PROHIBITIN3 Forms Complexes with ISOCHORISMATE SYNTHASE1 to Regulate Stress-Induced Salicylic Acid Biosynthesis in Arabidopsis

Seguel, Aldo; Jeleńska, Joanna; Herrera-Vásquez, Ariel; Marr, Sharon K.; Joyce, Michael B; Gagesch, Kelsey R; Shakoor, Nadia; Jiang, Shang-Chuan; Fonseca, Alejandro; Wildermuth, Mary C.; Greenberg, Jean T.; Holuigue, Loreto

doi:10.1104/pp.17.00941

Cited by 56 publications

(49 citation statements)

References 105 publications

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“…Among the membrane-located non-OXPHOS proteins only AOX1A exhibited strong accumulation in ftsh4 seeds, while VDAC1, VDAC3, and PHB3 showed no significant differences in abundance. Dual localization in the cell was reported for VDAC3 (Robert et al, 2012 ) and also recently for PHB3 (Seguel et al, 2018 ). Taking into account the fact that our MRM assay was conducted with the total seed protein extract, it is not possible to interpret the above-mentioned results in the aspect of the inner membrane biogenesis.…”

Section: Discussionsupporting

confidence: 64%

Targeted Proteomics Approach Toward Understanding the Role of the Mitochondrial Protease FTSH4 in the Biogenesis of OXPHOS During Arabidopsis Seed Germination

et al. 2018

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Seed germination provides an excellent model to study the process of mitochondrial biogenesis. It is a complex and strictly regulated process which requires a proper biogenesis of fully active organelles from existing promitochondrial structures. We have previously reported that the lack of the inner mitochondrial membrane protease FTSH4 delayed Arabidopsis seed germination. Here, we implemented a targeted mass spectrometry-based approach, Multiple Reaction Monitoring (MRM), with stable-isotope-labeled standard peptides for increased sensitivity, to quantify mitochondrial proteins in dry and germinating wild-type and ftsh4 mutant seeds, lacking the FTSH4 protease. Using total seed protein extracts we measured the abundance of the peptide targets belonging to the OXPHOS complexes, AOX1A, transport, and inner membrane scaffold as well as mitochondrial proteins that are highly specific to dry and germinating seeds. The MRM assay showed that the abundance of these proteins in ftsh4 did not differ substantially from that observed in wild-type at the level of dry seed and after stratification, but we observed a reduction in protein abundance in most of the examined OXPHOS subunits in the later stages of germination. These changes in OXPHOS protein levels in ftsh4 mutants were accompanied by a lower cytochrome pathway activity as well as an increased AOX1A amount at the transcript and protein level and alternative pathway activity. The analyses of the steady-state transcript levels of mitochondrial and nuclear genes encoding OXPHOS subunits did not show significant difference in their amount, indicating that the observed changes in the OXPHOS occurred at the post-transcriptional level. At the time when ftsh4 seeds were fully germinated, the abundance of the OXPHOS proteins in the mutant was either slightly lowered or comparable to these amounts in wild-type seeds at the similar developmental stage. By the implementation of an integrative approach combining targeted proteomics, quantitative transcriptomics, and physiological studies we have shown that the FTSH4 protease has an important role in the biogenesis of OXPHOS and thus biogenesis of mitochondria during germination of Arabidopsis seeds.

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Section: Discussionsupporting

confidence: 64%

Targeted Proteomics Approach Toward Understanding the Role of the Mitochondrial Protease FTSH4 in the Biogenesis of OXPHOS During Arabidopsis Seed Germination

et al. 2018

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“…Previous studies have shown that prohibitins regulate salicylic acid biosynthesis [30]. We suspected that NAL8 functions as a prohibitin complex subunit and is also involved in hormone signaling regulation networks.…”

Section: Resultsmentioning

confidence: 93%

“…In Arabidopsis , PHB3 is a nucleo-mitochondrial dual-localized protein that maintains genome integrity and cell proliferation in the root meristem through MINICHROMOSOME MAINTENANCE 2 ( MCM2 ) [31]. Another recent study also showed that PHB3 is localized in the chloroplasts [30]. Considering that PHB3 forms complex with other PHBs, we inferred that NAL8 is localized in mitochondria and chloroplasts.…”

Section: Resultsmentioning

confidence: 99%

“…In Arabidopsis , there are seven conserved PHB genes [27] that are associated with meristem development. The Arabidopsis PHB3 gene displays multiple functions in ethylene-induced gene expression [28], nitric oxide (NO) accumulation and response [29], salicylic acid (SA) biosynthesis induction [30], quiescent center cell (QC) and distal stem cell (DSC) identity [31], and root meristem cell proliferation [32, 33]. Furthermore, OsPHB1 was shown to be involved in cell death and senescence through the formation dimers in the defense reaction and programmed cell death (PCD) in rice [34].…”

Section: Introductionmentioning

confidence: 99%

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NAL8 encodes a prohibitin that contributes to leaf and spikelet development by regulating mitochondria and chloroplasts stability in rice

Chen

Guo²,

Li³

et al. 2019

BMC Plant Biol

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Background Leaf morphology and spikelet number are two important traits associated with grain yield. To understand how genes coordinating with sink and sources of cereal crops is important for grain yield improvement guidance. Although many researches focus on leaf morphology or grain number in rice, the regulating molecular mechanisms are still unclear. Results In this study, we identified a prohibitin complex 2α subunit, NAL8, that contributes to multiple developmental process and is required for normal leaf width and spikelet number at the reproductive stage in rice. These results were consistent with the ubiquitous expression pattern of NAL8 gene. We used genetic complementation, CRISPR/Cas9 gene editing system, RNAi gene silenced system and overexpressing system to generate transgenic plants for confirming the fuctions of NAL8. Mutation of NAL8 causes a reduction in the number of plastoglobules and shrunken thylakoids in chloroplasts, resulting in reduced cell division. In addition, the auxin levels in nal8 mutants are higher than in TQ, while the cytokinin levels are lower than in TQ. Moreover, RNA-sequencing and proteomics analysis shows that NAL8 is involved in multiple hormone signaling pathways as well as photosynthesis in chloroplasts and respiration in mitochondria. Conclusions Our findings provide new insights into the way that NAL8 functions as a molecular chaperone in regulating plant leaf morphology and spikelet number through its effects on mitochondria and chloroplasts associated with cell division.

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“…The plant hormone, salicylic acid (SA), plays a central role in the overall plant defense response against pathogens and mediates several other aspects of plant growth and development (Vlot et al 2009;Dempsey et al 2011;Klessig et al 2018;Zhang and Li 2019). As observed with other plant hormones, the level of SA within tissues is known to be tightly regulated to ensure the proper function of defense and developmental programs (Zhang et al 2010;Dempsey et al 2011;Seguel et al 2018). With over a half century of research into SA metabolism, the biosynthetic steps toward SA have been almost fully elucidated (Rekhter et al 2019;Torrens-Spence et al 2019).…”

Section: Introductionmentioning

confidence: 99%

Evidence from stable-isotope labeling that catechol is an intermediate in salicylic acid catabolism in the flowers of Silene latifolia (white campion)

Gelder

Forrester

Akhtar

2020

Planta

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PROHIBITIN3 Forms Complexes with ISOCHORISMATE SYNTHASE1 to Regulate Stress-Induced Salicylic Acid Biosynthesis in Arabidopsis

Cited by 56 publications

References 105 publications

Targeted Proteomics Approach Toward Understanding the Role of the Mitochondrial Protease FTSH4 in the Biogenesis of OXPHOS During Arabidopsis Seed Germination

Targeted Proteomics Approach Toward Understanding the Role of the Mitochondrial Protease FTSH4 in the Biogenesis of OXPHOS During Arabidopsis Seed Germination

NAL8 encodes a prohibitin that contributes to leaf and spikelet development by regulating mitochondria and chloroplasts stability in rice

Evidence from stable-isotope labeling that catechol is an intermediate in salicylic acid catabolism in the flowers of Silene latifolia (white campion)

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