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Abstract The proteins produced just prior to maturation desiccation in the developing, orthodox seed, are stored in the desiccated state and recruited as the functional proteome upon imbibition. For the resumption of protein function, these stored proteins must be protected from permanent denaturation while dehydrating, throughout desiccation, and during rehydration. For some forms of damage there is the possibility of repair following imbibition potentially coordinated with de-aggregation into monodispersed polypeptides capable of refolding into a functional configuration. While studying aspects of the natural protection and repair mechanism in seeds, evidence has accrued that those proteins directly involved in translation are particular targets of both protection and protein repair. Such a phenomenon was first described by Rajjou et al . (2008) examining the frequency with which proteins involved in translation were identified as differentially abundant between aged and un-aged Arabidopsis seeds and the translational competence of aged versus un-aged seeds. The inference drawn from these observations was that, of all the stored proteins, it is imperative that those involved in translation endure desiccation, quiescence and rehydration in a functional state if the seed is to survive. Proteins involved in any other process other than translation can be replaced from the stored transcriptome or by de novo transcription but no mRNA is of value without the translational machinery. This has become known as ‘Job's rule’ in honour of the laboratory from which this hypothesis was first put forward (Rajjou et al ., 2008). We review in this manuscript the evidence accrued to date on which Job's rule is based.
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Protein surface chemistry encodes an adaptive resistance to desiccation
Proteins must be hydrated to function. Desiccation, a common event in an increasing number of ecosystems, can drive proteome-wide unfolding and aggregation. For cells to survive, proteins must disaggregate and retain their function upon rehydration. The molecular determinants that underlie protein desiccation resistance remain unknown. Here, we use mass spectrometry to show that some proteins possess an innate ability to survive dehydration and subsequent rehydration. Structural analysis correlates the ability of proteins to resist desiccation with their surface area chemistry. Remarkably, highly resistant proteins are responsible for the production of the cell's building blocks - amino acids, metabolites, and sugars. Conversely, those proteins that are desiccation-sensitive are responsible for ribosome biogenesis. As a result, the rehydrated proteome is preferentially enriched with metabolite and small molecule producers and depleted of ribosomes - the cell's heaviest consumers. We propose this functional bias allows cells to kickstart their metabolism and promote cell survival upon rehydration.
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- PAR ID:
- 10528468
- Publisher / Repository:
- bioRxiv
- Date Published:
- Format(s):
- Medium: X
- Institution:
- bioRxiv
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript1.0
- Posted Content:
- https://doi.org/10.1101/2024.07.28.604841
