Sulfur redirects carbon metabolism to optimize nitrogen utilization and promote andrographolide biosynthesis in Andrographis paniculata seedlings

Abstract

Sulfur (S) is an important mineral nutrient element that improves plant growth and secondary metabolism. S affects the biosynthesis of andrographolide in medicinal plant Androgaphis paniculata by regulating nitrogen (N) metabolism. However, its specific role in N utilization and the connection with andrographolide biosynthesis have not yet been thoroughly understood. Here, a soilless cultivation experiment with low S (LS, 0.1 mM) and high S (HS, 2.4 mM) was conducted to investigate how S influences carbon (C) metabolism and N utilization to promote andographolide biosynthesis in Andrographis paniculata. The results showed that HS significantly increased plant biomass and N use efficiency (NUE), accompanying with remarkable enhanced andrographolide content. HS promoted the expression of photosynthetic genes, and redirected C metabolism towards to sugars accumulation by enhancing the activities of NAD-dependent glutamate dehydrogenase (NAD-GDH), malic enzyme (ME) and phosphoenolpyruvate carboxykinase (PEPCK) (P < 0.05). On the other hand, HS reduced N and S assimilation, and stimulated a greater N allocation in photosynthesis. Accordingly, NUE was increased and andrographolided biosynthesis could profit from the shift of C resource reallocation. Additionally, the significantly increased activities of ME, glucose 6-phosphate dehydrogenase (G6PDH) and isocitrate dehydrogenase (ICDH) provided reductants for secondary metabolism. HS also considerably upregulated the expression of genes in andrographolide biosynthetic pathway, including ApDXS, ApDXR, ApHDS and ApHDR in the MEP pathway, and ApGGPS. Transcription factors in the families of MYB, WRKY, ERF and bHLH, and plant hormones ABA and JA were in response to HS. Our results revealed that S synergistically promotes NUE and andrographolide biosynthesis via remodeling of C metabolism in A. paniculata.