Haplotype-resolved telomere-to-telomere genome of Aphelenchus avenae implicates P5CS in nematode desiccation stress response

Abstract

The remarkable ability to survive desiccation and persist in a dry state is among nature's most fascinating adaptations, enabling certain organisms to withstand extreme dehydration without damage. This phenomenon has been widespread across diverse life forms, including plants, fungi, and nematodes. However, our understanding of its molecular basis, particularly in animals, remains limited. Aphelenchus avenae nematodes are notable for their exceptional tolerance to dehydration, and multiple genes related to this trait have been identified. However, the absence of a chromosome-scale, high-contiguity genome for A. avenae has been a limitation in the genome-wide identification of gene families potentially involved in desiccation tolerance. In this study, we assemble a high-quality, telomere-to-telomere haplotype genome of A. avenae. Transcriptomic analyses reveal distinct sets of genes involved in responses to desiccation and freezing stress. Notably, under desiccation stress, several desiccation-tolerance genes exhibit allelic imbalance expression. Among these, we identify the stress response gene P5CS in A. avenae nematodes. Aap5cs RNAi experiments demonstrate that knockdown of Aap5cs results in increased accumulation of reactive oxygen species under desiccation stress and reduced desiccation survival time, suggesting that Aap5cs plays a role in the stress response of A. avenae. This finding also raises the possibility of functional parallels between plant and nematode responses to dehydration. This study enhances our understanding of nematode resistance to desiccation stress and provides valuable genetic resources for investigating the intricate regulatory pathway that organisms use for dehydration stress adaptation.