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The juxtamembrane and carboxy-terminal domains of Arabidopsis PRK2 are critical for ROP-induced growth in pollen tubes.

ABSTRACT: Polarized growth of pollen tubes is a critical step for successful reproduction in angiosperms and is controlled by ROP GTPases. Spatiotemporal activation of ROP (Rho GTPases of plants) necessitates a complex and sophisticated regulatory system, in which guanine nucleotide exchange factors (RopGEFs) are key components. It was previously shown that a leucine-rich repeat receptor-like kinase, Arabidopsis pollen receptor kinase 2 (AtPRK2), interacted with RopGEF12 for its membrane recruitment. However, the mechanisms underlying AtPRK2-mediated ROP activation in vivo are yet to be defined. It is reported here that over-expression of AtPRK2 induced tube bulging that was accompanied by the ectopic localization of ROP-GTP and the ectopic distribution of actin microfilaments. Tube depolarization was also induced by a potentially kinase-dead mutant, AtPRK2K366R, suggesting that the over-expression effect of AtPRK2 did not require its kinase activity. By contrast, deletions of non-catalytic domains in AtPRK2, i.e. the juxtamembrane (JM) and carboxy-terminal (CT) domains, abolished its ability to affect tube polarization. Notably, AtPRK2K366R retained the ability to interact with RopGEF12, whereas AtPRK2 truncations of these non-catalytic domains did not. Lastly, it has been shown that the JM and CT domains of AtPRK2 were not only critical for its interaction with RopGEF12 but also critical for its distribution at the plasma membrane. These results thus provide further insight into pollen receptor kinase-mediated ROP activation during pollen tube growth.

SUBMITTER: Zhao XY

PROVIDER: S-EPMC3871813 | biostudies-other | 2013 Dec

REPOSITORIES: biostudies-other

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The juxtamembrane and carboxy-terminal domains of Arabidopsis PRK2 are critical for ROP-induced growth in pollen tubes.

Zhao Xin-Ying XY Wang Qun Q Li Sha S Ge Fu-Rong FR Zhou Liang-Zi LZ McCormick Sheila S Zhang Yan Y

Journal of experimental botany 20131017 18

Polarized growth of pollen tubes is a critical step for successful reproduction in angiosperms and is controlled by ROP GTPases. Spatiotemporal activation of ROP (Rho GTPases of plants) necessitates a complex and sophisticated regulatory system, in which guanine nucleotide exchange factors (RopGEFs) are key components. It was previously shown that a leucine-rich repeat receptor-like kinase, Arabidopsis pollen receptor kinase 2 (AtPRK2), interacted with RopGEF12 for its membrane recruitment. Howe ...[more]

PMID: 24136420

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Project description:BACKGROUND:Glycosylphosphatidylinositol (GPI) addition is one of the several post-translational modifications to proteins that increase their affinity for membranes. In eukaryotes, the GPI transamidase complex (GPI-T) catalyzes the attachment of pre-assembled GPI anchors to GPI-anchored proteins (GAPs) through a transamidation reaction. A mutation in AtGPI8 (gpi8-2), the putative catalytic subunit of GPI-T in Arabidopsis, is transmitted normally through the female gametophyte (FG), indicating the FG tolerates loss of GPI transamidation. In contrast, gpi8-2 almost completely abolishes male gametophyte (MG) function. Still, the unexpected finding that gpi8-2 FGs function normally requires further investigation. Additionally, specific developmental defects in the MG caused by loss of GPI transamidation remain poorly characterized. RESULTS:Here we investigated the effect of loss of AtPIG-S, another GPI-T subunit, in both gametophytes. Like gpi8-2, we showed that a mutation in AtPIG-S (pigs-1) disrupted synergid localization of LORELEI (LRE), a putative GAP critical for pollen tube reception by the FG. Still, pigs-1 is transmitted normally through the FG. Conversely, pigs-1 severely impaired male gametophyte (MG) function during pollen tube emergence and growth in the pistil. A pPIGS:GFP-PIGS transgene complemented these MG defects and enabled generation of pigs-1/pigs-1 seedlings. However, the pPIGS:GFP-PIGS transgene seemingly failed to rescue the function of AtPIG-S in the sporophyte, as pigs-1/pigs-1, pPIGS:GFP-PIGS seedlings died soon after germination. CONCLUSIONS:Characterization of pigs-1 provided further evidence that the FG tolerates loss of GPI transamidation more than the MG and that the MG compared to the FG may be a better haploid system to study the role of GPI-anchoring. Pigs-1 pollen develops normally and thus represent a tool in which GPI anchor biosynthesis and transamidation of GAPs have been uncoupled, offering a potential way to study free GPI in plant development. While previously reported male fertility defects of GPI biosynthesis mutants could have been due either to loss of GPI or GAPs lacking the GPI anchor, our results clarified that the loss of mature GAPs underlie male fertility defects of GPI-deficient pollen grains, as pigs-1 is defective only in the downstream transamidation step.

Dataset Information

The juxtamembrane and carboxy-terminal domains of Arabidopsis PRK2 are critical for ROP-induced growth in pollen tubes.

Publications

The juxtamembrane and carboxy-terminal domains of Arabidopsis PRK2 are critical for ROP-induced growth in pollen tubes.

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