Allantoin, a purine metabolite, confers saline–alkaline tolerance to sugar beet by triggering a self-amplifying feedback loop comprising jasmonic acid and nitric oxide

Abstract

Saline–alkaline (SA) soil inhibits plant growth and development. A few plants have evolved strategies to combat SA stress, but the underlying mechanisms remain elusive. In the current study, we performed a combined proteome and metabolome profiling to capture the major pathways and specified metabolites involved in the sugar beet tolerance to SA stress. Protein abundance and metabolite accumulation in purine metabolism were altered to favour allantoin accumulation under SA stress. Exogenous allantoin alleviated the oxidative damage caused by SA stress, whereas inhibition of allantoin biosynthesis weakened SA tolerance. Transcriptome analysis revealed that allantoin altered the expression patterns of genes involved in jasmonic acid (JA) and nitric oxide (NO) biosynthesis to elevate their levels under SA stress. Inhibition of allantoin biosynthesis completely abolished the JA and NO accumulation. The application of JA and NO promoted the accumulation of each other, and both enhanced SA tolerance. Inhibition of JA biosynthesis completely abolished allantoin-induced SA tolerance and NO accumulation and weakened sodium nitroprusside (SNP, a donor of NO) -induced SA tolerance, whereas inhibition of NO biosynthesis only attenuated allantoin-induced SA tolerance and JA accumulation and JA-induced SA tolerance. Our results suggest that allantoin accumulation is assisted under SA stress, promoting JA accumulation and consequently NO biosynthesis. Subsequently, NO in turn assists JA biosynthesis, forming a self-amplifying feedback loop, in which JA and NO synergistically improve SA tolerance. The current study provides a novel insight into SA tolerance in sugar beet and preliminary reveals the regulatory role of allantoin in SA tolerance.