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A conserved role for the ARC1 E3 ligase in Brassicaceae self-incompatibility.

Indriolo E, Goring DR - Front Plant Sci (2014)

Bottom Line: In the Brassicaceae (mustard family), self-incompatibility drives the rejection of self-pollen by preventing pollen hydration following pollen contact with the stigmatic surface.Self-pollen is recognized by a ligand-receptor pair: the pollen S-locus cysteine rich/S-locus protein 11 (SCR/SP11) ligand and the pistil S receptor kinase (SRK).Following self-pollen contact, the SCR/SP11 ligand on the pollen surface binds to SRK on the pistil surface, and the SRK-activated signaling pathway is initiated.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell & Systems Biology, University of Toronto Toronto, ON, Canada.

ABSTRACT
Ubiquitination plays essential roles in the regulation of many processes in plants including pollen rejection in self-incompatible species. In the Brassicaceae (mustard family), self-incompatibility drives the rejection of self-pollen by preventing pollen hydration following pollen contact with the stigmatic surface. Self-pollen is recognized by a ligand-receptor pair: the pollen S-locus cysteine rich/S-locus protein 11 (SCR/SP11) ligand and the pistil S receptor kinase (SRK). Following self-pollen contact, the SCR/SP11 ligand on the pollen surface binds to SRK on the pistil surface, and the SRK-activated signaling pathway is initiated. This pathway includes the armadillo repeat containing 1 (ARC1) protein, a member of the plant U-box (PUB) family of E3 ubiquitin ligases. ARC1 is a functional E3 ligase and is required downstream of SRK for the self-incompatibility response. This mini review highlights our recent progress in establishing ARC1's conserved role in self-pollen rejection in Brassica and Arabidopsis species and discusses future research directions in this field.

No MeSH data available.


Related in: MedlinePlus

Model for the Self-Incompatibility response in Arabidopsis. Upon pollen contact with the stigmatic papilla, the papilla must determine if the pollen grain is self or non-self. For a self-pollen grain, the SCR/SP11 ligand binds to SRK, and SRK will then become phosphorylated. ARC1 interacts with the phosphorylated cytoplasmic kinase domain of SRK and become phosphorylated and activated. ARC1 then seeks its target for ubiquitination, Exo70A1, which is located at the plasma membrane in preparation for exocyst-mediated exocytosis. ARC1, with the help of an E1 activating enzyme and E2 conjugating enzyme, ubiquitinates Exo70A1. The nature of this ubiquitination is not known, as it could be either mono-ubiqitination resulting in Exo70A1 relocalization, or poly ubiquitination leading to degradation of Exo70A1 by the 26S proteosome. Either way, the inhibition of Exo70A1 appears to activate an autophagic response that leads to degradation of the secretory vesicles. There is also another (unknown) factor functioning downstream of SRK in this pathway. How ARC1, this factor, and the ubiquitination of Exo70A1 signals for autophagy is not known. Once the secretory vesicles have been removed, the self-pollen grain will not receive the resources needed for hydration and germination; as a result will be rejected.
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Figure 1: Model for the Self-Incompatibility response in Arabidopsis. Upon pollen contact with the stigmatic papilla, the papilla must determine if the pollen grain is self or non-self. For a self-pollen grain, the SCR/SP11 ligand binds to SRK, and SRK will then become phosphorylated. ARC1 interacts with the phosphorylated cytoplasmic kinase domain of SRK and become phosphorylated and activated. ARC1 then seeks its target for ubiquitination, Exo70A1, which is located at the plasma membrane in preparation for exocyst-mediated exocytosis. ARC1, with the help of an E1 activating enzyme and E2 conjugating enzyme, ubiquitinates Exo70A1. The nature of this ubiquitination is not known, as it could be either mono-ubiqitination resulting in Exo70A1 relocalization, or poly ubiquitination leading to degradation of Exo70A1 by the 26S proteosome. Either way, the inhibition of Exo70A1 appears to activate an autophagic response that leads to degradation of the secretory vesicles. There is also another (unknown) factor functioning downstream of SRK in this pathway. How ARC1, this factor, and the ubiquitination of Exo70A1 signals for autophagy is not known. Once the secretory vesicles have been removed, the self-pollen grain will not receive the resources needed for hydration and germination; as a result will be rejected.

Mentions: Armadillo repeat-containing 1 was originally identified in B. napus, through a yeast two-hybrid screen for SRK kinase domain interactors, and ARC1 was found to bind to SRK through its ARM repeat domain (Gu et al., 1998). ARC1 can be phosphorylated by SRK, but is more strongly phosphorylated by MLPK in vitro (Gu et al., 1998; Samuel et al., 2008). ARC1 is composed of the three distinct protein domains described above (UND, U-box, ARM repeat domain), and has functional nuclear localization and nuclear export signals. When transiently expressed in tobacco BY2 cells, ARC1 was localized to both the cytoplasm and nucleus, shuttling back and forth between these two compartments (Stone et al., 2003). The function of ARC1’s nuclear localization is still unclear, especially as it is expected to be near the plasma membrane for its role in self-incompatibility (Figure 1, described in more detail below). When ARC1 was co-expressed with active SRK or MLPK kinase domains, it no longer shuttled to the nucleus suggesting that ARC1 phosphorylation alters its localization and may be important for its function in the self-incompatibility pathway (Stone et al., 2003; Samuel et al., 2008). B. napus ARC1 displays stigma-specific expression, and the knock-down of ARC1 expression by antisense suppression resulted in a gained self-pollen acceptance, instead of rejection, indicating a breakdown in the self-incompatible pathway (Gu et al., 1998; Stone et al., 1999). ARC1 was shown to have in vitro E3 ligase activity, and the importance of ubiquitination in self-incompatibility came from analyses of ubiquitinated proteins in the stigma. Wild-type B. napus stigmas that were pollinated with self-incompatible pollen were shown, by immunoblotting with an anti-ubiquitin antibody, to be enriched in ubiquitinated proteins (Stone et al., 2003; Samuel et al., 2011). In contrast, self-pollinated ARC1-antisense-suppressed stigmas had a lower level of ubiquitinated proteins. Therefore, these data suggest that the presence of ARC1 led to ubiquitinated stigma proteins following self-incompatible pollinations. Given that all this work was done in B. napus, an outstanding question in the field was whether ARC1’s function was conserved in other Brassicaceae species.


A conserved role for the ARC1 E3 ligase in Brassicaceae self-incompatibility.

Indriolo E, Goring DR - Front Plant Sci (2014)

Model for the Self-Incompatibility response in Arabidopsis. Upon pollen contact with the stigmatic papilla, the papilla must determine if the pollen grain is self or non-self. For a self-pollen grain, the SCR/SP11 ligand binds to SRK, and SRK will then become phosphorylated. ARC1 interacts with the phosphorylated cytoplasmic kinase domain of SRK and become phosphorylated and activated. ARC1 then seeks its target for ubiquitination, Exo70A1, which is located at the plasma membrane in preparation for exocyst-mediated exocytosis. ARC1, with the help of an E1 activating enzyme and E2 conjugating enzyme, ubiquitinates Exo70A1. The nature of this ubiquitination is not known, as it could be either mono-ubiqitination resulting in Exo70A1 relocalization, or poly ubiquitination leading to degradation of Exo70A1 by the 26S proteosome. Either way, the inhibition of Exo70A1 appears to activate an autophagic response that leads to degradation of the secretory vesicles. There is also another (unknown) factor functioning downstream of SRK in this pathway. How ARC1, this factor, and the ubiquitination of Exo70A1 signals for autophagy is not known. Once the secretory vesicles have been removed, the self-pollen grain will not receive the resources needed for hydration and germination; as a result will be rejected.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4017152&req=5

Figure 1: Model for the Self-Incompatibility response in Arabidopsis. Upon pollen contact with the stigmatic papilla, the papilla must determine if the pollen grain is self or non-self. For a self-pollen grain, the SCR/SP11 ligand binds to SRK, and SRK will then become phosphorylated. ARC1 interacts with the phosphorylated cytoplasmic kinase domain of SRK and become phosphorylated and activated. ARC1 then seeks its target for ubiquitination, Exo70A1, which is located at the plasma membrane in preparation for exocyst-mediated exocytosis. ARC1, with the help of an E1 activating enzyme and E2 conjugating enzyme, ubiquitinates Exo70A1. The nature of this ubiquitination is not known, as it could be either mono-ubiqitination resulting in Exo70A1 relocalization, or poly ubiquitination leading to degradation of Exo70A1 by the 26S proteosome. Either way, the inhibition of Exo70A1 appears to activate an autophagic response that leads to degradation of the secretory vesicles. There is also another (unknown) factor functioning downstream of SRK in this pathway. How ARC1, this factor, and the ubiquitination of Exo70A1 signals for autophagy is not known. Once the secretory vesicles have been removed, the self-pollen grain will not receive the resources needed for hydration and germination; as a result will be rejected.
Mentions: Armadillo repeat-containing 1 was originally identified in B. napus, through a yeast two-hybrid screen for SRK kinase domain interactors, and ARC1 was found to bind to SRK through its ARM repeat domain (Gu et al., 1998). ARC1 can be phosphorylated by SRK, but is more strongly phosphorylated by MLPK in vitro (Gu et al., 1998; Samuel et al., 2008). ARC1 is composed of the three distinct protein domains described above (UND, U-box, ARM repeat domain), and has functional nuclear localization and nuclear export signals. When transiently expressed in tobacco BY2 cells, ARC1 was localized to both the cytoplasm and nucleus, shuttling back and forth between these two compartments (Stone et al., 2003). The function of ARC1’s nuclear localization is still unclear, especially as it is expected to be near the plasma membrane for its role in self-incompatibility (Figure 1, described in more detail below). When ARC1 was co-expressed with active SRK or MLPK kinase domains, it no longer shuttled to the nucleus suggesting that ARC1 phosphorylation alters its localization and may be important for its function in the self-incompatibility pathway (Stone et al., 2003; Samuel et al., 2008). B. napus ARC1 displays stigma-specific expression, and the knock-down of ARC1 expression by antisense suppression resulted in a gained self-pollen acceptance, instead of rejection, indicating a breakdown in the self-incompatible pathway (Gu et al., 1998; Stone et al., 1999). ARC1 was shown to have in vitro E3 ligase activity, and the importance of ubiquitination in self-incompatibility came from analyses of ubiquitinated proteins in the stigma. Wild-type B. napus stigmas that were pollinated with self-incompatible pollen were shown, by immunoblotting with an anti-ubiquitin antibody, to be enriched in ubiquitinated proteins (Stone et al., 2003; Samuel et al., 2011). In contrast, self-pollinated ARC1-antisense-suppressed stigmas had a lower level of ubiquitinated proteins. Therefore, these data suggest that the presence of ARC1 led to ubiquitinated stigma proteins following self-incompatible pollinations. Given that all this work was done in B. napus, an outstanding question in the field was whether ARC1’s function was conserved in other Brassicaceae species.

Bottom Line: In the Brassicaceae (mustard family), self-incompatibility drives the rejection of self-pollen by preventing pollen hydration following pollen contact with the stigmatic surface.Self-pollen is recognized by a ligand-receptor pair: the pollen S-locus cysteine rich/S-locus protein 11 (SCR/SP11) ligand and the pistil S receptor kinase (SRK).Following self-pollen contact, the SCR/SP11 ligand on the pollen surface binds to SRK on the pistil surface, and the SRK-activated signaling pathway is initiated.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell & Systems Biology, University of Toronto Toronto, ON, Canada.

ABSTRACT
Ubiquitination plays essential roles in the regulation of many processes in plants including pollen rejection in self-incompatible species. In the Brassicaceae (mustard family), self-incompatibility drives the rejection of self-pollen by preventing pollen hydration following pollen contact with the stigmatic surface. Self-pollen is recognized by a ligand-receptor pair: the pollen S-locus cysteine rich/S-locus protein 11 (SCR/SP11) ligand and the pistil S receptor kinase (SRK). Following self-pollen contact, the SCR/SP11 ligand on the pollen surface binds to SRK on the pistil surface, and the SRK-activated signaling pathway is initiated. This pathway includes the armadillo repeat containing 1 (ARC1) protein, a member of the plant U-box (PUB) family of E3 ubiquitin ligases. ARC1 is a functional E3 ligase and is required downstream of SRK for the self-incompatibility response. This mini review highlights our recent progress in establishing ARC1's conserved role in self-pollen rejection in Brassica and Arabidopsis species and discusses future research directions in this field.

No MeSH data available.


Related in: MedlinePlus