provides a novel venue for a pattern of adaptive radiation that is among the most characteristic of flowering plants. SEXUAL reproduction in flowering plants is depennation by birds, bats, butterflies, or flies, each with distinct characteristics (Proctor et al. 1996). Pollination dent on the correct delivery of pollen grains to conspecific stigmata. In nature, the vectors for this delivery syndromes are outstanding examples of biological adaptation, involving a variety of developmental and physioare often animals that forage for pollen and nectar. Many flowers have evolved complex syndromes of morlogical systems. They raise questions about their genetic basis and the mutational steps that lead from one polliphological and physiological characters to attract and nation syndrome to another. reward pollinators and thereby to enhance the effiDifferent pollination syndromes can often be seen ciency and accuracy of pollen deposition (e.g., Proctor among closely related and sexually compatible sister et al. 1996). Pollinators are important factors for the species, enabling their genetic dissection. For example, evolution of variety in floral display among angiosperms interspecific crosses of bird-and bee-pollinated species and in some cases can contribute to reproductive isolaof the genus Mimulus (Bradshaw et al. 1995; Bradtion by differential visitation (e.g., Grant 1994).shaw et al. 1998) have suggested a relatively simple In m...
The composition and timing of flower odour emission by wild Petunia axillaris coincide with the antennal perception and nocturnal activity of the pollinator Manduca sexta Abstract In the genus Petunia, distinct pollination syndromes may have evolved in association with bee-visitation (P. integrifolia spp.) or hawk moth-visitation (P. axillaris spp). We investigated the extent of congruence between floral fragrance and olfactory perception of the hawk moth Manduca sexta. Hawk moth pollinated P. axillaris releases high levels of several compounds compared to the bee-pollinated P. integrifolia that releases benzaldehyde almost exclusively. The three dominating compounds in P. axillaris were benzaldehyde, benzyl alcohol and methyl benzoate. In P. axillaris, benzenoids showed a circadian rhythm with an emission peak at night, which was absent from P. integrifolia. These characters were highly conserved among different P. axillaris subspecies and P. axillaris accessions, with some differences in fragrance composition. Electroantennogram (EAG) recordings using flower-blends of different wild Petunia species on female M. sexta antennae showed that P. axillaris odours elicited stronger responses than P. integrifolia odours. EAG responses were highest to the three dominating compounds in the P. axillaris flower odours. Further, EAG responses to odour-samples collected from P. axillaris flowers confirmed that odours collected at night evoked stronger responses from M. sexta than odours collected during the day. These results show that timing of odour emissions by P. axillaris is in tune with nocturnal hawk moth activity and that flower-volatile composition is adapted to the antennal perception of these pollinators.
SUMMARYMost terrestrial plants engage into arbuscular mycorrhizal (AM) symbiosis with fungi of the phylum Glomeromycota. The initial recognition of the fungal symbiont results in the activation of a symbiosis signalling pathway that is shared with the root nodule symbiosis (common SYM pathway). The subsequent intracellular accommodation of the fungus, and the elaboration of its characteristic feeding structures, the arbuscules, depends on a genetic programme in the plant that has recently been shown to involve the VAPYRIN gene in Medicaco truncatula. We have previously identified a mutant in Petunia hybrida, penetration and arbuscule morphogenesis 1 (pam1), that is defective in the intracellular stages of AM development. Here, we report on the cloning of PAM1, which encodes a VAPYRIN homologue. PAM1 protein localizes to the cytosol and the nucleus, with a prominent affinity to mobile spherical structures that are associated with the tonoplast, and are therefore referred to as tonospheres. In mycorrhizal roots, tonospheres were observed in the vicinity of intracellular hyphae, where they may play an essential role in the accommodation and morphogenesis of the fungal endosymbiont.
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