Abstract Background A 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 <it>CalS </it>gene family members in <it>Arabidopsis</it>, only one (<it>CalS5</it>) has been directly linked to pollen tube callose. <it>CalS5 </it>orthologues are present in several monocot and eudicot genomes, but little is known about the evolutionary origin of <it>CalS5 </it>or what its ancestral function may have been. Results We investigated expression of <it>CalS </it>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 <it>CalS5 </it>orthologue from <it>Cabomba caroliniana </it>(<it>CcCalS5</it>) (Nymphaeales). Semi-quantitative RT-PCR demonstrated low <it>CcCalS5 </it>expression within several vegetative tissues, but strong expression in mature pollen. <it>CalS </it>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 <it>CalS5</it>. We also report <it>in silico </it>evidence of a putative <it>CalS5 </it>orthologue from <it>Amborella</it>. Among gymnosperms, <it>CalS5 </it>transcripts were recovered from germinating pollen of <it>Gnetum </it>and <it>Ginkgo</it>, but a novel <it>CalS </it>paralog was instead amplified from germinating pollen of <it>Pinus taeda</it>. Conclusion The 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 <it>CalS5 </it>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.</p

Abercrombie, Jason M

Moffatt, Andrew R

O'Meara, Brian C

Williams, Joseph H

English

PubMed

Abstract
 
 Background
 A 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.
 
 
 Results
 We 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.
 
 
 Conclusion
 The 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.
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Jason M Abercrombie

Brian C O'Meara

Andrew R Moffatt

Joseph H Williams

Crossref

EvoDevo

Developmental evolution of flowering plant pollen tube cell walls: callose synthase (CalS) gene expression patterns

Springer - Publisher Connector

Abstract Background A 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. Results We 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. Conclusion The 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.</p

Abercrombie Jason M

O'Meara Brian C

Moffatt Andrew R

Williams Joseph H

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Developmental evolution of flowering plant pollen tube cell walls: callose synthase (<it>CalS</it>) gene expression patterns

A fast bootstrapping algorithm for the RAxML web-servers. Syst Biol

Amborella trichopoda (Amborellaceae) and the evolutionary developmental origins of the angiosperm progamic phase.

Ancestral angiosperm genome project.

Aspects of the structure, cytochemistry and germination of the pollen of rye (Secale cereale L.). Ann Bot

Bacic A: Location of cellulose and callose in pollen tubes and grains of Nicotiana tabacum. Planta

Bacic A: Proteomic and biochemical evidence links the callose synthase in Nicotiana alata pollen tubes to the product of the NaGSL1 gene. Plant J

Bairoch A: The PROSITE database, its status in 2002. Nucleic Acids Res

Callose (beta1,3 glucan) is essential for Arabidopsis pollen wall patterning, but not tube growth.

Callose microsporocyteaire et callose pollinique.

Cellulose biosynthesis. Annu Rev Plant Physiol

Cellulose synthases and related enzymes.

Cheung AY: Programmed cell death in plant reproduction. Plant Mol Bio

Coccuci AE: Importancia taxonomica de la calosa de los tubos polinicos en Tubiflorae. Kurtziana

Comparison of callose plug structure between dicotyledon and monocotyledon pollen germinated in vitro. Grana

Consequences of pollination syndrome evolution for post-pollination biology in an ancient angiosperm family.

Detection in primitive gymnosperms of proteins and glycoproteins of possible significance in reproduction. Nature

Distribution of callose synthase, cellulose synthase and sucrose synthase in tobacco pollen tube is controlled in dissimilar ways by actin filaments and microtubules. Plant Physiol

DL: Genetic applications of an inverse polymerase chain reaction. Genetics

DP: A cell plate-specific callose synthase and its interaction with phragmoplastin. Plant Cell

DP: Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant J

Dual function of Arabidopsis glucan synthase-like genes GSL8 and GSL10 in male gametophyte development and plant growth.

Functional interactions among cytoskeleton, membranes, and cell wall in the pollen tube of flowering plants. Int Rev Cytol

GB: An Arabidopsis Callose Synthase, GSL5, Is Required for Wound and Papillary Callose Formation. Plant Cell

Geitmann A: More than a leak sealant. The mechanical properties of callose in pollen tubes. Plant Physiol

Guerts H: The wall of Pinus sylvestris pollen tubes. Protoplasma

Hong Z: Plant callose synthase complexes. Plant Mol Biol

Immunochemical and cytochemical detection of wall components of germinated pollen of gymnosperms. Grana

Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol

JX: Isolation of de-exined pollen and cytotogical studies of the pollen intines of Pinus bungeana Zucc. Ex Endl. and Picea wilsonii Mast.

JY: Arabidopsis glucan synthase-like 10 functions in male gametogenesis.

Korban S: RNA extraction from different apple tissues rich in polyphenols and polysaccharides for cDNA library construction. Plant Mol Bio Rep

Kwak BH: The essential role of calcium ion in pollen germination and pollen tube growth.

MA: A duplicate gene rooting of seed plants and the phylogenetic position of flowering plants. Phil Trans Roy Soc B

Maddison DR: Mesquite: a modular system for evolutionary analysis.

Male gametophyte development and evolution in extant gymnosperms.

Malho R: cAMP acts as a second messenger in pollen tube growth and reorientation.

Microsporogenesis in Pinus sylvestris L. VIII. Tapetal and late pollen grain development. Plant Syst Evol

ML: Pollen tube growth and the pollen-tube pathway of Nymphaea odorata (Nymphaeaceae). Bot J Lin Soc

Molecular control of the glucan synthase-like protein NaGSL1 and callose synthesis during growth of Nicotiana alata pollen tubes.

Molecular mechanisms of pollen tube growth and differentiation. Plant Cell

Novelties of the flowering plant pollen tube underlie diversification of a key life history stage.

Organization and symmetry of microspores and origin of intine in Pinus sylvestris. Phytomorph

PBIL Network protein sequence analysis.

Phytozome: a tool for green plant comparative genomics.

Pollen tube development and characteristics of protein emission in conifers. Ann Bot

Pollen-pistil interactions. In Cellular Interactions. Edited by: Linskens HF, Heslop-Harrison J.

ProtTest: selection of best-fit models of protein evolution. Bioinformatics

PS: Polyploidy and angiosperm diversification.

RAxML-VI-HPC: Maximum Likelihood-based Phylogenetic Analyses with Thousands of Taxa and Mixed Models. Bioinformatics

Renzaglia KS: Novel localization of callose in the spores of Physcomitrella patens and phylogenomics of the callose synthase gene family. Ann Bot

Ripe pollen structure and histochemistry of some gymnosperms. Plant Syst Evol

SK: Perspective: the origin of flowering plants and their reproductive biology - a tale of two phylogenies. Evolution

SM: A novel callose synthase from pollen tubes of Nicotiana. Planta

SM: Pollen tubes of Nicotiana alata express two genes from different β-glucan synthase families.

SM: Uridine diphosphate glucose metabolism and callose synthesis in cultured pollen tubes of Nicotiana alata Link et Otto. Plant Phys

Staehelin A: Plant Cell Walls: from Chemistry to Biology

T: MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res

The “callose stage” of the generative cells in pollen grains. Grana

The CIPRES Portals.

The evolutionary history of the seed plant male gametophyte. Trends Ecol Evol

The location of 1,3-β-glucans in the walls of pollen tubes of Nicotiana alata using a 1,3-β-glucan-specific monoclonal antibody. Planta

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Ultrastructural and immunocytochemical demonstration of gametophytic proteins in the pollen tube wall of the primitive gymnosperm Cycas.

Vandepoele K: The flowering world: a tale of duplications. Trends Plant Sci

Vrba ES: Exaptation: a missing term in the science of form. Paleobiology

Waterkeyn L: Structure du pollen “ailé” chez les Coniféres. Cellule

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Developmental evolution of flowering plant pollen tube cell walls: callose synthase (CalS) gene expression patterns

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