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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

Modes of abscission. (A) Abscission of (a) sepals, (b) petals, (c) stamen, and (d) carpels. (B) Abscission of leaves at the axil of the pedicel, and abscission of entire male inflorescence (catkin) in Populus spp. (C) Opening of valves in dehiscence zones of dry many-seeded capsules, and abscission of individual seeds. (D) Abscission of fleshy fruits at AZ on pedicel. (E) The oil palm drupe fruit are tightly arranged within spikelets and abscise one by one when ripe. (A–D) Image courtesy the private collection of Roy Winkelman. First published in Gray (1858) and Foster (1921). (E) Image courtesy Missouri Botanical Garden. http://www.botanicus.org.
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Figure 5: Modes of abscission. (A) Abscission of (a) sepals, (b) petals, (c) stamen, and (d) carpels. (B) Abscission of leaves at the axil of the pedicel, and abscission of entire male inflorescence (catkin) in Populus spp. (C) Opening of valves in dehiscence zones of dry many-seeded capsules, and abscission of individual seeds. (D) Abscission of fleshy fruits at AZ on pedicel. (E) The oil palm drupe fruit are tightly arranged within spikelets and abscise one by one when ripe. (A–D) Image courtesy the private collection of Roy Winkelman. First published in Gray (1858) and Foster (1921). (E) Image courtesy Missouri Botanical Garden. http://www.botanicus.org.

Mentions: Fall of whole flowers is less common than floral organ abscission (Figure 5A), but occurs in both monocot and eudicot species, when pollination or fertilization fail (van Doorn, 2002). Abscission of immature fruit is a normal event in several cultivated species. In Citrus spp. (Sapindales), abscission of flowers and young fruit results from cell separation at an AZ at the base of the floral pedicel. The CicIDA3 gene, expressed in Citrus clementina AZs, encodes a protein with a PIP motif identical to mIDA with the exception of a Gly instead of an Ala in position 6 (Estornell et al., submitted). Overexpression of CicIDA3 in A. thaliana induced the same phenotypic changes as have been shown for overexpression of IDA and AtIDL1 (Figures 4A–D) (Estornell et al., submitted), suggesting that the citrus prepropeptide undergo the correct processing, that the Citrus peptide can activate IDA's receptors and thus provides experimental evidence supporting a function in citrus abscission events.


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)

Modes of abscission. (A) Abscission of (a) sepals, (b) petals, (c) stamen, and (d) carpels. (B) Abscission of leaves at the axil of the pedicel, and abscission of entire male inflorescence (catkin) in Populus spp. (C) Opening of valves in dehiscence zones of dry many-seeded capsules, and abscission of individual seeds. (D) Abscission of fleshy fruits at AZ on pedicel. (E) The oil palm drupe fruit are tightly arranged within spikelets and abscise one by one when ripe. (A–D) Image courtesy the private collection of Roy Winkelman. First published in Gray (1858) and Foster (1921). (E) Image courtesy Missouri Botanical Garden. http://www.botanicus.org.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 5: Modes of abscission. (A) Abscission of (a) sepals, (b) petals, (c) stamen, and (d) carpels. (B) Abscission of leaves at the axil of the pedicel, and abscission of entire male inflorescence (catkin) in Populus spp. (C) Opening of valves in dehiscence zones of dry many-seeded capsules, and abscission of individual seeds. (D) Abscission of fleshy fruits at AZ on pedicel. (E) The oil palm drupe fruit are tightly arranged within spikelets and abscise one by one when ripe. (A–D) Image courtesy the private collection of Roy Winkelman. First published in Gray (1858) and Foster (1921). (E) Image courtesy Missouri Botanical Garden. http://www.botanicus.org.
Mentions: Fall of whole flowers is less common than floral organ abscission (Figure 5A), but occurs in both monocot and eudicot species, when pollination or fertilization fail (van Doorn, 2002). Abscission of immature fruit is a normal event in several cultivated species. In Citrus spp. (Sapindales), abscission of flowers and young fruit results from cell separation at an AZ at the base of the floral pedicel. The CicIDA3 gene, expressed in Citrus clementina AZs, encodes a protein with a PIP motif identical to mIDA with the exception of a Gly instead of an Ala in position 6 (Estornell et al., submitted). Overexpression of CicIDA3 in A. thaliana induced the same phenotypic changes as have been shown for overexpression of IDA and AtIDL1 (Figures 4A–D) (Estornell et al., submitted), suggesting that the citrus prepropeptide undergo the correct processing, that the Citrus peptide can activate IDA's receptors and thus provides experimental evidence supporting a function in citrus abscission events.

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