skip to main content

Explore Research Products in the NSF-PAR

  • NSF Public Access
  • Search Results
  • mTERF18 and ATAD3 are required for mitochondrial nucleoid structure and their disruption confers heat tolerance in Arabidopsis thaliana
Title: mTERF18 and ATAD3 are required for mitochondrial nucleoid structure and their disruption confers heat tolerance in Arabidopsis thaliana
Summary

Mitochondria play critical roles in generating ATP through oxidative phosphorylation (OXPHOS) and produce both damaging and signaling reactive oxygen species (ROS). They have reduced genomes that encode essential subunits of the OXPHOS machinery. Mitochondrial Transcription tERmination Factor‐related (mTERF) proteins are involved in organelle gene expression, interacting with organellar DNA or RNA.

We previously found that mutations inArabidopsis thaliana mTERF18/SHOT1enable plants to better tolerate heat and oxidative stresses, presumably due to low ROS production and reduced oxidative damage.

Here we discover thatshot1mutants have greatly reduced OXPHOS complexes I and IV and reveal that suppressor ofhot1‐41 (SHOT1) binds DNA and localizes to mitochondrial nucleoids, which are disrupted inshot1. Furthermore, three homologues of animal ATPase family AAA domain‐containing protein 3 (ATAD3), which is involved in mitochondrial nucleoid organization, were identified as SHOT1‐interacting proteins. Importantly, disrupting ATAD3 function disrupts nucleoids, reduces accumulation of complex I, and enhances heat tolerance, as is seen inshot1mutants.

Our data link nucleoid organization to OXPHOS biogenesis and suggest that the common defects inshot1mutants and ATAD3‐disrupted plants lead to critical changes in mitochondrial metabolism and signaling that result in plant heat tolerance.

  more » « less
NSF-PAR ID:
10359929
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
New Phytologist
Volume:
232
Issue:
5
ISSN:
0028-646X
Page Range / eLocation ID:
p. 2026-2042
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ; ( , The Journal of Physiology)
    Key points

    Small mammals native to high altitude must sustain high rates of thermogenesis to cope with cold. Skeletal muscle is a key site of shivering and non‐shivering thermogenesis, but the importance of mitochondrial plasticity in cold hypoxic environments remains unresolved.

    We examined high‐altitude deer mice, which have evolved a high capacity for aerobic thermogenesis, to determine the mechanisms of mitochondrial plasticity during chronic exposure to cold and hypoxia, alone and in combination.

    Cold exposure in normoxia or hypoxia increased mitochondrial leak respiration and decreased phosphorylation efficiency and OXPHOS coupling efficiency, which may serve to augment non‐shivering thermogenesis. Cold also increased muscle oxidative capacity, but reduced the capacity for mitochondrial respiration via complex II relative to complexes I and II combined.

    High‐altitude mice had a more oxidative muscle phenotype than low‐altitude mice.

    Therefore, both plasticity and evolved changes in muscle mitochondria contribute to thermogenesis at high altitude.

     Abstract

    Small mammals native to high altitude must sustain high rates of thermogenesis to cope with cold and hypoxic environments. Skeletal muscle is a key site of shivering and non‐shivering thermogenesis, but the importance of mitochondrial plasticity in small mammals at high altitude remains unresolved. High‐altitude deer mice (Peromyscus maniculatus) and low‐altitude white‐footed mice (P. leucopus) were born and raised in captivity, and chronically exposed as adults to warm (25°C) normoxia, warm hypoxia (12 kPa O2), cold (5°C) normoxia, or cold hypoxia. We then measured oxidative enzyme activities, oxidative fibre density and capillarity in the gastrocnemius, and used a comprehensive substrate titration protocol to examine the function of muscle mitochondria by high‐resolution respirometry. Exposure to cold in both normoxia or hypoxia increased the activities of citrate synthase and cytochrome oxidase. In lowlanders, this was associated with increases in capillary density and the proportional abundance of oxidative muscle fibres, but in highlanders, these traits were unchanged at high levels across environments. Environment had some distinct effects on mitochondrial OXPHOS capacity between species, but the capacity of complex II relative to the combined capacity of complexes I and II was consistently reduced in both cold environments. Both cold environments also increased leak respiration and decreased phosphorylation efficiency and OXPHOS coupling efficiency in both species, which may serve to augment non‐shivering thermogenesis. These cold‐induced changes in mitochondrial function were overlaid upon the generally more oxidative phenotype of highlanders. Therefore, both plasticity and evolved changes in muscle mitochondria contribute to thermogenesis at high altitudes.

     
    more » « less
  2. ; ; ; ; ; ; ; ( , New Phytologist)
    Summary

    SUMOylation as one of the protein post‐translational modifications plays crucial roles in multiple biological processes of eukaryotic organisms.Botrytis cinereais a devastating fungal pathogen and capable of infecting plant hosts at low temperature. However, the molecular mechanisms of low‐temperature adaptation are largely unknown in fungi.

    Combining with biochemical methods and biological analyses, we report that SUMOylation regulates pathogen survival at low temperature and oxidative DNA damage response during infection inB. cinerea. The heat shock protein (Hsp70) BcSsb and E3 ubiquitin ligase BcRad18 were identified as substrates of SUMOylation; moreover, their SUMOylation both requires a single unique SUMO‐interacting motif (SIM).

    SUMOylated BcSsb regulates β‐tubulin accumulation, thereby affecting the stability of microtubules and consequently mycelial growth at low temperature. On the contrary, SUMOylated BcRad18 modulates mono‐ubiquitination of the sliding clamp protein proliferating cell nuclear antigen (PCNA), which is involved in response to oxidative DNA damage during infection.

    Our study uncovers the molecular mechanisms of SUMOylation‐mediated low‐temperature survival and oxidative DNA damage tolerance during infection in a devastating fungal pathogen, which provides novel insights into low‐temperature adaptation and pathogenesis for postharvest pathogens as well as new targets for inhibitor invention in disease control.

     
    more » « less
  3. ; ; ; ; ; ; ; ; ( , New Phytologist)
    Summary

    All aerial epidermal cells in land plants are covered by the cuticle, an extracellular hydrophobic layer that provides protection against abiotic and biotic stresses and prevents organ fusion during development.

    Genetic and morphological analysis of the classic maizeadherent1(ad1) mutant was combined with genome‐wide binding analysis of the maize MYB transcription factor FUSED LEAVES1 (FDL1), coupled with transcriptional profiling offdl1mutants.

    We show thatAD1encodes an epidermally‐expressed 3‐KETOACYL‐CoA SYNTHASE (KCS) belonging to a functionally uncharacterized clade of KCS enzymes involved in cuticular wax biosynthesis. Wax analysis inad1mutants indicates thatAD1functions in the formation of very‐long‐chain wax components. We demonstrate that FDL1 directly binds to CCAACC core motifs present inAD1regulatory regions to activate its expression. Over 2000 additional target genes of FDL1, including many involved in cuticle formation, drought response and cell wall organization, were also identified.

    Our results identify a regulatory module of cuticle biosynthesis in maize that is conserved across monocots and eudicots, and highlight previously undescribed factors in lipid metabolism, transport and signaling that coordinate organ development and cuticle formation.

     
    more » « less
  4. ; ; ( , Plant And Cell Physiology)
    Abstract

    ATPase family AAA domain–containing 3 (ATAD3) proteins are unique mitochondrial proteins that arose deep in the eukaryotic lineage but that are surprisingly absent in Fungi and Amoebozoa. These ∼600-amino acid proteins are anchored in the inner mitochondrial membrane and are essential in metazoans and Arabidopsis thaliana. ATAD3s comprise a C-terminal ATPases Associated with a variety of cellular Activities (AAA+) matrix domain and an ATAD3_N domain, which is located primarily in the inner membrane space but potentially extends to the cytosol to interact with the ER. Sequence and structural alignments indicate that ATAD3 proteins are most similar to classic chaperone unfoldases in the AAA+ family, suggesting that they operate in mitochondrial protein quality control. A. thaliana has four ATAD3 genes in two distinct clades that appear first in the seed plants, and both clades are essential for viability. The four genes are generally coordinately expressed, and transcripts are highest in growing apices and imbibed seeds. Plants with disrupted ATAD3 have reduced growth, aberrant mitochondrial morphology, diffuse nucleoids and reduced oxidative phosphorylation complex I. These and other pleiotropic phenotypes are also observed in ATAD3 mutants in metazoans. Here, we discuss the distribution of ATAD3 proteins as they have evolved in the plant kingdom, their unique structure, what we know about their function in plants and the challenges in determining their essential roles in mitochondria.

     
    more » « less
  5. ; ; ; ; ; ; ; ; ; ; et al ( , New Phytologist)
    Summary

    Plant adaptation to a desert environment and its endemic heat stress is poorly understood at the molecular level. The naturally heat‐tolerant Brassicaceae speciesAnastatica hierochunticais an ideal extremophyte model to identify genetic adaptations that have evolved to allow plants to tolerate heat stress and thrive in deserts.

    We generated anA. hierochunticareference transcriptome and identified extremophyte adaptations by comparingArabidopsis thalianaandA. hierochunticatranscriptome responses to heat, and detecting positively selected genes inA. hierochuntica.

    The two species exhibit similar transcriptome adjustment in response to heat and theA. hierochunticatranscriptome does not exist in a constitutive heat ‘stress‐ready’ state. Furthermore, theA. hierochunticaglobal transcriptome as well as heat‐responsive orthologs, display a lower basal and higher heat‐induced expression than inA. thaliana. Genes positively selected in multiple extremophytes are associated with stomatal opening, nutrient acquisition, and UV‐B induced DNA repair while those unique toA. hierochunticaare consistent with its photoperiod‐insensitive, early‐flowering phenotype.

    We suggest that evolution of a flexible transcriptome confers the ability to quickly react to extreme diurnal temperature fluctuations characteristic of a desert environment while positive selection of genes involved in stress tolerance and early flowering could facilitate an opportunistic desert lifestyle.

     
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email