mTERF18 and ATAD3 are required for mitochondrial nucleoid structure and their disruption confers heat tolerance in <i>Arabidopsis thaliana</i>

Kim, Minsoo; Schulz, Vincent; Brings, Lea; Schoeller, Theresa; Kühn, Kristina; Vierling, Elizabeth

doi:10.1111/nph.17717

Cited by 28 publications

(18 citation statements)

References 82 publications

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“…On the other hand, mitochondria looked enlarged in size and less electron dense than those from WT, suggesting that it is the mitochondrion that is predominantly affected in radA . Bigger mitochondria were also reported in other mutants impaired in mitochondrial gene expression or genome maintenance, such RNAi lines affected in the expression of organellar RNase P and in mutants of SHOT1 that is apparently involved in the organization of mitochondrial nucleoids [ 33 , 34 ].…”

Section: Resultsmentioning

confidence: 99%

RADA-dependent branch migration has a predominant role in plant mitochondria and its defect leads to mtDNA instability and cell cycle arrest

et al. 2022

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Mitochondria of flowering plants have large genomes whose structure and segregation are modulated by recombination activities. The post-synaptic late steps of mitochondrial DNA (mtDNA) recombination are still poorly characterized. Here we show that RADA, a plant ortholog of bacterial RadA/Sms, is an organellar protein that drives the major branch-migration pathway of plant mitochondria. While RadA/Sms is dispensable in bacteria, RADA-deficient Arabidopsis plants are severely impacted in their development and fertility, correlating with increased mtDNA recombination across intermediate-size repeats and accumulation of recombination-generated mitochondrial subgenomes. The radA mutation is epistatic to recG1 that affects the additional branch migration activity. In contrast, the double mutation radA recA3 is lethal, underlining the importance of an alternative RECA3-dependent pathway. The physical interaction of RADA with RECA2 but not with RECA3 further indicated that RADA is required for the processing of recombination intermediates in the RECA2-depedent recombination pathway of plant mitochondria. Although RADA is dually targeted to mitochondria and chloroplasts we found little to no effects of the radA mutation on the stability of the plastidial genome. Finally, we found that the deficient maintenance of the mtDNA in radA apparently triggers a retrograde signal that activates nuclear genes repressing cell cycle progression.

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Section: Resultsmentioning

confidence: 99%

RADA-dependent branch migration has a predominant role in plant mitochondria and its defect leads to mtDNA instability and cell cycle arrest

et al. 2022

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“…Several studies based on the phenotype of mTERF mutants suggested that these genes are essential for functional acclimation to diverse abiotic stresses, including heat stress [ 94 ]. For instance, it has been shown that an insertional mutant of mTERF18 is more heat-tolerant than the wild-type plants and exhibited higher transcript levels of HSPs in Arabidopsis [ 94 , 95 ].…”

Section: Resultsmentioning

confidence: 99%

Transcriptomic and Physiological Response of Durum Wheat Grain to Short-Term Heat Stress during Early Grain Filling

Arenas‐M

Castillo

Godoy

et al. 2021

Plants

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In a changing climate, extreme weather events such as heatwaves will be more frequent and could affect grain weight and the quality of crops such as wheat, one of the most significant crops in terms of global food security. In this work, we characterized the response of Triticum turgidum L. spp. durum wheat to short-term heat stress (HS) treatment at transcriptomic and physiological levels during early grain filling in glasshouse experiments. We found a significant reduction in grain weight (23.9%) and grain dimensions from HS treatment. Grain quality was also affected, showing a decrease in starch content (20.8%), in addition to increments in grain protein levels (14.6%), with respect to the control condition. Moreover, RNA-seq analysis of durum wheat grains allowed us to identify 1590 differentially expressed genes related to photosynthesis, response to heat, and carbohydrate metabolic process. A gene regulatory network analysis of HS-responsive genes uncovered novel transcription factors (TFs) controlling the expression of genes involved in abiotic stress response and grain quality, such as a member of the DOF family predicted to regulate glycogen and starch biosynthetic processes in response to HS in grains. In summary, our results provide new insights into the extensive transcriptome reprogramming that occurs during short-term HS in durum wheat grains.

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“…In addition to multiple intragenic suppressors (Lee et al, 2005), we also identified extragenic suppressors. We previously reported identification of the extragenic suppressor shot1 (suppressor of hot1-4 1), which is a bypass suppressor mutant with defects in mitochondrial function (30,31). Here, we report the isolation of three additional extragenic suppressor mutants (shot2, 3 and 4) and the identification of the shot2 mutation in a gene encoding the CstF77 protein (AT1G17760), a component of the polyadenylation complex involved in formation of the 3' end of mRNA.…”

Section: Introductionmentioning

confidence: 88%

“…The first mutant allele of CstF77 identified in A. thaliana, cstf77-1, carries a deletion from Y339 to K385 in the HAT-C domain, and was reported as one of the suppressors of overexpressed FLOWERING CONTROL LOCUS A (FCA) (34). A T-DNA insertional knockout allele, cstf77-2, was initially reported to be lethal in the same study (31), but later found to be viable, although it has serious growth defects (43). Importantly, the shot2 mutation has no negative effect on plant growth under standard growth conditions, indicating that the shot2 mutation does not cause any obvious defects to CstF77 function in the absence of temperature stress (Additional file 1: Fig.…”

Section: The Shot2 Gene Encodes Cstf77 a Component Of The Pre-mrna 3′ End Processing Complexmentioning

confidence: 99%

A temperature sensitive mutation in the CstF77 subunit of the polyadenylation complex reveals the critical function of mRNA 3’ end formation for a robust heat stress response in plants

Kim

Swenson

McLoughlin

et al. 2021

Preprint

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BackgroundHeat Shock Protein 101 (HSP101) in plants and orthologs in bacteria (Caseinolytic peptidase B, ClpB) and yeast (Hsp104) are essential for thermotolerance. To investigate molecular mechanisms of thermotolerance involving HSP101, we performed a suppressor screen in Arabidopsis thaliana of a semi-dominant, missense HSP101 allele, hot1-4 (A499T). Plants carrying the hot1-4 mutation are more heat-sensitive than an HSP101 null mutant (hot1-3), indicating the toxicity of hot1-4 allele.ResultsWe report that one suppressor (shot2, suppressor of hot1-4 2) has a temperature-sensitive, missense mutation (E170K) in the CstF77 (Cleavage stimulation factor 77) subunit of the polyadenylation complex, which is critical for 3’ end maturation of pre-mRNA. RNA-Seq analysis of total RNA depleted of ribosomes reveals that heat treatment causes transcriptional readthrough events in shot2, specifically in highly heat-induced genes, including the toxic hot1-4 gene. In addition, failure of correct transcript processing leads to reduced accumulation of many HSP RNAs and proteins, suppressing heat sensitivity of the hot1-4 mutant, due to reduction of the toxic mutant HSP101 protein. Notably, the shot2 mutation makes plants more sensitive to heat stress in the HSP101 null (hot1-3) and wild-type backgrounds correlated with the reduced expression of other heat-inducible genes required for thermotolerance.ConclusionsOur study reveals the critical function of CstF77 for 3’ end formation of mRNA during heat stress, as well as the dominant role of HSP101 in dictating the outcome of severe heat stress in plants.

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mTERF18 and ATAD3 are required for mitochondrial nucleoid structure and their disruption confers heat tolerance in Arabidopsis thaliana

Cited by 28 publications

References 82 publications

RADA-dependent branch migration has a predominant role in plant mitochondria and its defect leads to mtDNA instability and cell cycle arrest

RADA-dependent branch migration has a predominant role in plant mitochondria and its defect leads to mtDNA instability and cell cycle arrest

Transcriptomic and Physiological Response of Durum Wheat Grain to Short-Term Heat Stress during Early Grain Filling

A temperature sensitive mutation in the CstF77 subunit of the polyadenylation complex reveals the critical function of mRNA 3’ end formation for a robust heat stress response in plants

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