WHIRLY2 plays a key role in mitochondria morphology, dynamics, and functionality in <i>Arabidopsis thaliana</i>

Golin, Serena; Negroni, Yuri L.; Bennewitz, Bationa; Klösgen, Ralf Bernd; Mulisch, Maria; Rocca, Nicoletta La; Cantele, Francesca; Vigani, Gianpiero; Schiavo, Fiorella Lo; Krupinska, Karin; Zottini, Michela

doi:10.1002/pld3.229

Cited by 17 publications

(47 citation statements)

References 47 publications

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“…During seed germination, normal mitochondrial biogenesis and mtDNA copy number are tightly controlled (Paszkiewicz et al, 2017). This connection between seed germination and mitochondrial defects was also reported in many other studies (Han et al, 2010; Virdi et al, 2015; Van Aken et al, 2016; Heidorn-Czarna et al, 2018; Golin et al, 2020). We showed that variation in root lengths at 5 DAS was heritable among different msh1 mutant families.…”

Section: Discussionsupporting

confidence: 86%

Long-read sequencing characterizes mitochondrial and plastid genome variants in Arabidopsismsh1mutants

Zou

Zhu

Sloan

et al. 2022

Preprint

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The abundant repeats in plant mitochondrial genomes can cause rapid genome rearrangements and are also a major obstacle in short-read sequencing studies. Nuclear-encoded proteins such as MSH1 are known to suppress the generation of repeat-associated mitochondrial genome variants, but our understanding of these mechanisms has been constrained by the limitations of short-read technologies. Here, we used highly accurate long-read sequencing (PacBio HiFi) to characterize mitochondrial and plastid genome variants in Arabidopsis thaliana msh1 mutant individuals. The HiFi reads successfully quantified parental and crossover recombination products of both large and small repeats, providing a global view of recombination dynamics. We found that recombination breakpoints were distributed relatively evenly across the length of repeated sequences and observed extensive non-crossover recombination (gene conversion) between pairs of imperfect repeats in the mitochondrial genome of msh1 mutants. Comparison of long-read assemblies of seven other Arabidopsis thaliana accessions showed that mitochondrial genome structural divergence between accessions paralleled the repeat-mediated dynamics observed in msh1 mutants. The Arabidopsis plastid genome generally lacks small repeats and exhibited a very different pattern of variant accumulation in msh1 mutants compared with the mitochondrial genome. Our data illustrate the power of HiFi technology in studying repeat-mediated recombination in plant mitochondrial genomes and improved the sequence resolution for recombinational processes suppressed by MSH1.

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Section: Discussionsupporting

confidence: 86%

Long-read sequencing characterizes mitochondrial and plastid genome variants in Arabidopsismsh1mutants

Zou

Zhu

Sloan

et al. 2022

Preprint

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“…While the algae and Marchantia have only one WHIRLY-like protein, higher plant species have at least two WHIRLY proteins. Both have an organelle targeting peptide at the N-terminus, directing them either to mitochondria, plastids, or both organelles ( Krause et al, 2005 ; Golin et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

WHIRLIES Are Multifunctional DNA-Binding Proteins With Impact on Plant Development and Stress Resistance

et al. 2022

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WHIRLIES are plant-specific proteins binding to DNA in plastids, mitochondria, and nucleus. They have been identified as significant components of nucleoids in the organelles where they regulate the structure of the nucleoids and diverse DNA-associated processes. WHIRLIES also fulfil roles in the nucleus by interacting with telomers and various transcription factors, among them members of the WRKY family. While most plants have two WHIRLY proteins, additional WHIRLY proteins evolved by gene duplication in some dicot families. All WHIRLY proteins share a conserved WHIRLY domain responsible for ssDNA binding. Structural analyses revealed that WHIRLY proteins form tetramers and higher-order complexes upon binding to DNA. An outstanding feature is the parallel localization of WHIRLY proteins in two or three cell compartments. Because they translocate from organelles to the nucleus, WHIRLY proteins are excellent candidates for transducing signals between organelles and nucleus to allow for coordinated activities of the different genomes. Developmental cues and environmental factors control the expression of WHIRLY genes. Mutants and plants with a reduced abundance of WHIRLY proteins gave insight into their multiple functionalities. In chloroplasts, a reduction of the WHIRLY level leads to changes in replication, transcription, RNA processing, and DNA repair. Furthermore, chloroplast development, ribosome formation, and photosynthesis are impaired in monocots. In mitochondria, a low level of WHIRLIES coincides with a reduced number of cristae and a low rate of respiration. The WHIRLY proteins are involved in the plants’ resistance toward abiotic and biotic stress. Plants with low levels of WHIRLIES show reduced responsiveness toward diverse environmental factors, such as light and drought. Consequently, because such plants are impaired in acclimation, they accumulate reactive oxygen species under stress conditions. In contrast, several plant species overexpressing WHIRLIES were shown to have a higher resistance toward stress and pathogen attacks. By their multiple interactions with organelle proteins and nuclear transcription factors maybe a comma can be inserted here? and their participation in organelle–nucleus communication, WHIRLY proteins are proposed to serve plant development and stress resistance by coordinating processes at different levels. It is proposed that the multifunctionality of WHIRLY proteins is linked to the plasticity of land plants that develop and function in a continuously changing environment.

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“…PPRs are RNA‐binding proteins and are found in complexes of organellar mRNA‐editing machineries in plants, which play roles in photosynthesis and respiration, as well as plant development and environmental responses (Barkan and Small, 2014). On the other hand, WHY3 is a member of the three‐gene WHIRLY family of single‐stranded DNA‐binding proteins in Arabidopsis (Cappadocia et al., 2013) and is believed to localize dually in the nucleus or in plastids and mitochondria (Golin et al., 2020; Jiang et al., 2017; Marechal et al., 2009). Its closest homolog WHY1 represses the senescence marker gene WRKY53 and coordinates leaf senescence in a developmental stage‐dependent manner (Huang et al., 2017, 2018; Lin et al., 2019; Miao et al., 2013; Ren et al., 2017).…”

Section: Discussionmentioning

confidence: 99%

“…The WHIRLY family includes the well‐known leaf senescence regulator WHY1 (Miao et al., 2013), the closest paralog of WHY3 . Although WHY3 was recently reported to be involved in protein trafficking between organelles in response to stress (Golin et al., 2020), the detailed role in connection with miR840 is poorly known.…”

Section: Introductionmentioning

confidence: 99%

MicroRNA840 (MIR840) accelerates leaf senescence by targeting the overlapping 3′UTRs of PPR and WHIRLY3 in Arabidopsis thaliana

Ren

Wan-zhen

et al. 2021

The Plant Journal

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SUMMARY MicroRNAs negatively regulate gene expression by promoting target mRNA cleavage and/or impairing its translation, thereby playing a crucial role in plant development and environmental stress responses. In Arabidopsis, the MIR840 gene is located within the overlapping 3′UTR of the PPR and WHIRLY3 (WHY3) genes, both being predicted targets of miR840* and miR840, the short maturation products of MIR840. Gain‐ and loss‐of‐function of MIR840 in Arabidopsis resulted in opposite senescence phenotypes. The highest expression levels of the MIR840 precursor transcript pre‐miR840 were observed at senescence initiation, and pre‐miR840 expression is significantly correlated with a reduction in PPR, but not WHY3, transcript levels. Although a reduction of transcript level of PPR, but not WHY3 transcript levels were not significantly affected by MIR840 overexpression, its protein levels were strongly reduced. Mutating the cleavage sites or replacing the target sequences abolishes the miR840*/miR840‐mediated degradation of PPR transcripts and accumulation of WHY3 protein. In support for this, concurrent knockdown of both PPR and WHY3 in wild‐type plants resulted in a senescence phenotype resembling that of the MIR840‐overexpressing plant. This indicates that both PRR and WHY3 are targets in the MIR840‐mediated senescence pathway. Moreover, single knockout mutants of PPR and WHY3 show a convergent upregulated subset of senescence‐associated genes, which are also found among those induced by MIR840 overexpression. Our data provide evidence for a regulatory role of MIR840 in plant senescence.

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WHIRLY2 plays a key role in mitochondria morphology, dynamics, and functionality in Arabidopsis thaliana

Cited by 17 publications

References 47 publications

Long-read sequencing characterizes mitochondrial and plastid genome variants in Arabidopsismsh1mutants

Long-read sequencing characterizes mitochondrial and plastid genome variants in Arabidopsismsh1mutants

WHIRLIES Are Multifunctional DNA-Binding Proteins With Impact on Plant Development and Stress Resistance

MicroRNA840 (MIR840) accelerates leaf senescence by targeting the overlapping 3′UTRs of PPR and WHIRLY3 in Arabidopsis thaliana

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