Localization of Arabidopsis Glucan Synthase-Like 5, 8, and 12 to plasmodesmata and the GSL8-dependent role of PDLP5 in regulating plasmodesmal permeability

ABSTRACT

Cell-to-cell communication via membranous channels called plasmodesmata (PD) plays critical roles during plant development and in response to biotic and abiotic stresses. Several enzymes and receptor-like proteins (RLPs), including Arabidopsis thaliana glucan synthase-likes (GSLs), also known as callose synthases (CALSs), and PD-located proteins (PDLPs), have been implicated in plasmodesmal permeability regulation and intercellular communication. Localization of PDLPs to punctate structures at the cell periphery and their receptor-like identity have raised the hypothesis that PDLPs are involved in the regulation of symplastic trafficking during plant development and in response to endogenous and exogenous signals. Indeed, it was shown that PDLP5 could limit plasmodesmal permeability through inducing an increase in callose accumulation at PD. However, mechanistically, how this is achieved remains to be elucidated. To address this key issue in understanding the regulation of PD, physical and functional interactions between PDLPs and GSLs (using the PDLP5–GSL8/CALS10 pair as a model) were investigated. Our results show that GSL8/CALS10 plays essential roles and is required for the function and plasmodesmal localization of PDLP5. Furthermore, it was demonstrated that the localization of PDLP5 to PD and its function in inducing callose deposition are GSL8-dependent. Importantly, our transgenic study shows that three key members of the GSL family, i.e., GSL5/CALS12, GSL8/CALS10, and GSL12/CALS3, localize to PD and co-localize with PDLP5, suggesting that GSL8/CALS10 might not be the only callose synthase with the determining role in PD regulation. These findings, together with our previous observation showing the direct interaction of GSL8/CALS10 with PDLP5, indicate the pivotal role of the GSL8/CALS10-PDLP5 interplay in regulating PD permeability. Future work is needed to investigate whether the PDLP5 functionality and localization are also disrupted in gsl5 and gsl12, or it is just gsl8-specific.

KEYWORDS:

• plasmodesmata
• glucan synthase-like
• callose
• symplastic trafficking
• plasmodesmal permeability

Acknowledgments

We thank the Arabidopsis Biological Resource Center for seeds of GSL8 T-DNA insertion line and Vi Nguyen for help with the Sanger DNA sequencing data acquisition and genotyping.

Author contributions

B.S. performed experiments, conducted data analysis, and wrote the article with contributions from all authors; B.S. and Y.C. designed the experiments and conceived the project; and S.E.K. provided technical assistance and complemented the writing. Y.C. serves as the author responsible for contact and ensures communication.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Accession numbers

Sequence data used in this article can be found on the Arabidopsis Information Resource (TAIR) database under the following accession numbers: GSL5/CALS12 (AT4G03550), GSL8/CALS10 (AT2G36850), GSL12/CALS3 (AT5G13000), and PDLP5 (AT1G70690).

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/15592324.2022.2164670

Additional information

Funding

This work was supported by funding from the Agriculture and Agri-Food Canada A-Base and the National Science and Engineering Research Council of Canada (RGPIN/04625-2017) to Y.C.