Arabidopsis paralogous genes RPL23aA and RPL23aB encode functionally equivalent proteins

Abstract Background In plants, each ribosomal protein (RP) is encoded by a small gene family but it is largely unknown whether the family members are functionally diversified. There are two RPL23a paralogous genes (RPL23aA and RPL23aB) encoding cytoplasmic ribosomal proteins in Arabidopsis thaliana....

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Main Authors: Wei Xiong, Xiangze Chen, Chengxin Zhu, Jiancong Zhang, Ting Lan, Lin Liu, Beixin Mo, Xuemei Chen
Format: Article
Language:English
Published: BMC 2020-10-01
Series:BMC Plant Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12870-020-02672-1
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author Wei Xiong
Xiangze Chen
Chengxin Zhu
Jiancong Zhang
Ting Lan
Lin Liu
Beixin Mo
Xuemei Chen
author_facet Wei Xiong
Xiangze Chen
Chengxin Zhu
Jiancong Zhang
Ting Lan
Lin Liu
Beixin Mo
Xuemei Chen
author_sort Wei Xiong
collection DOAJ
description Abstract Background In plants, each ribosomal protein (RP) is encoded by a small gene family but it is largely unknown whether the family members are functionally diversified. There are two RPL23a paralogous genes (RPL23aA and RPL23aB) encoding cytoplasmic ribosomal proteins in Arabidopsis thaliana. Knock-down of RPL23aA using RNAi impeded growth and led to morphological abnormalities, whereas knock-out of RPL23aB had no observable phenotype, thus these two RPL23a paralogous proteins have been used as examples of ribosomal protein paralogues with functional divergence in many published papers. Results In this study, we characterized T-DNA insertion mutants of RPL23aA and RPL23aB. A rare non-allelic non-complementation phenomenon was found in the F1 progeny of the rpl23aa X rpl23ab cross, which revealed a dosage effect of these two genes. Both RPL23aA and RPL23aB were found to be expressed almost in all examined tissues as revealed by GUS reporter analysis. Expression of RPL23aB driven by the RPL23aA promoter can rescue the phenotype of rpl23aa, indicating these two proteins are actually equivalent in function. Interestingly, based on the publicly available RNA-seq data, we found that these two RPL23a paralogues were expressed in a concerted manner and the expression level of RPL23aA was much higher than that of RPL23aB at different developmental stages and in different tissues. Conclusions Our findings suggest that the two RPL23a paralogous proteins are functionally equivalent but the two genes are not. RPL23aA plays a predominant role due to its higher expression levels. RPL23aB plays a lesser role due to its lower expression. The presence of paralogous genes for the RPL23a protein in plants might be necessary to maintain its adequate dosage.
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spelling doaj.art-e8b44fbc835042988720a8652d6a59d02022-12-21T18:10:06ZengBMCBMC Plant Biology1471-22292020-10-0120111110.1186/s12870-020-02672-1Arabidopsis paralogous genes RPL23aA and RPL23aB encode functionally equivalent proteinsWei Xiong0Xiangze Chen1Chengxin Zhu2Jiancong Zhang3Ting Lan4Lin Liu5Beixin Mo6Xuemei Chen7Guangdong Provincial Key Laboratory for Plant Epigenetics, Longhua Bioindustry and Innovation Research Institute, College of Life Sciences and Oceanography, Shenzhen UniversityGuangdong Provincial Key Laboratory for Plant Epigenetics, Longhua Bioindustry and Innovation Research Institute, College of Life Sciences and Oceanography, Shenzhen UniversityGuangdong Provincial Key Laboratory for Plant Epigenetics, Longhua Bioindustry and Innovation Research Institute, College of Life Sciences and Oceanography, Shenzhen UniversityGuangdong Provincial Key Laboratory for Plant Epigenetics, Longhua Bioindustry and Innovation Research Institute, College of Life Sciences and Oceanography, Shenzhen UniversityGuangdong Provincial Key Laboratory for Plant Epigenetics, Longhua Bioindustry and Innovation Research Institute, College of Life Sciences and Oceanography, Shenzhen UniversityGuangdong Provincial Key Laboratory for Plant Epigenetics, Longhua Bioindustry and Innovation Research Institute, College of Life Sciences and Oceanography, Shenzhen UniversityGuangdong Provincial Key Laboratory for Plant Epigenetics, Longhua Bioindustry and Innovation Research Institute, College of Life Sciences and Oceanography, Shenzhen UniversityDepartment of Botany and Plant Sciences, Institute of Integrative Genome Biology, University of CaliforniaAbstract Background In plants, each ribosomal protein (RP) is encoded by a small gene family but it is largely unknown whether the family members are functionally diversified. There are two RPL23a paralogous genes (RPL23aA and RPL23aB) encoding cytoplasmic ribosomal proteins in Arabidopsis thaliana. Knock-down of RPL23aA using RNAi impeded growth and led to morphological abnormalities, whereas knock-out of RPL23aB had no observable phenotype, thus these two RPL23a paralogous proteins have been used as examples of ribosomal protein paralogues with functional divergence in many published papers. Results In this study, we characterized T-DNA insertion mutants of RPL23aA and RPL23aB. A rare non-allelic non-complementation phenomenon was found in the F1 progeny of the rpl23aa X rpl23ab cross, which revealed a dosage effect of these two genes. Both RPL23aA and RPL23aB were found to be expressed almost in all examined tissues as revealed by GUS reporter analysis. Expression of RPL23aB driven by the RPL23aA promoter can rescue the phenotype of rpl23aa, indicating these two proteins are actually equivalent in function. Interestingly, based on the publicly available RNA-seq data, we found that these two RPL23a paralogues were expressed in a concerted manner and the expression level of RPL23aA was much higher than that of RPL23aB at different developmental stages and in different tissues. Conclusions Our findings suggest that the two RPL23a paralogous proteins are functionally equivalent but the two genes are not. RPL23aA plays a predominant role due to its higher expression levels. RPL23aB plays a lesser role due to its lower expression. The presence of paralogous genes for the RPL23a protein in plants might be necessary to maintain its adequate dosage.http://link.springer.com/article/10.1186/s12870-020-02672-1RibosomeRibosomal proteinRPL23aGene dosageParalogueFunctional specialization
spellingShingle Wei Xiong
Xiangze Chen
Chengxin Zhu
Jiancong Zhang
Ting Lan
Lin Liu
Beixin Mo
Xuemei Chen
Arabidopsis paralogous genes RPL23aA and RPL23aB encode functionally equivalent proteins
BMC Plant Biology
Ribosome
Ribosomal protein
RPL23a
Gene dosage
Paralogue
Functional specialization
title Arabidopsis paralogous genes RPL23aA and RPL23aB encode functionally equivalent proteins
title_full Arabidopsis paralogous genes RPL23aA and RPL23aB encode functionally equivalent proteins
title_fullStr Arabidopsis paralogous genes RPL23aA and RPL23aB encode functionally equivalent proteins
title_full_unstemmed Arabidopsis paralogous genes RPL23aA and RPL23aB encode functionally equivalent proteins
title_short Arabidopsis paralogous genes RPL23aA and RPL23aB encode functionally equivalent proteins
title_sort arabidopsis paralogous genes rpl23aa and rpl23ab encode functionally equivalent proteins
topic Ribosome
Ribosomal protein
RPL23a
Gene dosage
Paralogue
Functional specialization
url http://link.springer.com/article/10.1186/s12870-020-02672-1
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