Diverged Early From CtpB and CtpC, CtpA Has Evolved to Process D1 Precursor in Oxygenic Photosynthetic Organisms
C-terminal peptidase (Ctp) cleaves the C-terminal extension of the D1 precursor (pD1) to form mature D1. Among the three homologs CtpA, CtpB, and CtpC in photosynthetic organisms only the first is capable of processing pD1 while the roles of CtpB and CtpC remain elusive. Phylogenetic analysis of Ctp...
| Main Authors: | , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2021-04-01
|
| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2021.676036/full |
| id |
doaj-dc7cc29b05214b31b9ba761971668fa5 |
|---|---|
| record_format |
Article |
| collection |
DOAJ |
| language |
English |
| format |
Article |
| sources |
DOAJ |
| author |
Weidong Chang Weidong Chang Chenggang Li Chenggang Li Zheng Cui Zheng Cui Wei Li Wei Li Haifeng Song Haifeng Song Han Chang Han Chang Weihan Fu Weihan Fu Chunyu Wang Chunyu Wang Ting Huang Ting Huang Yixin Luo Yixin Luo Yelin Shan Yelin Shan Yuhua Wang Yuhua Wang Fei Wang Fei Wang Min Xu Min Xu Aigen Fu Aigen Fu |
| spellingShingle |
Weidong Chang Weidong Chang Chenggang Li Chenggang Li Zheng Cui Zheng Cui Wei Li Wei Li Haifeng Song Haifeng Song Han Chang Han Chang Weihan Fu Weihan Fu Chunyu Wang Chunyu Wang Ting Huang Ting Huang Yixin Luo Yixin Luo Yelin Shan Yelin Shan Yuhua Wang Yuhua Wang Fei Wang Fei Wang Min Xu Min Xu Aigen Fu Aigen Fu Diverged Early From CtpB and CtpC, CtpA Has Evolved to Process D1 Precursor in Oxygenic Photosynthetic Organisms Frontiers in Plant Science CtpA CtpB CtpC C-terminal peptidase D1 maturation photosynthesis |
| author_facet |
Weidong Chang Weidong Chang Chenggang Li Chenggang Li Zheng Cui Zheng Cui Wei Li Wei Li Haifeng Song Haifeng Song Han Chang Han Chang Weihan Fu Weihan Fu Chunyu Wang Chunyu Wang Ting Huang Ting Huang Yixin Luo Yixin Luo Yelin Shan Yelin Shan Yuhua Wang Yuhua Wang Fei Wang Fei Wang Min Xu Min Xu Aigen Fu Aigen Fu |
| author_sort |
Weidong Chang |
| title |
Diverged Early From CtpB and CtpC, CtpA Has Evolved to Process D1 Precursor in Oxygenic Photosynthetic Organisms |
| title_short |
Diverged Early From CtpB and CtpC, CtpA Has Evolved to Process D1 Precursor in Oxygenic Photosynthetic Organisms |
| title_full |
Diverged Early From CtpB and CtpC, CtpA Has Evolved to Process D1 Precursor in Oxygenic Photosynthetic Organisms |
| title_fullStr |
Diverged Early From CtpB and CtpC, CtpA Has Evolved to Process D1 Precursor in Oxygenic Photosynthetic Organisms |
| title_full_unstemmed |
Diverged Early From CtpB and CtpC, CtpA Has Evolved to Process D1 Precursor in Oxygenic Photosynthetic Organisms |
| title_sort |
diverged early from ctpb and ctpc, ctpa has evolved to process d1 precursor in oxygenic photosynthetic organisms |
| publisher |
Frontiers Media S.A. |
| series |
Frontiers in Plant Science |
| issn |
1664-462X |
| publishDate |
2021-04-01 |
| description |
C-terminal peptidase (Ctp) cleaves the C-terminal extension of the D1 precursor (pD1) to form mature D1. Among the three homologs CtpA, CtpB, and CtpC in photosynthetic organisms only the first is capable of processing pD1 while the roles of CtpB and CtpC remain elusive. Phylogenetic analysis of Ctps from photosynthetic organisms revealed that CtpA has diverged early from CtpB and CtpC during evolution implying distinct roles for the Ctps. Analysis of Arabidopsis Ctp-deficient mutants revealed that pD1 processing was not affected in atctpb, atctpc, or atctpbatctpc mutants, demonstrating that AtCtpA, not AtCtpB or AtCtpC, is responsible for cleaving the pD1 C-terminal extension. Ectopic expression of CtpAs from Synechococcus elongatus, Chlamydomonas reinhardtii, and Physcomitrella patens in atctpa rescued the lethal phenotype of the mutant indicating that SeCtpA, CrCtpA, and PpCtpA could process pD1 in Arabidopsis. Enzyme activity assays showed that PpCtpA and CrCtpA could convert pD1 into mature D1 in vitro. In contrast, expressing CtpB or CtpC from Arabidopsis, C. reinhardtii, or P. patens in atctpa did not rescue its D1 maturation deficiency, and enzyme activity assays also showed that neither CtpB nor CtpC could process pD1 in vitro. Taken together, we conclude that the function of pD1 processing by CtpA is conserved in photosynthetic organisms. It is possible that among other factors CtpA developed this function to initiate the formation of the oxygenic D1/D2 type PSII complex during evolution whereas CtpB or CtpC have other roles that are still unclear. |
| topic |
CtpA CtpB CtpC C-terminal peptidase D1 maturation photosynthesis |
| url |
https://www.frontiersin.org/articles/10.3389/fpls.2021.676036/full |
| work_keys_str_mv |
AT weidongchang divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT weidongchang divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT chenggangli divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT chenggangli divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT zhengcui divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT zhengcui divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT weili divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT weili divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT haifengsong divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT haifengsong divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT hanchang divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT hanchang divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT weihanfu divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT weihanfu divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT chunyuwang divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT chunyuwang divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT tinghuang divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT tinghuang divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT yixinluo divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT yixinluo divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT yelinshan divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT yelinshan divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT yuhuawang divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT yuhuawang divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT feiwang divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT feiwang divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT minxu divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT minxu divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT aigenfu divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms AT aigenfu divergedearlyfromctpbandctpcctpahasevolvedtoprocessd1precursorinoxygenicphotosyntheticorganisms |
| _version_ |
1721497786732511232 |
| spelling |
doaj-dc7cc29b05214b31b9ba761971668fa52021-04-30T16:23:21ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-04-011210.3389/fpls.2021.676036676036Diverged Early From CtpB and CtpC, CtpA Has Evolved to Process D1 Precursor in Oxygenic Photosynthetic OrganismsWeidong Chang0Weidong Chang1Chenggang Li2Chenggang Li3Zheng Cui4Zheng Cui5Wei Li6Wei Li7Haifeng Song8Haifeng Song9Han Chang10Han Chang11Weihan Fu12Weihan Fu13Chunyu Wang14Chunyu Wang15Ting Huang16Ting Huang17Yixin Luo18Yixin Luo19Yelin Shan20Yelin Shan21Yuhua Wang22Yuhua Wang23Fei Wang24Fei Wang25Min Xu26Min Xu27Aigen Fu28Aigen Fu29Chinese Education Ministry’s Key Laboratory of Western Resources and Modern Biotechnology, Northwest University, Xi’an, ChinaKey Laboratory of Biotechnology Shaanxi Province, College of Life Sciences, Northwest University, Xi’an, ChinaChinese Education Ministry’s Key Laboratory of Western Resources and Modern Biotechnology, Northwest University, Xi’an, ChinaKey Laboratory of Biotechnology Shaanxi Province, College of Life Sciences, Northwest University, Xi’an, ChinaChinese Education Ministry’s Key Laboratory of Western Resources and Modern Biotechnology, Northwest University, Xi’an, ChinaKey Laboratory of Biotechnology Shaanxi Province, College of Life Sciences, Northwest University, Xi’an, ChinaChinese Education Ministry’s Key Laboratory of Western Resources and Modern Biotechnology, Northwest University, Xi’an, ChinaKey Laboratory of Biotechnology Shaanxi Province, College of Life Sciences, Northwest University, Xi’an, ChinaChinese Education Ministry’s Key Laboratory of Western Resources and Modern Biotechnology, Northwest University, Xi’an, ChinaKey Laboratory of Biotechnology Shaanxi Province, College of Life Sciences, Northwest University, Xi’an, ChinaChinese Education Ministry’s Key Laboratory of Western Resources and Modern Biotechnology, Northwest University, Xi’an, ChinaKey Laboratory of Biotechnology Shaanxi Province, College of Life Sciences, Northwest University, Xi’an, ChinaChinese Education Ministry’s Key Laboratory of Western Resources and Modern Biotechnology, Northwest University, Xi’an, ChinaKey Laboratory of Biotechnology Shaanxi Province, College of Life Sciences, Northwest University, Xi’an, ChinaChinese Education Ministry’s Key Laboratory of Western Resources and Modern Biotechnology, Northwest University, Xi’an, ChinaKey Laboratory of Biotechnology Shaanxi Province, College of Life Sciences, Northwest University, Xi’an, ChinaChinese Education Ministry’s Key Laboratory of Western Resources and Modern Biotechnology, Northwest University, Xi’an, ChinaKey Laboratory of Biotechnology Shaanxi Province, College of Life Sciences, Northwest University, Xi’an, ChinaChinese Education Ministry’s Key Laboratory of Western Resources and Modern Biotechnology, Northwest University, Xi’an, ChinaKey Laboratory of Biotechnology Shaanxi Province, College of Life Sciences, Northwest University, Xi’an, ChinaChinese Education Ministry’s Key Laboratory of Western Resources and Modern Biotechnology, Northwest University, Xi’an, ChinaKey Laboratory of Biotechnology Shaanxi Province, College of Life Sciences, Northwest University, Xi’an, ChinaChinese Education Ministry’s Key Laboratory of Western Resources and Modern Biotechnology, Northwest University, Xi’an, ChinaKey Laboratory of Biotechnology Shaanxi Province, College of Life Sciences, Northwest University, Xi’an, ChinaChinese Education Ministry’s Key Laboratory of Western Resources and Modern Biotechnology, Northwest University, Xi’an, ChinaKey Laboratory of Biotechnology Shaanxi Province, College of Life Sciences, Northwest University, Xi’an, ChinaChinese Education Ministry’s Key Laboratory of Western Resources and Modern Biotechnology, Northwest University, Xi’an, ChinaKey Laboratory of Biotechnology Shaanxi Province, College of Life Sciences, Northwest University, Xi’an, ChinaChinese Education Ministry’s Key Laboratory of Western Resources and Modern Biotechnology, Northwest University, Xi’an, ChinaKey Laboratory of Biotechnology Shaanxi Province, College of Life Sciences, Northwest University, Xi’an, ChinaC-terminal peptidase (Ctp) cleaves the C-terminal extension of the D1 precursor (pD1) to form mature D1. Among the three homologs CtpA, CtpB, and CtpC in photosynthetic organisms only the first is capable of processing pD1 while the roles of CtpB and CtpC remain elusive. Phylogenetic analysis of Ctps from photosynthetic organisms revealed that CtpA has diverged early from CtpB and CtpC during evolution implying distinct roles for the Ctps. Analysis of Arabidopsis Ctp-deficient mutants revealed that pD1 processing was not affected in atctpb, atctpc, or atctpbatctpc mutants, demonstrating that AtCtpA, not AtCtpB or AtCtpC, is responsible for cleaving the pD1 C-terminal extension. Ectopic expression of CtpAs from Synechococcus elongatus, Chlamydomonas reinhardtii, and Physcomitrella patens in atctpa rescued the lethal phenotype of the mutant indicating that SeCtpA, CrCtpA, and PpCtpA could process pD1 in Arabidopsis. Enzyme activity assays showed that PpCtpA and CrCtpA could convert pD1 into mature D1 in vitro. In contrast, expressing CtpB or CtpC from Arabidopsis, C. reinhardtii, or P. patens in atctpa did not rescue its D1 maturation deficiency, and enzyme activity assays also showed that neither CtpB nor CtpC could process pD1 in vitro. Taken together, we conclude that the function of pD1 processing by CtpA is conserved in photosynthetic organisms. It is possible that among other factors CtpA developed this function to initiate the formation of the oxygenic D1/D2 type PSII complex during evolution whereas CtpB or CtpC have other roles that are still unclear.https://www.frontiersin.org/articles/10.3389/fpls.2021.676036/fullCtpACtpBCtpCC-terminal peptidaseD1 maturationphotosynthesis |