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Conservation of the abscission signaling peptide IDA during Angiosperm evolution: withstanding genome duplications and gain and loss of the receptors HAE/HSL2.

Stø IM, Orr RJ, Fooyontphanich K, Jin X, Knutsen JM, Fischer U, Tranbarger TJ, Nordal I, Aalen RB - Front Plant Sci (2015)

Bottom Line: Genes encoding IDA or IDA-LIKE (IDL) peptides and HSL proteins were found in all investigated species, which were selected as to represent each angiosperm order with available genomic sequences.IDA has been duplicated in eudicots to give rise to functionally divergent IDL peptides.We postulate that the high number of IDL homologs present in the core eudicots is a result of multiple whole genome duplications (WGD).

View Article: PubMed Central - PubMed

Affiliation: Section for Genetics and Evolutionary Biology, Department of Biosciences, University of Oslo Oslo, Norway.

ABSTRACT
The peptide INFLORESCENCE DEFICIENT IN ABSCISSION (IDA), which signals through the leucine-rich repeat receptor-like kinases HAESA (HAE) and HAESA-LIKE2 (HSL2), controls different cell separation events in Arabidopsis thaliana. We hypothesize the involvement of this signaling module in abscission processes in other plant species even though they may shed other organs than A. thaliana. As the first step toward testing this hypothesis from an evolutionarily perspective we have identified genes encoding putative orthologs of IDA and its receptors by BLAST searches of publically available protein, nucleotide and genome databases for angiosperms. Genes encoding IDA or IDA-LIKE (IDL) peptides and HSL proteins were found in all investigated species, which were selected as to represent each angiosperm order with available genomic sequences. The 12 amino acids representing the bioactive peptide in A. thaliana have virtually been unchanged throughout the evolution of the angiosperms; however, the number of IDL and HSL genes varies between different orders and species. The phylogenetic analyses suggest that IDA, HSL2, and the related HSL1 gene, were present in the species that gave rise to the angiosperms. HAE has arisen from HSL1 after a genome duplication that took place after the monocot-eudicots split. HSL1 has also independently been duplicated in the monocots, while HSL2 has been lost in gingers (Zingiberales) and grasses (Poales). IDA has been duplicated in eudicots to give rise to functionally divergent IDL peptides. We postulate that the high number of IDL homologs present in the core eudicots is a result of multiple whole genome duplications (WGD). We substantiate the involvement of IDA and HAE/HSL2 homologs in abscission by providing gene expression data of different organ separation events from various species.

No MeSH data available.


Related in: MedlinePlus

Evolution of the IDA HAE/HSL2 signaling module. Phylogeny of Angiosperms adapted from Zhang et al. (2012), Vanneste et al. (2014), Zeng et al. (2014), and Dohm et al. (2014). Taxonomical levels are taken from Zeng et al. (2014). Numbers in superscript behind order names represent the number of species used in the analysis. Order names in bold represent those orders with at least one completely sequenced genome. The two possible evolutionary origins of IDA (PIPQ) in monocots are illustrated.
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Figure 7: Evolution of the IDA HAE/HSL2 signaling module. Phylogeny of Angiosperms adapted from Zhang et al. (2012), Vanneste et al. (2014), Zeng et al. (2014), and Dohm et al. (2014). Taxonomical levels are taken from Zeng et al. (2014). Numbers in superscript behind order names represent the number of species used in the analysis. Order names in bold represent those orders with at least one completely sequenced genome. The two possible evolutionary origins of IDA (PIPQ) in monocots are illustrated.

Mentions: Our phylogenetic analyses of the HSL LRR-RLKs have revealed that the evolution of this receptor family is congruent with that of angiosperm species evolution, and makes it likely that the common ancestor of angiosperms had both a HSL1 and a HSL2 gene (Figure 7). Both receptors are present already in the basal angiosperm (e.g., Amborella), where stamen abscission is a common feature that facilitates the access of pollinators (beetles and flies bringing pollen from other flowers) to the female organ (Endress, 2010). The IDA gene with PIPR motif identified in Amborella, may play a role here, similar to IDA's role as a signaling ligand in sepal, petal, and stamen abscission in A. thaliana (Butenko et al., 2003, 2014).


Conservation of the abscission signaling peptide IDA during Angiosperm evolution: withstanding genome duplications and gain and loss of the receptors HAE/HSL2.

Stø IM, Orr RJ, Fooyontphanich K, Jin X, Knutsen JM, Fischer U, Tranbarger TJ, Nordal I, Aalen RB - Front Plant Sci (2015)

Evolution of the IDA HAE/HSL2 signaling module. Phylogeny of Angiosperms adapted from Zhang et al. (2012), Vanneste et al. (2014), Zeng et al. (2014), and Dohm et al. (2014). Taxonomical levels are taken from Zeng et al. (2014). Numbers in superscript behind order names represent the number of species used in the analysis. Order names in bold represent those orders with at least one completely sequenced genome. The two possible evolutionary origins of IDA (PIPQ) in monocots are illustrated.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4627355&req=5

Figure 7: Evolution of the IDA HAE/HSL2 signaling module. Phylogeny of Angiosperms adapted from Zhang et al. (2012), Vanneste et al. (2014), Zeng et al. (2014), and Dohm et al. (2014). Taxonomical levels are taken from Zeng et al. (2014). Numbers in superscript behind order names represent the number of species used in the analysis. Order names in bold represent those orders with at least one completely sequenced genome. The two possible evolutionary origins of IDA (PIPQ) in monocots are illustrated.
Mentions: Our phylogenetic analyses of the HSL LRR-RLKs have revealed that the evolution of this receptor family is congruent with that of angiosperm species evolution, and makes it likely that the common ancestor of angiosperms had both a HSL1 and a HSL2 gene (Figure 7). Both receptors are present already in the basal angiosperm (e.g., Amborella), where stamen abscission is a common feature that facilitates the access of pollinators (beetles and flies bringing pollen from other flowers) to the female organ (Endress, 2010). The IDA gene with PIPR motif identified in Amborella, may play a role here, similar to IDA's role as a signaling ligand in sepal, petal, and stamen abscission in A. thaliana (Butenko et al., 2003, 2014).

Bottom Line: Genes encoding IDA or IDA-LIKE (IDL) peptides and HSL proteins were found in all investigated species, which were selected as to represent each angiosperm order with available genomic sequences.IDA has been duplicated in eudicots to give rise to functionally divergent IDL peptides.We postulate that the high number of IDL homologs present in the core eudicots is a result of multiple whole genome duplications (WGD).

View Article: PubMed Central - PubMed

Affiliation: Section for Genetics and Evolutionary Biology, Department of Biosciences, University of Oslo Oslo, Norway.

ABSTRACT
The peptide INFLORESCENCE DEFICIENT IN ABSCISSION (IDA), which signals through the leucine-rich repeat receptor-like kinases HAESA (HAE) and HAESA-LIKE2 (HSL2), controls different cell separation events in Arabidopsis thaliana. We hypothesize the involvement of this signaling module in abscission processes in other plant species even though they may shed other organs than A. thaliana. As the first step toward testing this hypothesis from an evolutionarily perspective we have identified genes encoding putative orthologs of IDA and its receptors by BLAST searches of publically available protein, nucleotide and genome databases for angiosperms. Genes encoding IDA or IDA-LIKE (IDL) peptides and HSL proteins were found in all investigated species, which were selected as to represent each angiosperm order with available genomic sequences. The 12 amino acids representing the bioactive peptide in A. thaliana have virtually been unchanged throughout the evolution of the angiosperms; however, the number of IDL and HSL genes varies between different orders and species. The phylogenetic analyses suggest that IDA, HSL2, and the related HSL1 gene, were present in the species that gave rise to the angiosperms. HAE has arisen from HSL1 after a genome duplication that took place after the monocot-eudicots split. HSL1 has also independently been duplicated in the monocots, while HSL2 has been lost in gingers (Zingiberales) and grasses (Poales). IDA has been duplicated in eudicots to give rise to functionally divergent IDL peptides. We postulate that the high number of IDL homologs present in the core eudicots is a result of multiple whole genome duplications (WGD). We substantiate the involvement of IDA and HAE/HSL2 homologs in abscission by providing gene expression data of different organ separation events from various species.

No MeSH data available.


Related in: MedlinePlus