Kisko M, Bouain N, Safi A, Medici A, Akkers RC, Secco D, Fouret G, Krouk G, Aarts MGM, Busch W, Rouached H✉ (2018) LPCAT1 controls phosphate homeostasis in a zinc-dependent manner. eLife, 7:e32077

In this study, we uncover the molecular and genetic bases for a highly important and conserved nutrient interaction: the interaction of Zinc and Phosphate. While it is clear the homeostasis of different nutrients is highly dependent on each other, they are usually studied independent of each other. Here we make significant progress in going towards a more integrative comprehension of the problem and identify key components and a complete molecular pathway underlying zinc dependent phosphate homeostasis.

 

Given the paucity of past studies assessing the biological significance of mineral nutrient homeostasis interaction, very little is known about the genetic and molecular basis of such interactions. We go significantly beyond previous investigations, identifying a novel pathway controlling Pi homeostasis that depends on the Zn status of the plant, in which the gene LPCAT1 and its effect on the composition phospholipid populations have central roles. Overall, we think there are several notable aspects of our work. First, this work reports the first GWA analysis on the accumulation of Pi not only in control condition but also in response to nutritional stress that affect Pi homeostasis, namely Zn deficiency (-Zn). We show that this trait is largely governed by genetic factors, and identified the Lyso-PhosphatidylCholine AcylTransferase 1 (LPCAT1) as key determinant of shoot Pi accumulation specifically under -Zn. We go on to show that regulatory variation at this locus contributes significantly to this natural variation.  Second, we provide evidence that LPCAT1 is downstream of the major regulators of -Zn signalling, bZIP23 transcription factors, providing a plausible mechanistic link between Zn deficiency signal and the regulation of the expression of LPCAT1. In silico analysis coupled with EMSA enabled us to provide evidences that bZIP23 not only can bind to the LPCAT1 promoter, but also, more importantly we identified a binding site for bZIP23; this new motif show polymorphism between different accessions having a contrasting capacity to accumulate Pi in -Zn. Using reverse genetic approaches we show that mutation in bZIP23 or LPCAT1 alters the phospholipid Lyso-PhosphatidylCholine/PhosphatidylCholine (Lyso-PC/PC) ratio, suggesting that phospholipid might be involved in Zn deficiency signalling, which is in line with reports in other organisms like yeast and mammalian cells. Third, expression analyses performed in lpcat1 mutant grown in -Zn reveals that the most important Pi transports PHT1 ;1 is induced shoots, pointing towards a novel and specific role for this Pi transporter in shoots Pi accumulation in response to Zn deficiency stress. This study therefore uncovers a fundamental link between phospholipid metabolism and Pi-Zn homeostasis interaction via LPCAT1, and lays the foundations to explore a new role for Lyso-PC and PC in control of macro- and micronutrients homeostasis interaction. Moreover, our discoveries offer a new perspective on how to improve Pi content in plants, as our findings suggests that modulating the Zn-deficiency signalling pathway might be a good and simple approach for that.