Functional diversification of thylakoidal processing peptidases in Arabidopsis thaliana.

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 si...

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Main Authors: Shih-Chi Hsu, Joshua K Endow, Nicholas J Ruppel, Rebecca L Roston, Amy J Baldwin, Kentaro Inoue
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2011-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3210150?pdf=render
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author Shih-Chi Hsu
Joshua K Endow
Nicholas J Ruppel
Rebecca L Roston
Amy J Baldwin
Kentaro Inoue
author_facet Shih-Chi Hsu
Joshua K Endow
Nicholas J Ruppel
Rebecca L Roston
Amy J Baldwin
Kentaro Inoue
author_sort Shih-Chi Hsu
collection DOAJ
description 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.
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spelling doaj.art-f620a9f63e6441618ca137d2207ac1382022-12-21T18:45:58ZengPublic Library of Science (PLoS)PLoS ONE1932-62032011-01-01611e2725810.1371/journal.pone.0027258Functional diversification of thylakoidal processing peptidases in Arabidopsis thaliana.Shih-Chi HsuJoshua K EndowNicholas J RuppelRebecca L RostonAmy J BaldwinKentaro InoueThylakoidal 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.http://europepmc.org/articles/PMC3210150?pdf=render
spellingShingle Shih-Chi Hsu
Joshua K Endow
Nicholas J Ruppel
Rebecca L Roston
Amy J Baldwin
Kentaro Inoue
Functional diversification of thylakoidal processing peptidases in Arabidopsis thaliana.
PLoS ONE
title Functional diversification of thylakoidal processing peptidases in Arabidopsis thaliana.
title_full Functional diversification of thylakoidal processing peptidases in Arabidopsis thaliana.
title_fullStr Functional diversification of thylakoidal processing peptidases in Arabidopsis thaliana.
title_full_unstemmed Functional diversification of thylakoidal processing peptidases in Arabidopsis thaliana.
title_short Functional diversification of thylakoidal processing peptidases in Arabidopsis thaliana.
title_sort functional diversification of thylakoidal processing peptidases in arabidopsis thaliana
url http://europepmc.org/articles/PMC3210150?pdf=render
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