A Role for Inositol Pyrophosphates in the Metabolic Adaptations to Low Phosphate in Arabidopsis

Abstract

Phosphate is a major plant macronutrient and low phosphate availability severely limits global crop productivity. In Arabidopsis, a key regulator of the transcriptional response to low phosphate, phosphate starvation response 1 (PHR1), is modulated by a class of signaling molecules called inositol pyrophosphates (PP-InsPs). Two closely related diphosphoinositol pentakisphosphate enzymes (AtVIP1 and AtVIP2) are responsible for the synthesis and turnover of InsP8, the most implicated molecule. This study is focused on characterizing Arabidopsis vip1/vip2 double mutants and their response to low phosphate. We present evidence that both local and systemic responses to phosphate limitation are dampened in the vip1/vip2 mutants as compared to wild-type plants. Specifically, we demonstrate that under Pi-limiting conditions, the vip1/vip2 mutants have shorter root hairs and lateral roots, less accumulation of anthocyanin and less accumulation of sulfolipids and galactolipids. However, phosphate starvation response (PSR) gene expression is unaffected. Interestingly, many of these phenotypes are opposite to those exhibited by other mutants with defects in the PP-InsP synthesis pathway. Our results provide insight on the nexus between inositol phosphates and pyrophosphates involved in complex regulatory mechanisms underpinning phosphate homeostasis in plants.

Translational approach to increase phosphate accumulation in two plant species through perturbance of inositol pyrophosphates

“…This increase in P i accumulation in severe DDP1 OX lines was also significantly higher than P i accumulation in ipk1 mutants (Figure 5a). This is notable as past studies demonstrate ipk1 mutants accumulate significantly higher P i compared to WT (Stevenson-Paulik et al ., 2005; Kuo et al ., 2014; Kuo et al ., 2018; Land et al ., 2021). Under our conditions, ipk1 mutants had higher P i from WT only after 4 weeks of growth whereas all other ipk1 timepoints showed no statistical difference in P i accumulation (Figure 5a).…”

“…PP-InsP signaling in plants has become an increased area of interest due to emerging evidence connecting the role of PP-InsPs to P i sensing and other hormone signaling pathways (Laha et al ., 2015; Kuo et al ., 2018; Adepoju et al ., 2019; Laha et al ., 2019; Zhu et al ., 2019; Laha et al ., 2020; Land et al ., 2021). In this work, we sought to use a synthetic biology approach to manipulate PP- InsPs in transgenic plants to study the long-term consequences of decreased PP-InsPs, and to evaluate the preliminary translational potential of depleting PP-InsPs in planta .…”

“…The role of PP-InsPs as critical players in eukaryotic Pi sensing and homeostasis has been facilitated by examination of loss-of-function mutants in the InsP and PP-InsP synthesis pathways (Zhu et al, 2019;Dong et al, 2019;Land et al, 2021). Specifically, depleting InsP 8 in vivo leads to alterations in a plant's ability to properly sense and respond to Pi (Zhu et al, 2019;Dong et al, 2019;Land et al, 2021). Arabidopsis loss-of-function mutants for both InsP 8 synthetic enzymes VIP1 and VIP2 (Desai et al, 2014;Freed et al, 2020), which are also referred to as VIH2 and VIH1 (Zhu et al 2019), have depleted levels of PP-InsPs, as well as altered physiological responses to Pi which include increased Pi accumulation, PSR gene induction, and impacted growth (Zhu et al, 2019;Dong et al, 2019).…”

“…The role of PP-InsPs as critical players in eukaryotic P i sensing and homeostasis has been facilitated by examination of loss-of-function mutants in the InsP and PP-InsP synthesis pathways (Zhu et al ., 2019; Dong et al ., 2019; Land et al ., 2021). Specifically, depleting InsP 8 in vivo leads to alterations in a plant’s ability to properly sense and respond to P i (Zhu et al ., 2019; Dong et al ., 2019; Land et al ., 2021).…”

Prospects of Genetics and Breeding for Low Phosphate Tolerance: an Integrated Approach from Soil to Cell

“…Interestingly, Arabidopsis Atipk1 and Atitpk1 mutants which are defective in the synthesis of IP 5 and IP 6 are also altered in Pi homeostasis (Kuo et al 2018), suggesting that speci c species of IP might play a speci c role in the regulation of plant Pi homeostasis and that it is not solely controlled by IP 8 . In support of this notion, a recent report of novel alleles of Atvih1 and Atvih2 double mutants showed that IP 8 levels are downregulated in these mutants, however, the expression of AtPHR1 targets remains responsive to Pi deprivation (Land et al 2021). Because IP 6 , IP 7 and IP 8 can bind the SPX domain (Wild et al 2016), further in planta studies on the speci c roles of IPs individual species are required.…”