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Title: LEA motifs promote desiccation tolerance in vivo
Abstract Background

Cells and organisms typically cannot survive in the absence of water. However, some animals including nematodes, tardigrades, rotifers, and some arthropods are able to survive near-complete desiccation. One class of proteins known to play a role in desiccation tolerance is the late embryogenesis abundant (LEA) proteins. These largely disordered proteins protect plants and animals from desiccation. A multitude of studies have characterized stress-protective capabilities of LEA proteins in vitro and in heterologous systems. However, the extent to which LEA proteins exhibit such functions in vivo, in their native contexts in animals, is unclear. Furthermore, little is known about the distribution of LEA proteins in multicellular organisms or tissue-specific requirements in conferring stress protection. Here, we used the nematodeC. elegansas a model to study the endogenous function of an LEA protein in an animal.

Results

We created a null mutant ofC. elegansLEA-1, as well as endogenous fluorescent reporters of the protein. LEA-1 mutant animals formed defective dauer larvae at high temperature. We confirmed thatC. eleganslacking LEA-1 are sensitive to desiccation. LEA-1 mutants were also sensitive to heat and osmotic stress and were prone to protein aggregation. During desiccation, LEA-1 expression increased and became more widespread throughout the body. LEA-1 was required at high levels in body wall muscle for animals to survive desiccation and osmotic stress, but expression in body wall muscle alone was not sufficient for stress resistance, indicating a likely requirement in multiple tissues. We identified minimal motifs withinC. elegansLEA-1 that were sufficient to increase desiccation survival ofE. coli. To test whether such motifs are central to LEA-1’s in vivo functions, we then replaced the sequence oflea-1with these minimal motifs and found thatC. elegansdauer larvae formed normally and survived osmotic stress and mild desiccation at the same levels as worms with the full-length protein.

Conclusions

Our results provide insights into the endogenous functions and expression dynamics of an LEA protein in a multicellular animal. The results show that LEA-1 buffers animals from a broad range of stresses. Our identification of LEA motifs that can function in both bacteria and in a multicellular organism in vivo suggests the possibility of engineering LEA-1-derived peptides for optimized desiccation protection.

 
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Award ID(s):
2028860
NSF-PAR ID:
10473879
Author(s) / Creator(s):
;
Publisher / Repository:
Springer Science + Business Media
Date Published:
Journal Name:
BMC Biology
Volume:
19
Issue:
1
ISSN:
1741-7007
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
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