Regulatory feedback response mechanisms to phosphate starvation in rice

Abstract

Phosphorus is a growth-limiting nutrient for plants. The growing scarcity of phosphate stocks threatens global food security. Phosphate-uptake regulation is so complex and incompletely known that attempts to improve phosphorus use efficiency have had extremely limited success. This study improves our understanding of the molecular mechanisms underlying phosphate uptake by investigating the transcriptional dynamics of two regulators: the Ubiquitin ligase PHO2 and the long non-coding RNA IPS1. Temporal measurements of RNA levels have been integrated into mechanistic mathematical models using advanced statistical techniques. Models based solely on current knowledge could not adequately explain the temporal expression profiles. Further modeling and bioinformatics analysis have led to the prediction of three regulatory features: the PHO2 protein mediates the degradation of its own transcriptional activator to maintain constant PHO2 mRNA levels; the binding affinity of the transcriptional activator of PHO2 is impaired by a phosphate-sensitive transcriptional repressor/inhibitor; and the extremely high levels of IPS1 and its rapid disappearance upon Pi re-supply are best explained by Pi-sensitive RNA protection. This work offers both new opportunities for plant phosphate research that will be essential for informing the development of phosphate efficient crop varieties, and a foundation for the development of models integrating phosphate with other stress responses.

Phosphate acquisition efficiency in wheat is related to root:shoot ratio, strigolactone levels, and PHO2 regulation

“…The initial down-regulation of PHO2 proposed in our model was not observed in the time-course experiment, probably because this regulation may occur within hours after Pi deprivation at this developmental stage. On the other hand, the IPS1– miR399 relationship did not fully explain the variation in PHO2 levels, which was in accordance with the responses observed in rice (Ajmera et al , 2018). We suggest two possibilities to explain this fact: (i) there must be more genes involved in this complex regulation; and/or (ii) when IPS1 transcripts reach a certain level, they are sufficient to sequester miR399.…”

“…However, there are only a few studies evaluating the effect of long-term Pi deprivation on the regulation of this pathway. In a time-course study in rice, Ajmera et al (2018) found that the number of IPS1 transcripts increased slowly, but more strongly than those of miR399, leading to a relative increase of PHO2 levels after 1 week of stress. A similar pattern was observed in barley plants after 16 d of Pi starvation, where cultivars showing high levels of HvIPS2 matched with those with higher HvPHO2 expression (Huang et al , 2011).…”

“…It is generally accepted that PHO2 activity is rapidly reduced under Pi deficiency due to high induction of miR399 in the first hours of stress, which overcomes protection by IPS1 (Ajmera et al , 2018). However, there are only a few studies evaluating the effect of long-term Pi deprivation on the regulation of this pathway.…”

“…Therefore, it seems that the regulation of P signalling and homeostasis by the triad IPS1 –miR399– PHO2 is dynamic, showing a different regulation over time. Based on the responses observed in wheat seedlings and other model plants at different developmental stages (Huang et al , 2011; Ouyang et al , 2016; Ajmera et al , 2018), we propose a model to explain the behaviour of these three regulators during early and late responses upon Pi starvation (Fig. 8).…”

An Integrative Systems Perspective on Plant Phosphate Research

“…With regard to resource acquisition by plants, a range of models at various physical (generally, supra-tissue) scales has been developed. These represent aspects of uptake of nutrient, water or contaminants [ 141 , 142 , 143 , 144 , 145 , 146 , 147 , 148 , 149 , 150 ], and the effect on soil nutrient availability of microbial [ 151 , 152 , 153 ] and exudate dynamics [ 154 ].…”