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Mitochondrial Malate Dehydrogenase Lowers Leaf Respiration and Alters Photorespiration and Plant Growth in Arabidopsis
Open accessAbstract
Malate dehydrogenase (MDH) catalyzes a reversible NAD+-dependent-dehydrogenase reaction involved in central metabolism and redox homeostasis between organelle compartments. To explore the role of mitochondrial MDH (mMDH) in Arabidopsis (Arabidopsis thaliana), knockout single and double mutants for the highly expressed mMDH1 and lower expressed mMDH2 isoforms were constructed and analyzed. A mmdh1mmdh2 mutant has no detectable mMDH activity but is viable, albeit small and slow growing. Quantitative proteome analysis of mitochondria shows changes in other mitochondrial NAD-linked dehydrogenases, indicating a reorganization of such enzymes in the mitochondrial matrix. The slow-growing mmdh1mmdh2 mutant has elevated leaf respiration rate in the dark and light, without loss of photosynthetic capacity, suggesting that mMDH normally uses NADH to reduce oxaloacetate to malate, which is then exported to the cytosol, rather than to drive mitochondrial respiration. Increased respiratory rate in leaves can account in part for the low net CO2 assimilation and slow growth rate of mmdh1mmdh2. Loss of mMDH also affects photorespiration, as evidenced by a lower postillumination burst, alterations in CO2 assimilation/intercellular CO2 curves at low CO2, and the light-dependent elevated concentration of photorespiratory metabolites. Complementation of mmdh1mmdh2 with an mMDH cDNA recovered mMDH activity, suppressed respiratory rate, ameliorated changes to photorespiration, and increased plant growth. A previously established inverse correlation between mMDH and ascorbate content in tomato (Solanum lycopersicum) has been consolidated in Arabidopsis and may potentially be linked to decreased galactonolactone dehydrogenase content in mitochondria in the mutant. Overall, a central yet complex role for mMDH emerges in the partitioning of carbon and energy in leaves, providing new directions for bioengineering of plant growth rate and a new insight into the molecular mechanisms linking respiration and photosynthesis in plants.
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“studies of Arabidopsis (Arabidopsis thaliana) knockout mutants of the mitochondrial isoforms of malate dehydrogenase show that they have pronounced growth defects under low-CO2 conditions that promote photorespiration (Tomaz et al., 2010; Lindén et al., 2016).”
From Leaf Energy Balance Requires Mitochondrial Respiration and Export of Chloroplast NADPH in the Light (2019) · cites this paper as Tomaz et al., 2010
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Dietz, K., Türkan, İ., & Krieger‐Liszkay, A. (2016) · PLANT PHYSIOLOGY · doi:10.1104/pp.16.00375 · Cited by 447
Rivero, R. M., Mestre, T. C., Mittler, R., Rubio, F., García‐Sánchez, F., & Martı́nez, V. (2013) · Plant Cell & Environment · doi:10.1111/pce.12199 · Cited by 413
Tolerance to Stress Combination in Tomato Plants: New Insights in the Protective Role of Melatonin
Martı́nez, V., Nieves‐Cordones, M., López-Delacalle, M., Ródenas, R., Mestre, T. C., García‐Sánchez, F., Rubio, F., Tortosa, P. A. N., Mittler, R., & Rivero, R. M. (2018) · Molecules · doi:10.3390/molecules23030535 · Cited by 357
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Plant mitochondria – past, present and future
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Metadata
- Authors
- Tomaz, T., Bagard, M., Pracharoenwattana, I., Lindén, P., Lee, C. P., Carroll, A. J., Ströher, E., Smith, S. M., Gardeström, P., & Millar, A. H.
- Affiliations
- Australian National University (AU)
- ORCID
- Venue
- Plant Physiology
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-09-27
- Volume
- 154
- Issue
- 3
- Pages
- 1143-1157
- ISSN
- 0032-0889 (ISSN-L)
- 1532-2548
- PMC
- PMC2971595
- OpenAlex
- W2039278227
- Cited by
- 264
- References
- 52
- Citations by year
- 2026: 9 · 2025: 10 · 2024: 22 · 2023: 19 · 2022: 18 · 2021: 22 · 2020: 28 · 2019: 17 · 2018: 18 · 2017: 16 · 2016: 21 · 2015: 17 · 2014: 13 · 2013: 12 · 2012: 11
- FWCI
- 4.43
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- PLANT PHYSIOLOGY (publishedVersion, cc-by)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- eCite Digital Repository (University of Tasmania) (submittedVersion)
- UWA Profiles and Research Repository (UWA) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- ANU Open Research (Australian National University) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant nutrient uptake and metabolism
- Keywords
- mitochondrial malate dehydrogenase, leaf respiration, photorespiration, carbon assimilation, vitamin C, redox homeostasis, carbon allocation, plant growth rate, Arabidopsis thaliana
- MeSH terms
- Carbon Dioxide, Genetic Complementation Test, Malate Dehydrogenase, Mutation, Photosynthesis, Mutagenesis, Insertional, Arabidopsis, Plant Leaves, Cell Respiration, Mitochondrial Proteins, Arabidopsis Proteins, Gene Knockout Techniques
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