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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

IDA and IDL peptides. (A) Structure of IDA and IDL prepropeptides. (B–D) Peptide consensus sequences as indicated. The alignment used for the construction of the peptide logos is available as Supplementary Data Sheet 3.
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Figure 3: IDA and IDL peptides. (A) Structure of IDA and IDL prepropeptides. (B–D) Peptide consensus sequences as indicated. The alignment used for the construction of the peptide logos is available as Supplementary Data Sheet 3.

Mentions: IDA and IDL are secreted peptides generated from prepropeptides (Figure 3A), where the hydrophobic N-terminus is a signal directing the protein to the secretory pathway. The variable middle part and the C-terminus are assumed to be cleaved off in the apoplastic space to release a mature 12 aa peptide named PIP after the three first residues, PIPPSAPSKRHN (Butenko et al., 2003). Synthetic mIDA peptide with hydroxylation on the central proline (Pro, P) can bind and activate HSL2 efficiently, and HAE at a higher concentration (Butenko et al., 2014). The Pro residues in positions 2, 3, and 7, serine (Ser, S) in positions 5 and 10, and histidine (His, H) asparagine (Asn, N) at the end are found in all A. thaliana IDA/IDL peptide sequences. Experiments where the part of the AtIDA gene encoding PIP was swapped with the corresponding AtIDL sequence and the recombinant AtIDA-IDL gene introduced in the ida mutant, indicate the importance of different aa residues (Stenvik et al., 2008). The AtIDL1 peptide (LVPPSGPSMRHN) complements the mutation, suggesting that the initial Pro is of little importance, that the hydrophobic isoleucine (Ile, I) and the small central Ala residues can be exchanged with the hydrophobic valine (Val, V) and the small Gly, respectively, without affecting the biological activity, and furthermore that a positively charged aa in position 9 is no absolute requirement. In contrast, AtIDL2, AtIDL3, AtIDL4, and AtIDL5 cannot fully complement the ida mutation (Stenvik et al., 2008). Their PIP motifs are characterized by arginine-lysine (ArgLys, RK) in position 9 and 10, in contrast to the LysArg (KR) found in mIDA.


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)

IDA and IDL peptides. (A) Structure of IDA and IDL prepropeptides. (B–D) Peptide consensus sequences as indicated. The alignment used for the construction of the peptide logos is available as Supplementary Data Sheet 3.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 3: IDA and IDL peptides. (A) Structure of IDA and IDL prepropeptides. (B–D) Peptide consensus sequences as indicated. The alignment used for the construction of the peptide logos is available as Supplementary Data Sheet 3.
Mentions: IDA and IDL are secreted peptides generated from prepropeptides (Figure 3A), where the hydrophobic N-terminus is a signal directing the protein to the secretory pathway. The variable middle part and the C-terminus are assumed to be cleaved off in the apoplastic space to release a mature 12 aa peptide named PIP after the three first residues, PIPPSAPSKRHN (Butenko et al., 2003). Synthetic mIDA peptide with hydroxylation on the central proline (Pro, P) can bind and activate HSL2 efficiently, and HAE at a higher concentration (Butenko et al., 2014). The Pro residues in positions 2, 3, and 7, serine (Ser, S) in positions 5 and 10, and histidine (His, H) asparagine (Asn, N) at the end are found in all A. thaliana IDA/IDL peptide sequences. Experiments where the part of the AtIDA gene encoding PIP was swapped with the corresponding AtIDL sequence and the recombinant AtIDA-IDL gene introduced in the ida mutant, indicate the importance of different aa residues (Stenvik et al., 2008). The AtIDL1 peptide (LVPPSGPSMRHN) complements the mutation, suggesting that the initial Pro is of little importance, that the hydrophobic isoleucine (Ile, I) and the small central Ala residues can be exchanged with the hydrophobic valine (Val, V) and the small Gly, respectively, without affecting the biological activity, and furthermore that a positively charged aa in position 9 is no absolute requirement. In contrast, AtIDL2, AtIDL3, AtIDL4, and AtIDL5 cannot fully complement the ida mutation (Stenvik et al., 2008). Their PIP motifs are characterized by arginine-lysine (ArgLys, RK) in position 9 and 10, in contrast to the LysArg (KR) found in mIDA.

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