Targeting plant cysteine oxidase activity for improved submergence tolerance

Abstract

SUMMARY Plant cysteine oxidases (PCOs) are plant O2‐sensing enzymes. They catalyse the O2‐dependent step which initiates the proteasomal degradation of Group VII ethylene response transcription factors (ERF‐VIIs) via the N‐degron pathway. When submerged, plants experience a reduction in O2 availability; PCO activity therefore decreases and the consequent ERF‐VII stabilisation leads to upregulation of hypoxia‐responsive genes which enable adaptation to low O2 conditions. Resulting adaptations include entering an anaerobic quiescent state to maintain energy reserves and rapid growth to escape floodwater and allow O2 transport to submerged tissues. Stabilisation of ERF‐VIIs has been linked to improved survival post‐submergence in Arabidopsis, rice (Oryza sativa) and barley (Hordeum vulgare). Due to climate change and increasing flooding events, there is an interest in manipulating the PCO/ERF‐VII interaction as a method of improving yields in flood‐intolerant crops. An effective way of achieving this may be through PCO inhibition; however, complete ablation of PCO activity is detrimental to growth and phenotype, likely due to other PCO‐mediated roles. Targeting PCOs will therefore require either temporary chemical inhibition or careful engineering of the enzyme structure to manipulate their O2 sensitivity and/or substrate specificity. Sufficient PCO structural and functional information should make this possible, given the potential to engineer site‐directed mutagenesis in vivo using CRISPR‐mediated base editing. Here, we discuss the knowledge still required for rational manipulation of PCOs to achieve ERF‐VII stabilisation without a yield penalty. We also take inspiration from the biocatalysis field to consider how enzyme engineering could be accelerated as a wider strategy to improve plant stress tolerance and productivity.

Structural analyses of the plant PRT6-UBR box in the Cys-Arg/N-degron pathway and insights into the plant submergence response

“…Given that plant PRT6 regulates ERF-VIIs levels, and the importance of ERF-VIIs in adapting to submergence, manipulation of PRT6 activity may be an effective strategy to enhance flood tolerance in plants as shown in plant model systems 11,15,17,39 . The ability to manipulate PRT6 is important because the loss of PRT6 activity alters ABA sensitity and causes germination defects in flowering plants 15,18–20 , as shown in similar concept on PCO manipulation 40,41 . However, PRT6 is essential in the plant Arg/N-degron pathway whereas PCO contains five isoforms, which makes PRT6 a more feasible target.…”

Transcriptomic and metabolomic analyses reveal the potential mechanism of waterlogging resistance in cotton (Gossypium hirsutum L.)

“…PCO activity is known as a signaling response to changes in oxygen availability. According to recent reports, during submergence, PCO activity drops, resulting in increased stabilization of ERF-VIIs ( Taylor-kearney and Flashman, 2021 ). However, in this study, PCO DEGs were highly expressed during waterlogging stress but suppressed at no stress in CJ1831056, compared with CJ1831072.…”

Elucidating the callus-to-shoot-forming mechanism in Capsicum annuum ‘Dempsey’ through comparative transcriptome analyses

“…Therefore, we also expected expression changes between clusters 1 and 5, where the expression patterns are thought to be underlying growth and development processes triggered by hypoxia, and Cluster 3, where the expression patterns are thought to underlie shoot formation. This is because, for escaping the depletion of oxygen and energy, the involvement of hypoxia and cell death-related genes during development plays a potential role in regulating cell survival under wound stress and submergence [ 60 , 66 – 70 ]. A previous study by Ikeuch et al (2022) highlighted the significant role of WUSCHEL-RELATED HOMEOBOX 13 (WOX13) in controlling tissue repair mechanisms via wound stress, in regulating WIND2 and WIND3 in callus tissue formation, with RNA-seq data pointing towards hypoxia as a key factor in this process in Arabidopsis [ 61 ].…”