Functional Diversification of Thylakoidal Processing Peptidases in Arabidopsis thaliana

Authors

Shih-Chi Hsu, Boyce Thompson Institute for Plant Research
Joshua K. Endow, Oberlin College
Nicholas J. Ruppel, Oberlin College
Rebecca Roston, University of Nebraska- LincolnFollow
Amy J. Baldwin, Cardiff University
Kentaro Inoue, University of California Davis

Date of this Version

2011

Citation

Hsu S-C, Endow JK, Ruppel NJ, Roston RL, Baldwin AJ, et al. (2011) Functional Diversification of Thylakoidal Processing Peptidases in Arabidopsis thaliana. PLoS ONE 6(11): e27258.

Comments

Copyright 2011 Hsu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License

Abstract

Thylakoidal processing peptidase (TPP) is responsible for removing amino-terminal thylakoid-transfer signals from several proteins in the thylakoid lumen. Three TPP isoforms are encoded by the nuclear genome of Arabidopsis thaliana. Previous studies showed that one of them termed plastidic type I signal peptidase 1 (Plsp1) was necessary for processing three thylakoidal proteins and one protein in the chloroplast envelope in vivo. The lack of Plsp1 resulted in seedling lethality, apparently due to disruption of proper thylakoid development. The physiological roles of the other two TPP homologs remain unknown. Here we show that the three A. thaliana TPP isoforms evolved to acquire diverse functions. Phylogenetic analysis revealed that TPP may have originated before the endosymbiotic event, and that there are two groups of TPP in seed plants: one includes Plsp1 and another comprises the other two A. thaliana TPP homologs, which are named as Plsp2A and Plsp2B in this study. The duplication leading to the two groups predates the gymnosperm-angiosperm divergence, and the separation of Plsp2A and Plsp2B occurred after the Malvaceae-Brassicaceae diversification. Quantitative reverse transcription-PCR assay revealed that the two PLSP2 genes were co-expressed in both photosynthetic tissues and roots, whereas the PLSP1 transcript accumulated predominantly in photosynthetic tissues. Both PLSP2 genes were expressed in the aerial parts of the plsp1-null mutant at levels comparable to those in wild-type plants. The seedling-lethal phenotype of the plsp1-null mutant could be rescued by a constitutive expression of Plsp1 cDNA but not by that of Plsp2A or Plsp2B. These results indicate that Plsp1 and Plsp2 evolved to function differently, and that neither of the Plsp2 isoforms is necessary for proper thylakoid development in photosynthetic tissues.