The intrinsic chaperone network of Arabidopsis stem cells confers protection against proteotoxic stress

Llamas, Ernesto; Torres‐Montilla, Salvador; Lee, Hyun Ju; Barja, M. Victoria; Schlimgen, Elena; Dunken, Nick; Wagle, Prerana; Werr, Wolfgang; Zuccaro, Alga; Rodríguez‐Concepción, Manuel

doi:10.1111/acel.13446

Cited by 20 publications

(29 citation statements)

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“…In addition, a CCT8-like transcript was dominant in CL3, which then gradually decreased in expression during the differentiation pathway ( Figures 4 A, 4B, and S4 ). CCT8 is part of the chaperone containing T-complex Theta, which assists in protecting stem cells from aggregating proteins and proteomic stress in plants ( Llamas et al., 2021 ) and animals ( Noormohammadi et al., 2016 ), and thus may be important in clearing up defective proteins that can be caused by high ROS production in the proliferating stem cells with high mitochondrial density ( Noormohammadi et al., 2016 ). Tentative stem cells (type 1 in Figure 3 B) are characterized by a high number of mitochondria per cell.…”

Section: Resultsmentioning

confidence: 99%

Characterization of hemocytes and hematopoietic cells of a freshwater crayfish based on single-cell transcriptome analysis

et al. 2022

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Section: Resultsmentioning

confidence: 99%

Characterization of hemocytes and hematopoietic cells of a freshwater crayfish based on single-cell transcriptome analysis

et al. 2022

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“…These results suggest that autophagic regulation of ARF7 abundance might be tissue-specific. Recent findings (Llamas et al , 2021), show that root meristem has tissue specific mechanisms ( i . e .…”

Section: Resultsmentioning

confidence: 99%

NBR1-mediated selective autophagy of ARF7 modulates root branching

Ebstrup

Ansboel

Chevalier

et al. 2022

Preprint

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Auxin is a critical hormone involved in growth and developmental regulation in plants. For instance, auxin dictates the roots architecture via the Auxin Response Factor (ARF) family of transcription factors, which control different aspects of lateral roots (LR) formation. In Arabidopsis, ARF7 is essential for the correct definition of LRs pre-branch sites (PBS) through an oscillatory mechanism controlling gene expression. Moreover, ARF7 also plays a pivotal role during the decision making necessary to initiate LR formation. Despite the relevance of ARF7 to this process, there is a surprising lack of knowledge about how proteostasis of ARF7 is regulated and how this impacts its function during root architecture patterning. Here, we show that ARF7 accumulates in autophagy mutants, localizes to autophagosomes and it is targeted for degradation through selective autophagy via the cargo adaptor NBR1. Moreover, we report that rhythmic changes to ARF7 abundance are a whole plant process and require functional autophagy to occur. Surprisingly, autophagy deficiency does not seem to impact PBS establishment but affects LR formation; this might be explained by the fact that autophagy mainly seems to regulate ARF7 abundance in mature root tissue but only play an accessory role in younger root tissue. In conclusion we report a novel role for autophagy during plant development, through the selective degradation of ARF7 to optimize root branching

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“…Plants are known for their striking resilience to abiotic stress due to their enhanced components of the proteostasis network (Finka et al 2011; Llamas et al 2021). To our knowledge, in contrast to mammals, plants do not suffer from proteinopathies or conformational disorders caused by structural abnormal proteins like amyloids.…”

Section: Discussionmentioning

confidence: 99%

“…Unpredictable daily temperature fluctuations due to global climate change trigger protein misfolding and aggregation resulting in decreased plant growth and productivity (Llamas et al 2021; Zhao et al 2017). Modulating retrograde signaling pathways and rewiring proteostasis mechanisms in crop plants could help to maintain plant productivity even in the face of frequent temperature changes.…”

Section: Discussionmentioning

confidence: 99%

Chloroplast protein import determines plant proteostasis and retrograde signaling

Llamas

Koyuncu

Lee

et al. 2022

Preprint

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Proteins containing polyglutamine (polyQ) repeats are prone to aggregation and can lead to distinct human pathologies. For instance, Huntington's disease is caused by an abnormal expansion of the polyQ stretch (> Q35) of Huntingtin (HTT) protein. However, plants express hundreds of proteins containing polyQ regions, but no pathologies arising from these factors have been reported to date. Here, we ask how plants maintain the proteostasis of polyQ-containing proteins, which are intrinsically enriched in the plant proteomes. To this end, we overexpressed an aggregation-prone fragment of human HTT (Q69) in plant cells. In contrast to invertebrate and mammalian transgenic models, we find that Arabidopsis thaliana plants suppress Q69 aggregation. This elevated proteostasis ability is mediated through the import and degradation of Q69 in chloroplasts. Conversely, inhibition of chloroplast protein import either genetically or pharmacologically reduces the capacity of plant cells to prevent Q69 aggregation. We find that Q69 interacts with the chloroplast stromal processing peptidase (SPP). Notably, expression of synthetic Arabidopsis SPP is sufficient to suppress aggregation of polyQ-expanded HTT in human cells. Beyond ectopically expressed Q69-HTT, endogenous polyQ-containing proteins also aggregate in Arabidopsis upon inhibition of chloroplast import. Among them, the plastid casein kinase 2 (pCK2), which contains a polyQ region next to the chloroplast targeting sequence motif, can also be localized into the nucleus. Upon inhibition of chloroplast import, pCK2 accumulates at higher levels in the nucleus and forms diamond-shaped amyloid-like fibrils surrounding the chloroplasts. These results indicate that the differential conformation and redistribution of pCK2 to the nucleus depends on chloroplast import efficiency, providing a role of polyQ repeats in chloroplast to nucleus communication (i.e. retrograde signaling). Together, our findings establish chloroplast protein import and proteases as determinants of polyQ proteostasis, with important implications for plant biology that can also lead to therapeutic approaches for human diseases that involve protein aggregation.

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The intrinsic chaperone network of Arabidopsis stem cells confers protection against proteotoxic stress

Cited by 20 publications

References 64 publications

Characterization of hemocytes and hematopoietic cells of a freshwater crayfish based on single-cell transcriptome analysis

Characterization of hemocytes and hematopoietic cells of a freshwater crayfish based on single-cell transcriptome analysis

NBR1-mediated selective autophagy of ARF7 modulates root branching

Chloroplast protein import determines plant proteostasis and retrograde signaling

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