Changing turn-over rates regulate abundance of tryptophan, GS biosynthesis, IAA transport and photosynthesis proteins in Arabidopsis growth defense transitions
Abstract Background Shifts in dynamic equilibria of the abundance of cellular molecules in plant-pathogen interactions need further exploration. We induced PTI in optimally growing Arabidopsis thaliana seedlings for 16 h, returning them to growth conditions for another 16 h. Methods Turn-over and ab...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-11-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-023-01739-3 |
| _version_ | 1797629979567063040 |
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| author | Mohammad Abukhalaf Carsten Proksch Domenika Thieme Jörg Ziegler Wolfgang Hoehenwarter |
| author_facet | Mohammad Abukhalaf Carsten Proksch Domenika Thieme Jörg Ziegler Wolfgang Hoehenwarter |
| author_sort | Mohammad Abukhalaf |
| collection | DOAJ |
| description | Abstract Background Shifts in dynamic equilibria of the abundance of cellular molecules in plant-pathogen interactions need further exploration. We induced PTI in optimally growing Arabidopsis thaliana seedlings for 16 h, returning them to growth conditions for another 16 h. Methods Turn-over and abundance of 99 flg22 responding proteins were measured chronologically using a stable heavy nitrogen isotope partial labeling strategy and targeted liquid chromatography coupled to mass spectrometry (PRM LC–MS). These experiments were complemented by measurements of mRNA and phytohormone levels. Results Changes in synthesis and degradation rate constants (K s and K d) regulated tryptophane and glucosinolate, IAA transport, and photosynthesis-associated protein (PAP) homeostasis in growth/PTI transitions independently of mRNA levels. K s values increased after elicitation while protein and mRNA levels became uncorrelated. mRNA returned to pre-elicitation levels, yet protein abundance remained at PTI levels even 16 h after media exchange, indicating protein levels were robust and unresponsive to transition back to growth. The abundance of 23 PAPs including FERREDOXIN-NADP( +)-OXIDOREDUCTASE (FNR1) decreased 16 h after PAMP exposure, their depletion was nearly abolished in the myc234 mutant. FNR1 K d increased as mRNA levels decreased early in PTI, its K s decreased in prolonged PTI. FNR1 K d was lower in myc234, mRNA levels decreased as in wild type. Conclusions Protein K d and K s values change in response to flg22 exposure and constitute an additional layer of protein abundance regulation in growth defense transitions next to changes in mRNA levels. Our results suggest photosystem remodeling in PTI to direct electron flow away from the photosynthetic carbon reaction towards ROS production as an active defense mechanism controlled post-transcriptionally and by MYC2 and homologs. Target proteins accumulated later and PAP and auxin/IAA depletion was repressed in myc234 indicating a positive effect of the transcription factors in the establishment of PTI. |
| first_indexed | 2024-03-11T11:01:30Z |
| format | Article |
| id | doaj.art-c0cd0a0b8a54427b823d89029f9b2caf |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-03-11T11:01:30Z |
| publishDate | 2023-11-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-c0cd0a0b8a54427b823d89029f9b2caf2023-11-12T12:30:18ZengBMCBMC Biology1741-70072023-11-0121111810.1186/s12915-023-01739-3Changing turn-over rates regulate abundance of tryptophan, GS biosynthesis, IAA transport and photosynthesis proteins in Arabidopsis growth defense transitionsMohammad Abukhalaf0Carsten Proksch1Domenika Thieme2Jörg Ziegler3Wolfgang Hoehenwarter4Present address: Institute for Experimental Medicine, Christian-Albrechts University KielDepartment Biochemistry of Plant Interactions, Leibniz Institute of Plant BiochemistryDepartment Biochemistry of Plant Interactions, Leibniz Institute of Plant BiochemistryDepartment Molecular Signal Processing, Leibniz Institute of Plant BiochemistryDepartment Biochemistry of Plant Interactions, Leibniz Institute of Plant BiochemistryAbstract Background Shifts in dynamic equilibria of the abundance of cellular molecules in plant-pathogen interactions need further exploration. We induced PTI in optimally growing Arabidopsis thaliana seedlings for 16 h, returning them to growth conditions for another 16 h. Methods Turn-over and abundance of 99 flg22 responding proteins were measured chronologically using a stable heavy nitrogen isotope partial labeling strategy and targeted liquid chromatography coupled to mass spectrometry (PRM LC–MS). These experiments were complemented by measurements of mRNA and phytohormone levels. Results Changes in synthesis and degradation rate constants (K s and K d) regulated tryptophane and glucosinolate, IAA transport, and photosynthesis-associated protein (PAP) homeostasis in growth/PTI transitions independently of mRNA levels. K s values increased after elicitation while protein and mRNA levels became uncorrelated. mRNA returned to pre-elicitation levels, yet protein abundance remained at PTI levels even 16 h after media exchange, indicating protein levels were robust and unresponsive to transition back to growth. The abundance of 23 PAPs including FERREDOXIN-NADP( +)-OXIDOREDUCTASE (FNR1) decreased 16 h after PAMP exposure, their depletion was nearly abolished in the myc234 mutant. FNR1 K d increased as mRNA levels decreased early in PTI, its K s decreased in prolonged PTI. FNR1 K d was lower in myc234, mRNA levels decreased as in wild type. Conclusions Protein K d and K s values change in response to flg22 exposure and constitute an additional layer of protein abundance regulation in growth defense transitions next to changes in mRNA levels. Our results suggest photosystem remodeling in PTI to direct electron flow away from the photosynthetic carbon reaction towards ROS production as an active defense mechanism controlled post-transcriptionally and by MYC2 and homologs. Target proteins accumulated later and PAP and auxin/IAA depletion was repressed in myc234 indicating a positive effect of the transcription factors in the establishment of PTI.https://doi.org/10.1186/s12915-023-01739-3Protein synthesis ratesProtein degradation ratesPost-transcriptional regulationPTIAuxinPin proteins |
| spellingShingle | Mohammad Abukhalaf Carsten Proksch Domenika Thieme Jörg Ziegler Wolfgang Hoehenwarter Changing turn-over rates regulate abundance of tryptophan, GS biosynthesis, IAA transport and photosynthesis proteins in Arabidopsis growth defense transitions BMC Biology Protein synthesis rates Protein degradation rates Post-transcriptional regulation PTI Auxin Pin proteins |
| title | Changing turn-over rates regulate abundance of tryptophan, GS biosynthesis, IAA transport and photosynthesis proteins in Arabidopsis growth defense transitions |
| title_full | Changing turn-over rates regulate abundance of tryptophan, GS biosynthesis, IAA transport and photosynthesis proteins in Arabidopsis growth defense transitions |
| title_fullStr | Changing turn-over rates regulate abundance of tryptophan, GS biosynthesis, IAA transport and photosynthesis proteins in Arabidopsis growth defense transitions |
| title_full_unstemmed | Changing turn-over rates regulate abundance of tryptophan, GS biosynthesis, IAA transport and photosynthesis proteins in Arabidopsis growth defense transitions |
| title_short | Changing turn-over rates regulate abundance of tryptophan, GS biosynthesis, IAA transport and photosynthesis proteins in Arabidopsis growth defense transitions |
| title_sort | changing turn over rates regulate abundance of tryptophan gs biosynthesis iaa transport and photosynthesis proteins in arabidopsis growth defense transitions |
| topic | Protein synthesis rates Protein degradation rates Post-transcriptional regulation PTI Auxin Pin proteins |
| url | https://doi.org/10.1186/s12915-023-01739-3 |
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