Abstract
BackgroundA number of innovations underlie the origin of rapid reproductive cycles in angiosperms. A critical early step involved the modification of an ancestrally short and slow-growing pollen tube for faster and longer distance transport of sperm to egg. Associated with this shift are the predominantly callose (1,3-β-glucan) walls and septae (callose plugs) of angiosperm pollen tubes. Callose synthesis is mediated by callose synthase (CalS). Of 12 CalS gene family members in Arabidopsis, only one (CalS5) has been directly linked to pollen tube callose. CalS5 orthologues are present in several monocot and eudicot genomes, but little is known about the evolutionary origin of CalS5 or what its ancestral function may have been.ResultsWe investigated expression of CalS in pollen and pollen tubes of selected non-flowering seed plants (gymnosperms) and angiosperms within lineages that diverged below the monocot/eudicot node. First, we determined the nearly full length coding sequence of a CalS5 orthologue from Cabomba caroliniana (CcCalS5) (Nymphaeales). Semi-quantitative RT-PCR demonstrated low CcCalS5 expression within several vegetative tissues, but strong expression in mature pollen. CalS transcripts were detected in pollen tubes of several species within Nymphaeales and Austrobaileyales, and comparative analyses with a phylogenetically diverse group of sequenced genomes indicated homology to CalS5. We also report in silico evidence of a putative CalS5 orthologue from Amborella. Among gymnosperms, CalS5 transcripts were recovered from germinating pollen of Gnetum and Ginkgo, but a novel CalS paralog was instead amplified from germinating pollen of Pinus taeda.ConclusionThe finding that CalS5 is the predominant callose synthase in pollen tubes of both early-diverging and model system angiosperms is an indicator of the homology of their novel callosic pollen tube walls and callose plugs. The data suggest that CalS5 had transient expression and pollen-specific functions in early seed plants and was then recruited to novel expression patterns and functions within pollen tube walls in an ancestor of extant angiosperms.
Highlights
A number of innovations underlie the origin of rapid reproductive cycles in angiosperms
Putative orthologues of CalS5 are expressed in pollen and pollen tubes of early-diverging angiosperms A nearly full length coding sequence was obtained from Cabomba caroliniana (Cabombaceae; Nymphaeales) (CcCalS5) comprising 5,562 bp which translated into a predicted 1854 amino acid polypeptide with 78% identity to Arabidopsis thaliana CalS5 (AtCalS5) and 66% identity to the moss orthologue (PpCalS5) from the Physcomitrella patens genome [25]
A 1,497 bp nucleotide sequence that shared 100% nucleotide identity with the Cabomba caroliniana CalS5 (CcCalS5) was amplified from N. odorata pollen and was used to designate the Nymphaea CalS5 orthologue (NoCalS5) in our RT-PCR experiments (Figure 1B)
Summary
A number of innovations underlie the origin of rapid reproductive cycles in angiosperms. In conifers and Gnetales pollen tubes function in a new way to deliver non-motile sperm to the egg (siphonogamy), while generally retaining a haustorial growth pattern [2,3]. Flowering plant (angiosperm) pollen tubes have lost most features of haustorial growth - their pollen tubes are typically short-lived and seem to function exclusively to deliver sperm to the egg [4,5]. The origin of siphonogamy has been held up as a classic example of exaptation [6], because the plesiomorphic function of the pollen tube - nutritional support for the male gametophyte - was subsequently co-opted for a novel role in sperm delivery [3]. Understanding the homologies of pollen tube structure and growth pattern may provide deeper insights into the origin(s) of this remarkable innovation
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