Environmental pH, a highly variable factor that plays a significant role in plant growth. Because it regulates the availability of nutrients, signaling to biotic stresses, elicitation (production of secondary metabolites in response to microbial infection).
Plants. Image Credit: sek_suwat/Shutterstock.com
Changes in the environmental pH cause pronounced changes in microbiome-induced metabolites, nutrient flux, and fluctuations in gene expression associated with microbial and environmental stresses.
Plant growth is dependent on many factors. These factors are the environmental pH, temperature, availability of nutrients, water, and beneficial soil microbiota. Environmental pH is a highly variable growth factor in natural and agricultural soils. It plays a crucial role in nutrient acquisition and the accumulation of beneficial microbiome at the rhizosphere. Environmental pH in plants is connected with many physiological activities like respiration, responses to biotic stresses, growth, toxic ions in the soil, and leaching of anions.
Throughout their life, plants are challenged to many stressful conditions. One such condition can be fluctuations in environmental or external pH. The alterations in external pH led to continuous adjustments in metabolic activities, modification in the pathogen-induced defense genes, and reprogramming of the plant's transcriptional profiles.
Tsai and Schmidt (2021) discussed the enigmatic sensing of the environmental pH in plants. Based on numerous studies, gene expression in plants is regulated by external pH (pHe). And they further discussed the role of trans-acting elements in the perception of the fluctuations in the external pH. Plants may possess and perceive changes in environmental pH through recruiting trans-acting factors that interfere with signaling cascades induced by external stimuli.
Mechanisms underlie the sensing of environmental pH in various biological systems
In fungal organisms such as Saccharomyces cerevisiae and Aspergillus nidulans, the external pH is sensed through the highly conserved pathway Rim101–PacC. In Saccharomyces cerevisiae, the pH is sensed through a plasma membrane complex comprising of Rim21 (the actual sensing component), Rim9 (chaperon), and Rim8 (α-arrestin). In the case of alkaline pH signal, the Rim8 binds with the cytoplasmic tail of Rim21, thus forming a proteolysis complex (Rim23 andRim20). This complex catalyzes the pH-dependent cleavage and activation of the transcription factor Rim10. This transcription factor regulates the expression of genes that are involved in the adaptation to alkaline pH.
In mammalian cells, the external pH is sensed through an alkali-sensing receptor or transmembrane G-protein receptors. These transmembrane proteins monitor hydrogen ion activity extracellular domains and initiate signaling to adapt to alkaline conditions.
The mechanisms of external pH sensing in bacterial cells are well studied. For instance, in Helicobacter pylori, the external pH is sensed through the histidine kinase ArsS sensors and a response regulator ArsR. Any changes in the environmental pH cause the autophosphorylation of the ArsS and transfer of phosphoryl group to the response regulator (ArsR) that subsequently cause the induction of genes involved in acid acclimation.
Like other biological cells, plants also possess external pH sensing mechanisms. In plants, the pH sensing mechanism is dependent on potassium ion fluxes. Different studies in Arabidopsis suggested that it consist of voltage-dependent potassium ion channels known as AtKAT1 and are activated by external stimuli and are critical for low pH. It consists of two histidine residues: one in the pore-forming region (H271) and the other linked with transmembrane proteins.
Transcriptomic studies of the Arabidopsis thaliana revealed that changes in the pH cause a prominent shift in the transcriptional profiles. For example, Arabidopsis plants grown at pH from 6.5 to 4.5 indicates a shift in gene expression.
Similarly, the transcriptomic data of Fe-deficient Arabidopsis plants grown on two pH5.5 or 7.0 conditions. The data revealed a suite of 857 differentially expressed genes, a subset of which was inversely regulated in plants that were subjected to a decrease in media pH. This study leads to the revelations that pH, iron deficiency, and biotic stress signaling mechanisms are interlinked. And led to pH-dependent prioritization of the environmental stimulus.
Iron (Fe) is an essential micronutrient, and it plays a crucial role in metabolic activities such as photosynthesis, respiration, and DNA synthesis. It has a complex relationship with soil pH and abundantly present in mineral soils. However, under alkaline soil conditions, it is not readily available to plants due to toxic hydroxides. Therefore, plants like Arabidopsis produce Fe-mobilizing coumarins that enable the binding of hydroxyl groups to Fe and making it readily available to plants.
Unlike animals, plant cells also have cell walls (a rigid structure that acts as a barrier to many pathogenic microbes). This hard structure is situated between the external environment and the plasma membrane. The cell wall acts as a buffer against rapid changes in the external pH. And contributes to the pH continuum within the apoplast of the acidic exterior to the alkaline milieu. The alkaline environment of the apoplast rigidifies the cell wall and suppresses the environmental stresses imposed on plants.
In all biological systems and particularly in plants, the sensing of external pH is of critical importance. Because in plants, changes in the external pH affect the activity of genes and transcriptomic profiles of cells. The transcriptomic profile of the trans-acting factors localizes the cell nucleus for gene expression to adapt to an acidic environment.