Acquisition of hypoxia inducibility by oxygen sensing N-terminal
cysteine oxidase in spermatophytes
Abstract
N-terminal cysteine oxidases (NCOs) use molecular oxygen to oxidize the
amino-terminal cysteine of specific proteins, thereby initiating the
proteolytic N-degron pathway. To expand the characterization of the
plant family of NCOs (PCOs), we performed a phylogenetic analysis across
different taxa in terms of sequence similarity and transcriptional
regulation. Based on this survey, we propose a distinction of PCOs into
two main groups. A-type PCOs are conserved across all plant species and
are generally unaffected at the mRNA level by oxygen availability.
Instead, B-type PCOs differentiated in spermatophytes to acquire
transcriptional regulation in response to hypoxia. The inactivation of
two A-type PCOs in Arabidopsis thaliana, PCO4 and PCO5, is sufficient to
activate the anaerobic response in young seedlings, whereas the
additional removal of B-type PCOs leads to a stronger induction of
anaerobic genes and impairs plant growth and development. Our results
show that both PCO types are required to regulate the anaerobic response
in angiosperms. Therefore, while it is possible to distinguish two
clades within the PCO family, we conclude that they all contribute to
restrain the anaerobic transcriptional program in normoxic conditions
and together generate a molecular switch to toggle the hypoxic response.