Local and Systemic Response to Heterogeneous Sulfate Resupply after Sulfur Deficiency in Rice

Sulfur (S) is an essential mineral nutrient required for plant growth and development. Plants usually face temporal and spatial variation in sulfur availability, including the heterogeneous sulfate content in soils. As sessile organisms, plants have evolved sophisticated mechanisms to modify their gene expression and physiological processes in order to optimize S acquisition and usage. Such plasticity relies on a complicated network to locally sense S availability and systemically respond to S status, which remains poorly understood. Here, we took advantage of a split-root system and performed transcriptome-wide gene expression analysis on rice plants in S deficiency followed by sulfate resupply. S deficiency altered the expressions of 6749 and 1589 genes in roots and shoots, respectively, accounting for 18.07% and 4.28% of total transcripts detected. Homogeneous sulfate resupply in both split-root halves recovered the expression of 27.06% of S-deficiency-responsive genes in shoots, while 20.76% of S-deficiency-responsive genes were recovered by heterogeneous sulfate resupply with only one split-root half being resupplied with sulfate. The local sulfate resupply response genes with expressions only recovered in the split-root half resupplied with sulfate but not in the other half remained in S deficiency were identified in roots, which were mainly enriched in cellular amino acid metabolic process and root growth and development. Several systemic response genes were also identified in roots, whose expressions remained unchanged in the split-root half resupplied with sulfate but were recovered in the other split-root half without sulfate resupply. The systemic response genes were mainly related to calcium signaling and auxin and ABA signaling. In addition, a large number of S-deficiency-responsive genes exhibited simultaneous local and systemic responses to sulfate resupply, such as the sulfate transporter gene OsSULTR1;1 and the O-acetylserine (thiol) lyase gene, highlighting the existence of a systemic regulation of sulfate uptake and assimilation in S deficiency plants followed by sulfate resupply. Our studies provided a comprehensive transcriptome-wide picture of a local and systemic response to heterogeneous sulfate resupply, which will facilitate an understanding of the systemic regulation of S homeostasis in rice.