Alternative 3′-untranslated regions regulate high-salt tolerance of Spartina alterniflora

High-salt stress continues to challenge the growth and survival of many plants. Alternative polyadenylation (APA) produces mRNAs with different 3′-untranslated regions (3′ UTRs) to regulate gene expression at the post-transcriptional level. However, the roles of alternative 3′ UTRs in response to salt stress remain elusive. Here, we report the function of alternative 3′ UTRs in response to high-salt stress in S. alterniflora (Spartina alterniflora), a monocotyledonous halophyte tolerant of high-salt environments. We found that high-salt stress induced global APA dynamics, and ∼42% of APA genes responded to salt stress. High-salt stress led to 3′ UTR lengthening of 207 transcripts through increasing the usage of distal poly(A) sites. Transcripts with alternative 3′ UTRs were mainly enriched in salt stress-related ion transporters. Alternative 3′ UTRs of HIGH-AFFINITY K+ TRANSPORTER 1 (SaHKT1) increased RNA stability and protein synthesis in vivo. Regulatory AU-rich elements were identified in alternative 3′ UTRs, boosting the protein level of SaHKT1. RNAi-knock-down experiments revealed that the biogenesis of 3′ UTR lengthening in SaHKT1 was controlled by the poly(A) factor CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR 30 (SaCPSF30). Over-expression of SaHKT1 with an alternative 3′ UTR in rice (Oryza sativa) protoplasts increased mRNA accumulation of salt-tolerance genes in an AU-rich element-dependent manner. These results suggest that mRNA 3′ UTR lengthening is a potential mechanism in response to high-salt stress. These results also reveal complex regulatory roles of alternative 3′ UTRs coupling APA and regulatory elements at the post-transcriptional level in plants.