Loss of the SNARE protein Sec22p selectively represses caesium accumulation in yeast and plants

The rare alkali ion caesium (Cs+) is assimilated by eukaryotes,
even though it is not an essential nutrient. It poses an
environmental concern through the anthropogenic release of its
radioisotopes, 134Cs and 137Cs. Bioavailability and long half-lives
favour its uptake and accumulation in plants, via which
radiocaesium can be introduced to the food chain. Cs+ ions are
taken up via potassium-(K+)-related pathways due to the biophysical
similarity of these cations. This makes it difficult to solely
manipulate Cs+ accumulation in plants without disturbing the
homeostasis of essential ions at the same time. This work shows
that the soluble N-ethylmaleimide sensitive factor attachment
receptor (SNARE) Sec22p, previously described as a member of the
protein sorting machinery, specifically affects Cs+ accumulation in
yeast by regulating the selectivity of vacuolar deposition. A
similar phenotype became apparent for a homologous plant protein,
SEC22. The loss of Saccharomyces cerevisiae Sec22p reduces Cs+
uptake by more than half, while at the same time leaving essential
cations undisturbed. Mathematical modelling of wild-type and mutant
Cs+ uptake kinetics proposes that sec22Δ is defective in vacuolar
compartmentalisation of Cs+, which is proven by biochemical
fractionation. Morphological alterations were not produced by the
loss of Sec22p, only a Cs+-dependent vacuolar fragmentation can be
observed. These results indicate a so far undescribed function of
Sec22p in assuring a non-selective ion deposition to the vacuole,
which is necessary in ion detoxification, while its loss induces
discrimination against vacuolar Cs+ deposition. A developmentally
controlled loss-of-function mutant of the orthologous gene SEC22
(At1g11890) in A. thaliana displays a similar phenotype, having
specifically reduced Cs+ enrichment without detrimental growth
defects, thereby translating the yeast findings to a multicellular
context. Furthermore, a functional complementation of the yeast
mutant Cs+ phenotype by the plant gene transcript was possible.
Selective reduction of Cs+ accumulation in plants by loss of a
single gene product represents a new route to limit radiocaesium
input to the food chain without disturbing basic plant nutrition
and growth.