Genetic polymorphism and transcriptomic analysis reveal LncRunt as a biomarker for growth and low-temperature resistance in the pearl oyster Pinctada fucata martensii

Molluskan aquaculture is increasingly constrained by low-temperature stress, which adversely affects growth and survival rates. To enhance aquaculture efficiency, it is crucial to identify molecular markers associated with growth performance and low-temperature resistance. In this study, we investigated the association between insertions and deletions (InDels) in the LncRunt gene and key phenotypic traits in Pinctada fucata martensii , while also exploring genotype distribution and the molecular mechanisms underlying growth and cold adaptation using transcriptome analysis. Results revealed a key InDel variant (InDel-16) significantly associated with shell growth traits, with individuals carrying the dominant ATATATAT genotype exhibiting significantly greater shell length, width, height, total weight, and shell dry weight ( p < 0.05) compared to other genotypes. This genotype likely enhances somatic growth by modulating the flexibility of LncRunt ’s protein interactions. Three alleles (A, B, and C) were identified at the LncRunt locus, with the C allele characterized by fragment deletions. Genotyping across four populations—including low-temperature resistance lines RF4 and RF5—revealed a strong enrichment of the CC genotype among low-temperature resistance individuals, while it was infrequent in other populations. Expression analysis under 17 °C low-temperature stress showed a significant downregulation of LncRunt expression in individuals from the base stock ( p < 0.05). To investigate its functional role, RNA interference was employed to knockdown LncRunt expression in mantle tissue, leading to the identification of 882 differentially expressed genes. Enrichment analysis revealed that these genes were primarily involved in the PI3K-AKT-mTOR pathways. Moreover, LncRunt knockdown led to reduced expression of key growth-related genes, including PmRunt , structural matrix proteins ( MMP , Pif , and N23 ), and genes associated with the PI3K-mTOR signaling pathway. Collectively, these findings highlight LncRunt as a promising molecular marker for growth and low-temperature resistance, with significant potential for marker-assisted selection and genomic breeding in pearl oyster aquaculture. ● ATATATAT genotype in LncRunt gene Indel-16 is the superior genotype for shell growth in P. f. martensii . ● CC genotype of LncRunt with fragments deletion is predominant in low-temperature-resistant lines. ● The mechanism of LncRunt participated in shell growth and low-temperature resistance explored by RNA-seq.