All living organisms require an adequate supply of nutrients for growth and survival. Nutrient deficiencies lead to decreased plant survival and lower nutritional value of foods, which have a profound impact on human health (Myers et al., 2014). In particular, zinc (Zn) and iron (Fe) deficiencies affect up to 2 billion people worldwide (Hilty et al., 2010). According to the World Health Organization, about 800,000 child deaths per year are attributable to Zn deficiency alone (Akhtar, 2013). The widespread occurrence of deficiencies in micronutrients such as Zn and Fe in human populations is due to low dietary intake (Rouached, 2013; Myers et al., 2014; Shahzad et al., 2014). In the light of crop optimization for yield and nutritional quality, it is therefore an important goal to understand the genetic and molecular basis of plant nutrition. A complicating circumstance is that plant uptake, storage and use of these nutrients are partly dependent of each other (Rouached and Rhee, 2017). For instance, physiological Zn deficiency leads to over-accumulation of phosphorus (P) in the shoots (for review, Bouain et al., 2014; Kisko et al., 2015). Noteworthy, when the Zn supply is low, increasing P supply causes a reduction of plant height, delayed development and severe leaf symptoms including chlorosis and necrosis (Ova et al., 2015). At high P supplies, Zn deficiency associated with elevated shoot P levels causes P toxicity (Marschner, 2012). Interestingly, this P-Zn interaction is also recognized in a wide variety of other biological systems, including rats (Wallwork et al., 1983), human cells (Sandström and Lönnerdal, 1989), and multiple fungal species (Freimoser et al., 2006). In Saccharomyces cerevisiae yeast, the Zn status acts as a major determinant of the ability to store P (Simm et al., 2007). Much like Zn nutrition, P homeostasis is of global relevance as current agricultural practices require large amounts of P. At the same time, world-wide P reserves are becoming increasingly scarce and a potential P crisis looms for agriculture at the end of this 21 st century (Abelson, 1999; Neset and Cordell, 2012). How P and Zn homeostases are coordinated is therefore not only a fundamental biological question but has also serious implications for global agronomic and biotechnological applications.

P is a critical component of many metabolites and macromolecules, including nucleic acids and phospholipids (PLs) (Poirier and Bucher, 2002; Rouached et al., 2010). Of equal importance, Zn provides chemical, structural and regulatory functions in biological systems (Christianson, 1991), for instance as cofactor for hundreds of enzymes, or by binding to PLs to maintain membrane structure (Binder et al., 2001; Sinclair and Krämer, 2012). Plants have evolved the ability to adjust to large fluctuations in external P or Zn supply. P is taken up by the root system in the form of inorganic phosphate (Pi). In Arabidopsis thaliana (Arabidopsis), this uptake relies on members of the high affinity Pi transporter family (PHT1) (Nussaume et al., 2011), of which PHT1;1 is the major contributor (Ayadi et al., 2015). Upon P deficiency, the expression of some PHT1 transporters increases as a result of the activation of the ‘PHR1-miR399-PHO2’ signalling pathway (Bari et al., 2006; Lin et al., 2008; Pant et al., 2008), causing a strong increase in the acquisition of Pi and its subsequent translocation to the shoots (Lin et al., 2008; Pant et al., 2008). In contrast to our understanding of the molecular mechanisms involved in sensing and signalling of Pi abundance (Chiou and Lin, 2011; Zhang et al., 2014), little is known about how plants sense and signal Zn deficiency. A putative working model of Zn deficiency signalling was proposed by Assunção et al. (2013), which is centred around two essential members of the bZIP transcription factor (TF) family in Arabidopsis, bZIP19 and bZIP23, without which plants are unable to respond to Zn starvation by inducing the expression of genes involved in Zn uptake and distribution such as the zinc transporter ZIP4 (Assunção et al., 2010). Beyond common set of genes targeted by these two TFs, each TF could regulate distinct genes (Inaba et al., 2015), but the identity of distinctive binding site recognized by each remains poorly unknown. Identifying such binding motif is necessary to better understand how plants regulate Zn homeostasis.

The interaction between Zn and Pi homeostasis in plants is also obvious at the molecular level (for reviews, Bouain et al., 2014; Kisko et al., 2015). For instance, Zn deprivation causes an up-regulation of PHT1;1 and consequently an over-accumulation of Pi in Arabidopsis thaliana (Jain et al., 2013; Khan et al., 2014). The expression of Pi uptake transporters is normally tightly controlled in roots in response to the P status of the plant, but it is clear that this tight control is lost under Zn deficiency. Remarkably, although the involvement of PHOSPHATE RESPONSE1 transcription factor (PHR1) in the coordination of Pi-Zn homeostasis has been demonstrated (Khan et al., 2014), the Zn deficiency-induced Pi uptake transporter expression is independent of the aforementioned canonical ‘PHR1-miR399-PHO2’ signalling pathway (Khan et al., 2014), indicative of room for new discoveries in Pi homeostasis under Zn deficiency in plants.

In this study, we set out to identify the genes controlling such novel mechanisms to cause Pi accumulation in shoots of Zn-deficient Arabidopsis plants. Genome wide association (GWA) mapping was employed using a subset of 223 Arabidopsis accessions from the RegMap panel (Horton et al., 2012), which enabled us to demonstrate that there is heritable natural variation of Pi accumulation in responses to Zn deficiency and that one major locus governing this is the LysoPhosphatidylCholine AcylTransferase 1 (LPCAT1) gene.Under Zn deficiency, lpcat1 mutants showed an alteration in the phospholipids Lyso-PhosphatidylCholine/PhosphatidylCholine (Lyso-PC/PC) ratio, and an up-regulation of the expression of the main high affinity Pi transporter gene PHT1;1. Finally, we demonstrate that LPCAT1 acts downstream of one of the two key Zn starvation signalling TFs, bZIP23, for which we identified a new binding site sequence. Overall, this study uncovered a novel pathway, in which LPCAT1 plays a key role in the coordination of Pi homeostasis and Zn deficiency response in plants through modulation of phospholipid metabolism and Pi transporter expression.

Understanding how Zn and Pi homeostasis are wired to regulate growth is crucial to offer a new perspective of improving Pi nutrition in plants by modulating the Zn-deficiency signalling pathway. Our study provides a first insight into the genetic and molecular mechanism that controls shoot Pi concentration under –Zn in plants by discovering a pathway which includes the –Zn response TF bZIP23 that target the LPCAT1, and the Pi transporter PHT1;1.

In A. thaliana, GWAS has been shown to be a powerful approach to detect loci involved in natural variation of complex traits including variation in the accumulation of non-essentials or toxic elements in plants, such as sodium (Baxter et al., 2010), cadmium (Chao et al., 2012) or arsenic (Chao et al., 2014). Here we used GWAS to identify genes involved in the regulation of the essential macronutrient (P) concentration in its anionic form (Pi) in plants grown under control conditions (+Zn) and -Zn. In both conditions, our GWA analysis reveals that there is widespread natural variation in shoot Pi concentration, and supports the existence of genetic factors that affect this trait (Figure 1). The GWAS data support the –Zn specificity of this response, since no association was detected around the LPCAT1 locus in our control condition (+Zn) (Figure 1). The presence of the Zinc Deficiency Response Element (ZDRE) (Assunção et al., 2010) in the promoter of LPCAT1 and more particularly the newly identified binding motif specific for bZIP23 (Figures 2 and 3) in the 5’ untranslated leader of LPCAT1 is a strong argument supporting the Zn-dependency of this response.

A ZDRE is present in the promoter regions of many genes targeted by bZIP19 and bZIP23 (Assunção et al., 2010). In addition to their positive regulatory role by inducing several Zn deficiency related genes, publicly available microarray showed that bZIP19 and bZIP23 may have a negative regulatory role as many genes were induced in the bzip19/bzip23 mutant background compared to WT plants grown in –Zn (Azevedo et al., 2016). A functional redundancy of these two TFs was proposed based on the oversensitivity of the bzip19 and bzip23 double mutant to –Zn, which was not observed with either bzip19 or bzip23 single mutants (Assunção et al., 2010). This redundancy may not be absolute, as recent physiological and genetic evidence indicates that bZIP19 and bZIP23 are not completely redundant and they not only regulate the same, but also separate sets of genes in Arabidopsis (Inaba et al., 2015). Our results support this finding by showing that only bZIP23 is involved in regulating LPCAT1 in response to -Zn. bZIP23 is likely to do so through two cis-elements in the non-coding part of the LPCAT1 gene. One being the aforementioned ZDRE, which can also be bound by the bZIP19 paralogue of bZIP23, the other a novel binding motif, with versions TGTCACA and TGTCGAA, which are specifically bound by bZIP23. Worth noting, in the accessions panel used in our work one other allele can be found, in the Alc-0 accession (TGTCAAA) that displayed the lowest Pi accumulation in our panel of accession (Supplementary file 3, Figure 3—figure supplement 1). Alc-0 is the only accession among all Arabidopsis accessions for which sequence information is available in the 1001 genome database, with this version of the ZDRE motif.

The new ZDRE motif resides in the 5’-untranslated leader of LPCAT1. Binding of bZIP23 to this element therefore might physically block the transcription of the LPCAT1 gene under Zn deficient conditions. This is further supported by the repressive role for bZIP23 on the expression of LPCAT1 under Zn deficiency. Genomic sequence surveys screening for this new TF-binding site promise to further help identifying a complete list of genes potentially regulated by bZIP23 in order to fully understand the involvement of bZIP23 in the -Zn response in a genome-wide manner.

Based on our results, we propose that the sequence change in the 5’UTR sequence impacts gene(s) expression, and consequently causes variation in the associated traits. It has been proposed that evolution of species complexity from lower organisms to higher organisms is accompanied by an increase in the regulatory complexity of 5’UTRs (Liu et al., 2012). Nevertheless, so far little is known about the role of the 5’UTR sequence in the regulation of gene expression at the transcriptional level. The role of 5’UTR in the regulation of gene expression is perhaps best studied in human. Several studies showed that point substitutions in the 5'UTR change the expression of several genes such as Ankirin Repeat Domain 26 (Pippucci et al., 2011), Solute Carrier Family 2 Member 4 (Malodobra-Mazur et al., 2016), and Cyclin D1 (Berardi et al., 2003). In contrast, few examples exist on the role of 5’UTR as cis regulators in plants. In Arabidopsis, it has been shown that the regulation of NRP1 gene expression involves WRKY DNA binding proteins, which act on a potential cis-acting regulatory element located within the 5'UTR of NRP1 (Yu et al., 2001). More general, a large-scale study of DNA affinity purification sequencing, which is a high-throughput TF -binding site discovery method, has revealed a global preference across TF families for enrichment at promoters and 5’UTRs (O'Malley et al., 2016). Taken together, our study has uncovered a new example for the role of the 5’UTR in gene expression regulation and evolution in plants.

Of a particular interest is that our study revealed that this novel bZIP23-interacting sequence motif is subject to natural variation in A. thaliana (Figure 3), and its alteration may be associated with changes in the binding capacity of bZIP23. There are several ways that genetic variants can mechanistically contribute to plant adaptation. Many reported examples with regards to nutrient accumulation involve a change in the coding sequence of a gene that then alters the amino acid sequence of the encoded protein, thus leading to the disruption of gene function and a phenotypic change (Baxter et al., 2010; Chao et al., 2012; Chao et al., 2014). Reports on the role of specific regulatory element polymorphisms in the regulation of complex traits such as nutrient homeostasis crosstalk are less common, also because it is difficult to identify these relevant sequence changes. In our study, we demonstrated that allelic variation (SNPs) in the novel bZIP23 binding motif upstream of the LPCAT1 gene is associated with variation in LPCAT1 expression levels, which in turn results in variation in Pi accumulation in –Zn conditions. The LPCAT1 natural variants such as found in this study offer new inspiration for agronomical and biotechnological applications to optimize Pi use efficiency in plants.

While mutation of LPCAT1 results in altered Lyso-PC and PC concentrations; an altered Lyso-PC/PC ratio; the up-regulation of LPCAT1 in bzip23 mutant background has no significant effect on this ratio. The simplest explanation for this observation would be that in the bzip23 mutant background a portion of the synthesized PC is fed into the Kennedy pathway leading to the biosynthesis of different molecules such diacylglycerol or phosphatidic acid, and therefore no changes in Lyso-PC/PC could be detected (Wang et al., 2012). Nevertheless, an attractive second explanation exists: LPCAT1 could be subjected to a regulation at the protein level as a strategy to optimize phosphatidylcholine specie levels. In animals, it has been proposed that the LPCAT1 primary protein sequence may contain additional motifs, structural features, or interact with second messengers or ligands that can, under certain circumstances, alter its protein half-life (Zou et al., 2011). The precise mechanism that regulates LPCAT1 protein stability by the ubiquitin-proteasomal pathway was already shown (Zou et al., 2011). Further studies will be required to verify the presence of such regulation pathway for LPCAT1 in Arabidopsis, and if confirmed, such a mechanism would add another level of our understanding of LPCAT1 activity in plants.

Mutation of LPCAT1 results in increased PHT1;1 expression levels (Figure 7D); and ultimately an over-accumulation of Pi under Zn deficiency. The induction of the expression of genes encoding P uptake transporters under Zn deficiency has been reported in crop plants such as barley (Hordeum vulgare) (Huang et al., 2000); and the model plant Arabidopsis (Jain et al., 2013; Khan et al., 2014; Pal et al., 2017). Our study showed an induction of PHT1;1 in lpcat1 plants grown under Zn deficiency. The increase in PHT1;1 expression levels is likely to explain the increased shoot Pi concentration in lpcat1 since it is known that CaMV 35S promoter driven overexpression of this Pi transporter significantly increases shoot Pi concentration (Mitsukawa et al., 1997; Shin et al., 2004; Catarecha et al., 2007). Moreover, our finding provides evidence supporting a role for a Lyso-PC/PC-derived signal in regulating Pi homeostasis under –Zn. Until recently our knowledge on PL-derived signals in plants was scarce; however, physiological and molecular studies have shown that some PL classes could serve as precursors for the generation of diverse signalling molecules (Spector and Yorek, 1985; Testerink and Munnik, 2005). For instance, Lyso-PC was shown to act as a signal for the regulation of the expression of arbuscular mycorrhiza (AM)-specific Pi transporter genes in potato, tomato and recently in Lotus japonicus (Drissner et al., 2007; Vijayakumar et al., 2016). In addition to the involvement of individual PLs in specific physiological processes in plants (e.g ion transport), a broader importance of changes in Lyso-PC/PC ratio for the regulation of plant development and basic cell biology is emerging. For instance, in Arabidopsis alteration of the Lyso-PC/PC ratio shortens the time to flower (Nakamura et al., 2014). In human cells, the Lyso-PC/PC ratio was also associated with an impairment of cell function, signalling and metabolism (Mulder et al., 2003; Klavins et al., 2015). Our data now demonstrate a fundamental link between PL metabolism, particularly Lyso-PC/PC, and Pi accumulation in –Zn condition, and lays the foundation for exploring the role of Lyso-PC/PC-derived signal in controlling ion homeostasis and response to environmental changes not only in plant cells but also in other organisms.

Overall, our study sheds light on molecular mechanism underlying an old observation made as early as 1970 s, namely P-Zn interaction in plants (Warnock, 1970; Marschner and Schropp, 1977; Loneragan et al., 1979). By combining GWAS and functional genomics approaches, we discovered a complete pathway involved in the regulation of shoot Pi accumulation in –Zn that can be defined as bZIP23-LPCAT1(Lyso-PC/PC)-PHT1;1. Beyond its fundamental importance, our study could have a direct impact on plant growth in field by improving plant growth while reducing P supply, and will help meeting one of challenges facing agriculture in the 21st century.

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Author details

1. Mushtak Kisko

   BPMP, Univ Montpellier, CNRS, INRA, SupAgro, Montpellier, France

   Contribution

   Data curation, Formal analysis, Investigation, Methodology

   Competing interests

   No competing interests declared

2. Nadia Bouain

   BPMP, Univ Montpellier, CNRS, INRA, SupAgro, Montpellier, France

   Contribution

   Formal analysis, Investigation, Methodology

   For correspondence

   nadia.bouain@gmail.com

   Competing interests

   No competing interests declared

3. Alaeddine Safi

   BPMP, Univ Montpellier, CNRS, INRA, SupAgro, Montpellier, France

   Contribution

   Formal analysis, Methodology

   For correspondence

   alaeddine.safi@inra.fr

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-1532-5708

4. Anna Medici

   BPMP, Univ Montpellier, CNRS, INRA, SupAgro, Montpellier, France

   Contribution

   Formal analysis, Methodology

   For correspondence

   anna.medici@supagro.fr

   Competing interests

   No competing interests declared

5. Robert C Akkers

   Laboratory of Genetics, Wageningen University, Wageningen, Netherlands

   Contribution

   Resources, Formal analysis, Methodology, Writing—original draft

   For correspondence

   robert.akkers@wur.nl

   Competing interests

   No competing interests declared

6. David Secco

   BPMP, Univ Montpellier, CNRS, INRA, SupAgro, Montpellier, France

   Contribution

   Formal analysis, Investigation, Methodology

   For correspondence

   david.secco@gmail.com

   Competing interests

   No competing interests declared

7. Gilles Fouret

   Unité Mixte de Recherche, Montpellier, France

   Contribution

   Formal analysis, Methodology

   For correspondence

   fouret@supagro.inra.fr

   Competing interests

   No competing interests declared

8. Gabriel Krouk

   BPMP, Univ Montpellier, CNRS, INRA, SupAgro, Montpellier, France

   Contribution

   Formal analysis, Methodology

   For correspondence

   gkrouk@gmail.com

   Competing interests

   No competing interests declared

9. Mark GM Aarts

   Unité Mixte de Recherche, Montpellier, France

   Contribution

   Resources, Formal analysis, Funding acquisition, Writing—original draft

   For correspondence

   mark.aarts@wur.nl

   Competing interests

   No competing interests declared

10. Wolfgang Busch

    1. Gregor Mendel Institute, Austrian Academy of Sciences, Vienna Biocenter, Vienna, Austria
    2. Plant Molecular and Cellular Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States

    Contribution

    Resources, Formal analysis, Validation, Methodology, Writing—original draft

    For correspondence

    wbusch@salk.edu

    Competing interests

    No competing interests declared

11. Hatem Rouached

    BPMP, Univ Montpellier, CNRS, INRA, SupAgro, Montpellier, France

    Present address

    Department of Plant Biology, Carnegie Institution for Science, Stanford, United States

    Contribution

    Conceptualization, Resources, Formal analysis, Supervision, Funding acquisition, Validation, Writing—original draft, Project administration

    For correspondence

    hatem.rouached@supagro.inra.fr

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0002-7751-0477

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