Abstract
BackgroundOrganic 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.ResultsOxalate 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 NaHCO3 stress. NaHCO3 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 NaHCO3 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 NaHCO3 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 NaHCO3-induced organic acid secretion, while the inhibition of indoleacetic acid synthesis reduced NaHCO3-induced organic acid secretion.ConclusionsOur 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.
Highlights
Organic acid secretion is a widespread physiological response of plants to alkalinity
Similar differences in organic acid concentrations were found in the culture solution (Fig. 1g-l); oxalate was the main organic acid synthesized and secreted by grapevine roots
The other organic acids were generally not affected by NaHCO3 treatment
Summary
Organic acid secretion is a widespread physiological response of plants to alkalinity. The characteristics and underlying mechanism of the alkali-induced secretion of organic acids are poorly understood. Soil alkalinity is an important environmental problem, and alkali stress primarily caused by NaHCO3 and Na2CO3 severely affects crop growth and development in more than 434 million hectares of land worldwide [1]. Plants must regulate intracellular pH and the pH outside roots to maintain root functions. Organic acids play a key role in regulating the cell and rhizosphere pH levels. It was reported that organic acid metabolism is closely correlated with alkali stress tolerance [4]. Puccinellia tenuiflora roots accumulate and secrete citric acid into the rhizosphere in response to alkali stress [5].
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