Late Embryogenesis Abundant (LEA)5 Regulates Translation in Mitochondria and Chloroplasts to Enhance Growth and Stress Tolerance
The late embryogenesis abundant (LEA)5 protein is predominantly expressed in Arabidopsis leaves in the dark, the levels of LEA5 transcripts decreasing rapidly upon illumination. LEA5 is important in plant responses to environmental stresses but the mechanisms involved have not been elucidated. We th...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-06-01
|
| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2022.875799/full |
| _version_ | 1811338036169932800 |
|---|---|
| author | Barbara Karpinska Nurhayati Razak Daniel S. Shaw William Plumb Eveline Van De Slijke Eveline Van De Slijke Jennifer Stephens Geert De Jaeger Geert De Jaeger Monika W. Murcha Christine H. Foyer |
| author_facet | Barbara Karpinska Nurhayati Razak Daniel S. Shaw William Plumb Eveline Van De Slijke Eveline Van De Slijke Jennifer Stephens Geert De Jaeger Geert De Jaeger Monika W. Murcha Christine H. Foyer |
| author_sort | Barbara Karpinska |
| collection | DOAJ |
| description | The late embryogenesis abundant (LEA)5 protein is predominantly expressed in Arabidopsis leaves in the dark, the levels of LEA5 transcripts decreasing rapidly upon illumination. LEA5 is important in plant responses to environmental stresses but the mechanisms involved have not been elucidated. We therefore explored LEA5 functions in Arabidopsis mutants (lea5) and transgenic Arabidopsis plants constitutively expressing LEA5 (OEX 2-5), as well as in transgenic barley lines expressing the Arabidopsis LEA5 gene. The OEX 2-5 plants grew better than controls and lea5 mutants in the presence of the prooxidants methyl viologen and menadione. Confocal microscopy of Arabidopsis mesophyll protoplasts expressing a LEA5-YFP fusion protein demonstrated that LEA5 could be localized to chloroplasts as well as mitochondria in Arabidopsis protoplasts. Tandem affinity purification (TAP) analysis revealed LEA5 interacts with the chloroplast DEAD-box ATP-dependent RNA helicase 22 (RH22) in Arabidopsis cells. Split YFP analysis confirmed the interaction between RH22 and LEA5 in chloroplasts. The abundance of translated protein products in chloroplasts was decreased in transgenic Arabidopsis plants and increased in lea5 knockout mutants. Conversely, the abundance of translated mitochondrial protein products was increased in OEX 2-5 plants and decreased in lea5 mutants. Mitochondrial electron transport rates were higher in the OEX 2-5 plants than the wild type. The transformed barley lines expressing the Arabidopsis LEA5 had increased seed yields, but they showed a greater drought-induced inhibition of photosynthesis than controls. Taken together, these data demonstrate that LEA5 regulates organellar translation, in order to enhance respiration relative to photosynthesis in response to stress. |
| first_indexed | 2024-04-13T18:05:00Z |
| format | Article |
| id | doaj.art-d7b7331a276a43b08f67fbad1e6bedbc |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-04-13T18:05:00Z |
| publishDate | 2022-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-d7b7331a276a43b08f67fbad1e6bedbc2022-12-22T02:36:06ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-06-011310.3389/fpls.2022.875799875799Late Embryogenesis Abundant (LEA)5 Regulates Translation in Mitochondria and Chloroplasts to Enhance Growth and Stress ToleranceBarbara Karpinska0Nurhayati Razak1Daniel S. Shaw2William Plumb3Eveline Van De Slijke4Eveline Van De Slijke5Jennifer Stephens6Geert De Jaeger7Geert De Jaeger8Monika W. Murcha9Christine H. Foyer10School of Biosciences, College of Life and Environmental Sciences, University of Birmingham, Birmingham, United KingdomSchool of Biosciences, College of Life and Environmental Sciences, University of Birmingham, Birmingham, United KingdomCentre for Plant Sciences, School of Biology, Faculty of Biological Sciences, University of Leeds, Leeds, United KingdomSchool of Biosciences, College of Life and Environmental Sciences, University of Birmingham, Birmingham, United KingdomDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, BelgiumVIB Center for Plant Systems Biology, Ghent, BelgiumCell and Molecular Sciences, The James Hutton Institute, Dundee, United KingdomDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, BelgiumVIB Center for Plant Systems Biology, Ghent, BelgiumSchool of Molecular Sciences, Perth, WA, AustraliaSchool of Biosciences, College of Life and Environmental Sciences, University of Birmingham, Birmingham, United KingdomThe late embryogenesis abundant (LEA)5 protein is predominantly expressed in Arabidopsis leaves in the dark, the levels of LEA5 transcripts decreasing rapidly upon illumination. LEA5 is important in plant responses to environmental stresses but the mechanisms involved have not been elucidated. We therefore explored LEA5 functions in Arabidopsis mutants (lea5) and transgenic Arabidopsis plants constitutively expressing LEA5 (OEX 2-5), as well as in transgenic barley lines expressing the Arabidopsis LEA5 gene. The OEX 2-5 plants grew better than controls and lea5 mutants in the presence of the prooxidants methyl viologen and menadione. Confocal microscopy of Arabidopsis mesophyll protoplasts expressing a LEA5-YFP fusion protein demonstrated that LEA5 could be localized to chloroplasts as well as mitochondria in Arabidopsis protoplasts. Tandem affinity purification (TAP) analysis revealed LEA5 interacts with the chloroplast DEAD-box ATP-dependent RNA helicase 22 (RH22) in Arabidopsis cells. Split YFP analysis confirmed the interaction between RH22 and LEA5 in chloroplasts. The abundance of translated protein products in chloroplasts was decreased in transgenic Arabidopsis plants and increased in lea5 knockout mutants. Conversely, the abundance of translated mitochondrial protein products was increased in OEX 2-5 plants and decreased in lea5 mutants. Mitochondrial electron transport rates were higher in the OEX 2-5 plants than the wild type. The transformed barley lines expressing the Arabidopsis LEA5 had increased seed yields, but they showed a greater drought-induced inhibition of photosynthesis than controls. Taken together, these data demonstrate that LEA5 regulates organellar translation, in order to enhance respiration relative to photosynthesis in response to stress.https://www.frontiersin.org/articles/10.3389/fpls.2022.875799/fullrespirationmitochondriachloroplaststranslationsignaling |
| spellingShingle | Barbara Karpinska Nurhayati Razak Daniel S. Shaw William Plumb Eveline Van De Slijke Eveline Van De Slijke Jennifer Stephens Geert De Jaeger Geert De Jaeger Monika W. Murcha Christine H. Foyer Late Embryogenesis Abundant (LEA)5 Regulates Translation in Mitochondria and Chloroplasts to Enhance Growth and Stress Tolerance Frontiers in Plant Science respiration mitochondria chloroplasts translation signaling |
| title | Late Embryogenesis Abundant (LEA)5 Regulates Translation in Mitochondria and Chloroplasts to Enhance Growth and Stress Tolerance |
| title_full | Late Embryogenesis Abundant (LEA)5 Regulates Translation in Mitochondria and Chloroplasts to Enhance Growth and Stress Tolerance |
| title_fullStr | Late Embryogenesis Abundant (LEA)5 Regulates Translation in Mitochondria and Chloroplasts to Enhance Growth and Stress Tolerance |
| title_full_unstemmed | Late Embryogenesis Abundant (LEA)5 Regulates Translation in Mitochondria and Chloroplasts to Enhance Growth and Stress Tolerance |
| title_short | Late Embryogenesis Abundant (LEA)5 Regulates Translation in Mitochondria and Chloroplasts to Enhance Growth and Stress Tolerance |
| title_sort | late embryogenesis abundant lea 5 regulates translation in mitochondria and chloroplasts to enhance growth and stress tolerance |
| topic | respiration mitochondria chloroplasts translation signaling |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2022.875799/full |
| work_keys_str_mv | AT barbarakarpinska lateembryogenesisabundantlea5regulatestranslationinmitochondriaandchloroplaststoenhancegrowthandstresstolerance AT nurhayatirazak lateembryogenesisabundantlea5regulatestranslationinmitochondriaandchloroplaststoenhancegrowthandstresstolerance AT danielsshaw lateembryogenesisabundantlea5regulatestranslationinmitochondriaandchloroplaststoenhancegrowthandstresstolerance AT williamplumb lateembryogenesisabundantlea5regulatestranslationinmitochondriaandchloroplaststoenhancegrowthandstresstolerance AT evelinevandeslijke lateembryogenesisabundantlea5regulatestranslationinmitochondriaandchloroplaststoenhancegrowthandstresstolerance AT evelinevandeslijke lateembryogenesisabundantlea5regulatestranslationinmitochondriaandchloroplaststoenhancegrowthandstresstolerance AT jenniferstephens lateembryogenesisabundantlea5regulatestranslationinmitochondriaandchloroplaststoenhancegrowthandstresstolerance AT geertdejaeger lateembryogenesisabundantlea5regulatestranslationinmitochondriaandchloroplaststoenhancegrowthandstresstolerance AT geertdejaeger lateembryogenesisabundantlea5regulatestranslationinmitochondriaandchloroplaststoenhancegrowthandstresstolerance AT monikawmurcha lateembryogenesisabundantlea5regulatestranslationinmitochondriaandchloroplaststoenhancegrowthandstresstolerance AT christinehfoyer lateembryogenesisabundantlea5regulatestranslationinmitochondriaandchloroplaststoenhancegrowthandstresstolerance |