Transcriptomic and phosphoproteomic profiling and metabolite analyses reveal the mechanism of NaHCO3-induced organic acid secretion in grapevine roots

Abstract

Background Organic acid secretion is a widespread physiological response of plants to alkalinity. However, the characteristics and underlying mechanism of the alkali-induced secretion of organic acids are poorly understood. Results Oxalate was the main organic acid synthesized and secreted in grapevine (a hybrid of Vitis amurensis , V. berlandieri and V. riparia ) roots, while acetate synthesis and malate secretion were also promoted under NaHCO 3 stress. NaHCO 3 stress enhanced the H + efflux rate of grapevine roots, which is related to the plasma membrane H + -ATPase activity. Transcriptomic profiling revealed that carbohydrate metabolism was the most significantly altered biological process under NaHCO 3 stress; a total of seven genes related to organic acid metabolism were significantly altered, including two phosphoenolpyruvate carboxylases and phosphoenolpyruvate carboxylase kinases. Additionally, the expression levels of five ATP-binding cassette transporters , particularly ATP-binding cassette B19 , and two Al-activated malate transporter 2 s were substantially upregulated by NaHCO 3 stress. Phosphoproteomic profiling demonstrated that the altered phosphoproteins were primarily related to binding, catalytic activity and transporter activity in the context of their molecular functions. The phosphorylation levels of phosphoenolpyruvate carboxylase 3, two plasma membrane H + -ATPases 4 and ATP-binding cassette B19 and pleiotropic drug resistance 12 were significantly increased. Additionally, the inhibition of ethylene synthesis and perception completely blocked NaHCO 3 -induced organic acid secretion, while the inhibition of indoleacetic acid synthesis reduced NaHCO 3 -induced organic acid secretion. Conclusions Our results demonstrated that oxalate was the main organic acid produced under alkali stress and revealed the necessity of ethylene in mediating organic acid secretion. Additionally, we further identified several candidate genes and phosphoproteins responsible for organic acid metabolism and secretion. Electronic supplementary material The online version of this article (10.1186/s12870-019-1990-9) contains supplementary material, which is available to authorized users.

Response Mechanisms of Plants Under Saline-Alkali Stress

“…Transcriptomic profiling in grapevine roots revealed that the underlying mechanism of the NaHCO 3 -induced synthesis of organic acids may be that phosphoenolpyruvate carboxylase catalyzes the carboxylation of phosphoenolpyruvate with -HCO 3 to oxaloacetate, which is then converted into oxalate, acetate and malate. The activity of phosphoenolpyruvate carboxylase was regulated by phosphoenolpyruvate carboxylase kinases, which were substantially upregulated by NaHCO 3 stress (Xiang et al, 2019). A relative study also showed that proton pump H + -ATPase may play an important role in organic acid secretion from roots under NaHCO 3 stress (Guo et al, 2018).…”

Root Involvement in Plant Responses to Adverse Environmental Conditions

“…Abiotic stress causes disturbances mainly to plasma membrane fluidity and it can modify cell membrane components to maintain their integrity and optimal function [65]. Thus, integral membrane proteins (channels and other transporters) and membrane-anchored receptor like kinases can be potential sensors [66,67]. Root capacity to sense variation in osmotic potential is basic to achieve an appropriate response to drought and high salinity.…”

Metabolic and Physiological Changes in the Roots of Two Oat Cultivars in Response to Complex Saline-Alkali Stress

“…Organic acids play an important role in maintaining the cell pH and ion balance ( Fang et al, 2021 ). To cope with high pH, the accumulations of organic acids such as citrate, formate, lactate, acetate, succinate, malate, and oxalate, were observed in tomatoes ( Wang et al, 2011 ), in Chloris virgata ( Yang et al, 2010 ), and in grapevines ( Xiang et al, 2019 ). Organic acids are synthesized to compensate for the deficiency of inorganic anions during saline-alkali stress, especially under alkaline stress ( Guo et al, 2018 ), and they also play a role in osmotic regulation ( Wang et al, 2021 ).…”