Nadia Bouain

Phosphate and zinc transport and signalling in plants: toward a better understanding of their homeostasis interaction

Inorganic phosphate (Pi) and zinc (Zn) are two essential nutrients for plant growth. In soils, these two minerals are either present in low amounts or are poorly available to plants. Consequently, worldwide agriculture has become dependent on external sources of Pi and Zn fertilizers to increase crop yields. However, this strategy is neither economically nor ecologically sustainable in the long term, particularly for Pi, which is a non-renewable resource. To date, research has emphasized the analysis of mineral nutrition considering each nutrient individually, and showed that Pi and Zn homeostasis is highly regulated in a complex process. Interestingly, numerous observations point to an unexpected interconnection between the homeostasis of the two nutrients. Nevertheless, despite their fundamental importance, the molecular bases and biological significance of these interactions remain largely unknown. Such interconnections can account for shortcomings of current agronomic models that typically focus on improving the assimilation of individual elements. Here, current knowledge on the regulation of the transport and signalling of Pi and Zn individually is reviewed, and then insights are provided on the recent progress made towards a better understanding of the Zn-Pi homeostasis interaction in plants.

Recent Advances in Understanding the Molecular Mechanisms Regulating the Root System Response to Phosphate Deficiency in Arabidopsis.

Phosphorus (P) is an essential macronutrient for plant growth and development. Inorganic phosphate (Pi) is the major form of P taken up from the soil by plant roots. It is well established that under Pi deficiency condition, plant roots undergo striking morphological changes; mainly a reduction in primary root length while increase in lateral root length as well as root hair length and density. This typical phenotypic change reflects complex interactions with other nutrients such as iron, and involves the activity of a large spectrum of plant hormones. Although, several key proteins involved in the regulation of root growth under Pi-deficiency have been identified in Arabidopsis, how plants adapt roots system architecture in response to Pi availability remains an open question. In the current post-genomic era, state of the art technologies like high-throughput phenotyping and sequencing platforms,“omics” methods, together with the widespread use of system biology and genome-wide association studies will help to elucidate the genetic architectures of root growth on different Pi regimes. It is clear that the large-scale characterization of molecular systems will improve our understanding of nutrient stress phenotype and biology. Herein, we summarize the recent advances and future directions towards a better understanding of Arabidopsis root developmental programs functional under Pi deficiency. Such a progress is necessary to devise strategies to improve the Pi use efficiency in plants that is an important issue for agriculture.

Phosphate, phytate and phytases in plants: from fundamental knowledge gained in Arabidopsis to potential biotechnological applications in wheat

Abstract Phosphorus (P) is an essential macronutrient for all living organisms. In plants, P is taken up from the rhizosphere by the roots mainly as inorganic phosphate (Pi), which is required in large and sufficient quantities to maximize crop yields. In today’s agricultural society, crop yield is mostly ensured by the excessive use of Pi fertilizers, a costly practice neither eco-friendly or sustainable. Therefore, generating plants with improved P use efficiency (PUE) is of major interest. Among the various strategies employed to date, attempts to engineer genetically modified crops with improved capacity to utilize phytate (PA), the largest soil P form and unfortunately not taken up by plants, remains a key challenge. To meet these challenges, we need a better understanding of the mechanisms regulating Pi sensing, signaling, transport and storage in plants. In this review, we summarize the current knowledge on these aspects, which are mainly gained from investigations conducted in Arabidopsis thaliana, and we extended it to those available on an economically important crop, wheat. Strategies to enhance the PA use, through the use of bacterial or fungal phytases and other attempts of reducing seed PA levels, are also discussed. We critically review these data in terms of their potential for use as a technology for genetic manipulation of PUE in wheat, which would be both economically and environmentally beneficial.

The Involvement of OsPHO1;1 in the Regulation of Iron Transport Through Integration of Phosphate and Zinc Deficiency Signaling

Plants survival depends on their ability to cope with multiple nutrient stresses that often occur simultaneously, such as the limited availability of essential elements inorganic phosphate (Pi), zinc (Zn), and iron (Fe). Previous research has provided information on the genes involved in efforts by plants to maintain homeostasis when a single nutrient (Pi, Zn, or Fe) is depleted. Recent findings on nutritional stress suggest that plant growth capacity is influenced by a complex tripartite interaction between Pi, Zn, and Fe homeostasis. However, despite its importance, how plants integrate multiple nutritional stimuli into complex developmental programs, and which genes are involved in this tripartite (Pi ZnFe) interaction is still not clear. The aim of this study was to examine the physiological and molecular responses of rice (Oriza sativa L.) to a combination of Pi, Zn, and/or Fe deficiency stress conditions. Results showed that Fe deficiency had the most drastic single-nutrient effect on biomass, while the Zn deficiency-effect depended on the presence of Pi in the medium. Interestingly, the observed negative effect of Fe starvation was alleviated by concomitant Pi or PiZn depletion. Members of the OsPHO1 family showed a differential transcriptional regulation in response PiZnFe combinatory stress conditions. Particularly, the transcripts of the OsPHO1;1 sense and its natural antisense cis-NatPHO1;1 showed the highest accumulation under PiZn deficiency. In this condition, the Ospho1;1 mutants showed over-accumulation of Fe in roots compared to wild type plants. These data reveal coordination between pathways involved in Fe transport and PiZn signaling in rice which involves the OsPHO1; 1, and support the hypothesis of a genetic basis for Pi, Zn, and Fe signaling interactions in plants.

Over-expression of the Bacterial Phytase US417 in Arabidopsis Reduces the Concentration of Phytic Acid and Reveals Its Involvement in the Regulation of Sulfate and Phosphate Homeostasis and Signaling

Phytic acid (PA) is the main phosphorus storage form in plant seeds. It is recognized as an anti-nutrient for humans and non-ruminant animals, as well as one of the major sources of phosphorus that contributes to eutrophication. Therefore, engineering plants with low PA content without affecting plant growth capacity has become a major focus in plant breeding. Nevertheless, lack of knowledge on the role of PA seed reserves in regulating plant growth and in maintaining ion homeostasis hinders such an agronomical application. In this context, we report here that the over-expression of the bacterial phytase PHY-US417 in Arabidopsis leads to a significant decrease in seed PA, without any effect on the seed germination potential. Interestingly, this over-expression also induced a higher remobilization of free iron during germination. Moreover, the PHY-over-expressor lines show an increase in inorganic phosphate and sulfate contents, and a higher biomass production after phosphate starvation. Finally, phosphate sensing was altered because of the changes in the expression of genes induced by phosphate starvation or involved in phosphate or sulfate transport. Together, these results show that the over-expression of PHY-US417 reduces PA concentration, and provide the first evidence for the involvement of PA in the regulation of sulfate and phosphate homeostasis and signaling.

Phosphate/Zinc Interaction Analysis in Two Lettuce Varieties Reveals Contrasting Effects on Biomass, Photosynthesis, and Dynamics of Pi Transport

Inorganic phosphate (Pi) and Zinc (Zn) are essential nutrients for normal plant growth. Interaction between these elements has been observed in many crop plants. Despite its agronomic importance, the biological significance and genetic basis of this interaction remain largely unknown. Here we examined the Pi/Zn interaction in two lettuce (Lactuca sativa) varieties, namely, “Paris Island Cos” and “Kordaat.” The effects of variation in Pi and Zn supply were assessed on biomass and photosynthesis for each variety. Paris Island Cos displayed better growth and photosynthesis compared to Kordaat under all the conditions tested. Correlation analysis was performed to determine the interconnectivity between Pi and Zn intracellular contents in both varieties. Paris Island Cos showed a strong negative correlation between the accumulation levels of Pi and Zn in shoots and roots. However, no relation was observed for Kordaat. The increase of Zn concentration in the medium causes a decrease in dynamics of Pi transport in Paris Island Cos, but not in Kordaat plants. Taken together, results revealed a contrasting behavior between the two lettuce varieties in terms of the coregulation of Pi and Zn homeostasis and provided evidence in favor of a genetic basis for the interconnection of these two elements.

Phosphorus and Iron Deficiencies Influences Rice Shoot Growth in an Oxygen Dependent Manner: Insight from Upland and Lowland Rice

Rice is the main staple crop for one-third of the world population. To maximize yields, large quantities and constant input of fertilizers containing essential nutrients such as phosphorus (P) and iron (Fe) are added. Rice can germinate in both aerobic and anaerobic conditions, but the crosstalk between oxygen (O2) and nutrients such as P and Fe on plant growth remains obscure. The aim of this work was to test whether such interactions exist, and, if so, if they are conserved between up- and lowland rice varieties. To do so, we assessed shoot and root biomass as well as inorganic phosphate (Pi) accumulation in four rice varieties, including two lowland rice varieties Nipponbare and Suphanburi 1 (SPR1) (adapted to non-aerated condition) and two upland rice varieties CMU122 and Sew Mae Jun (SMJ) (adapted to aerated condition) under various conditions of Pi and/or Fe deficiencies, in aerated and non-areated solution. Under these different experimental conditions, our results revealed that the altered shoot biomass in Nipponbare and SPR1 was O2-dependent but to a lesser extent in CMU122 and SMJ cultivars. In this perspective, discovering the biological significance and molecular basis of these mineral elements and O2 signal interaction is needed to fully appreciate the performance of plants to multiple environmental changes.

LPCAT1 controls phosphate homeostasis in a zinc-dependent manner

All living organisms require a variety of essential elements for their basic biological functions. While the homeostasis of nutrients is highly intertwined, the molecular and genetic mechanisms of these dependencies remain poorly understood. Here, we report a discovery of a molecular pathway that controls phosphate (Pi) accumulation in plants under Zn deficiency. Using genome-wide association studies, we first identified allelic variation of the Lyso-PhosphatidylCholine (PC) AcylTransferase 1 (LPCAT1) gene as the key determinant of shoot Pi accumulation under Zn deficiency. We then show that regulatory variation at the LPCAT1 locus contributes significantly to this natural variation and we further demonstrate that the regulation of LPCAT1 expression involves bZIP23 TF, for which we identified a new binding site sequence. Finally, we show that in Zn deficient conditions loss of function of LPCAT1 increases the phospholipid Lyso-PhosphatidylCholine/PhosphatidylCholine ratio, the expression of the Pi transporter PHT1;1, and that this leads to shoot Pi accumulation.

Individual versus Combinatorial Effects of Silicon, Phosphate, and Iron Deficiency on the Growth of Lowland and Upland Rice Varieties

Mineral nutrient homeostasis is essential for plant growth and development. Recent research has demonstrated that the occurrence of interactions among the mechanisms regulating the homeostasis of different nutrients in plants is a general rule rather than an exception. Therefore, it is important to understand how plants regulate the homeostasis of these elements and how multiple mineral nutrient signals are wired to influence plant growth. Silicon (Si) is not directly involved in plant metabolism but it is an essential element for a high and sustainable production of crops, especially rice, because of its high content in the total shoot dry weight. Although some mechanisms underlying the role of Si in plants responses to both abiotic and biotic stresses have been proposed, the involvement of Si in regulating plant growth in conditions where the availability of essential macro- and micronutrients changes remains poorly investigated. In this study, the existence of an interaction between Si, phosphate (Pi), and iron (Fe) availability was examined in lowland (Suphanburi 1, SPR1) and upland (Kum Hom Chiang Mai University, KH CMU) rice varieties. The effect of Si and/or Fe deficiency on plant growth, Pi accumulation, Pi transporter expression (OsPHO1;2), and Pi root-to-shoot translocation in these two rice varieties grown under individual or combinatorial nutrient stress conditions were determined. The phenotypic, physiological, and molecular data of this study revealed an interesting tripartite Pi-Fe-Si homeostasis interaction that influences plant growth in contrasting manners in the two rice varieties. These results not only reveal the involvement of Si in modulating rice growth through an interaction with essential micro- and macronutrients, but, more importantly, they opens new research avenues to uncover the molecular basis of Pi-Fe-Si signaling crosstalk in plants.

Natural allelic variation of the AZI1 gene controls root growth under zinc-limiting condition

Zinc is an essential micronutrient for all living organisms and is involved in a plethora of processes including growth and development, and immunity. However, it is unknown if there is a common genetic and molecular basis underlying multiple facets of zinc function. Here we used natural variation in Arabidopsis thaliana to study the role of zinc in regulating growth. We identify allelic variation of the systemic immunity gene AZI1 as a key for determining root growth responses to low zinc conditions. We further demonstrate that this gene is important for modulating primary root length depending on the zinc and defence status. Finally, we show that the interaction of the immunity signal azelaic acid and zinc level to regulate root growth is conserved in rice. This work demonstrates that there is a common genetic and molecular basis for multiple zinc dependent processes and that nutrient cues can determine the balance of growth and immune responses in plants.