The transcription factor PHR1 regulates lipid remodeling and triacylglycerol accumulation in Arabidopsis thaliana during phosphorus starvation

Pant, Bikram Datt; Burgos, Asdrúbal; Pant, Pooja; Cuadros-Inostroza, Álvaro; Willmitzer, Lothar; Scheible, Wolf‐Rüdiger

doi:10.1093/jxb/eru535

Cited by 138 publications

(136 citation statements)

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“…One of the major Pi suppliers is the membrane phospholipids, which are converted into galactolipids and sulfolipids when this nutrient is limited (Nakamura, 2013;Pant et al, 2015). Although the enzymes involved in the initial lipid degradation and the different pathways are well described, the processes involved in the recycling of subcomponents, and particularly the recycling of phospholipid polar heads, remains unknown.…”

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

“…Since most regulated genes that respond to Pi starvation are under the control of the Myb transcription factor PHR1 and its close homolog PHL1 Bustos et al, 2010;Thibaud et al, 2010;Pant et al, 2015;Sun et al, 2016), we examined the role of these factors in PPsPase1 and PECP1 induction, including MGD3 as a control. By comparing gene induction levels using RT-qPCR in the wild type and phr1 phl1 double mutants , we observed that only a residual induction remained for these three genes in phr1 phl1 (Fig.…”

Section: Ppspase1 and Pecp1 Are Dynamic Markers Of Pi Starvationmentioning

confidence: 99%

“…Indeed, in Arabidopsis, the in vivo role of these overexpressors seems more directly linked to the degradation of PCho and PEth polar heads, the by-products of phospholipid degradation triggered in response to Pi starvation. We have demonstrated that their induction is largely under the control of PHR1/PHL1, adding them to the list of proteins involved in lipid metabolism under the control of these transcription factors (Rouached et al, 2010;Pant et al, 2015).The superfamily of HAD phosphatases is a very large and divergent group of enzymes, with very little overall homology but great diversity in substrates (Burroughs et al, 2006). These phosphatases are subdivided into different classes based on the overall structural arrangement of their active core (Burroughs et al, 2006).…”

mentioning

confidence: 99%

“…Most of the systemically induced genes are under the control of PHR1 (a MYB family transcription factor) and its homolog PHL1 . Furthermore, their corresponding mutants exhibit altered gene induction and classical Pi starvation responses, including diminished effects on Pi content and lipid remobilization (Pant et al, 2015). Candidates for the systemic control of Pi starvation responses have been proposed, including substantial transport of mRNAs throughout the plant (as reviewed in Puga et al, 2017), and the direct sensing of Pi concentration (or Pi-containing metabolites) by SPX-type proteins (Wang et al, 2009;Puga et al, 2014;Wild et al, 2016).…”

mentioning

confidence: 99%

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The Phosphate Fast-Responsive Genes PECP1 and PPsPase1 Affect Phosphocholine and Phosphoethanolamine Content

et al. 2018

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Phosphate starvation-mediated induction of the HAD-type phosphatases PPsPase1 (AT1G73010) and PECP1 (AT1G17710) has been reported in Arabidopsis (Arabidopsis thaliana). However, little is known about their in vivo function or impact on plant responses to nutrient deficiency. The preferences of PPsPase1 and PECP1 for different substrates have been studied in vitro but require confirmation in planta. Here, we examined the in vivo function of both enzymes using a reverse genetics approach. We demonstrated that PPsPase1 and PECP1 affect plant phosphocholine and phosphoethanolamine content, but not the pyrophosphate-related phenotypes. These observations suggest that the enzymes play a similar role in planta related to the recycling of polar heads from membrane lipids that is triggered during phosphate starvation. Altering the expression of the genes encoding these enzymes had no effect on lipid composition, possibly due to compensation by other lipid recycling pathways triggered during phosphate starvation. Furthermore, our results indicated that PPsPase1 and PECP1 do not influence phosphate homeostasis, since the inactivation of these genes had no effect on phosphate content or on the induction of molecular markers related to phosphate starvation. A combination of transcriptomics and imaging analyses revealed that PPsPase1 and PECP1 display a highly dynamic expression pattern that closely mirrors the phosphate status. This temporal dynamism, combined with the wide range of induction levels, broad expression, and lack of a direct effect on Pi content and regulation, makes PPsPase1 and PECP1 useful molecular markers of the phosphate starvation response.Plant growth is highly sensitive to a lack of phosphate (Pi); hence, the application of Pi fertilizers has become standard practice for high-throughput crop production (Cordell et al., 2009). Most phosphorus in the soil is not available to plants, as it is combined with other minerals or parts of organic compounds (Bieleski, 1973;Raghothama and Karthikeyan, 2005). Only a small fraction of soluble Pi (usually present at a concentration of ,10 mM in the soil) can be taken up by plants.Although growth is not optimal under limiting conditions, plants can withstand changing Pi concentrations within heterogeneous soils or in the external nutrient supply that can lead to reprogramming of their metabolism and architecture (Hammond et al., 2003;Péret et al., 2011;Plaxton and Tran, 2011). Root architecture can be modified to facilitate Pi uptake by favoring the development of lateral roots (at the expense of primary root elongation in many plants including Arabidopsis), increasing the density and length of root hairs, and limiting the development of aerial parts (López-Bucio et al., 2002;Svistoonoff et al., 2007;Gruber et al., 2013). Pi uptake mechanisms are enhanced at the root/soil interface, particularly through the stimulation of Pi transport activity (Mudge et al., 2002;Shin et al., 2004;Nussaume et al., 2011; Ayadi et al., 2015). In parallel, mobilization of Pi sources fr...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Ppspase1 and Pecp1 Are Dynamic Markers Of Pi Starvationmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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The Phosphate Fast-Responsive Genes PECP1 and PPsPase1 Affect Phosphocholine and Phosphoethanolamine Content

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MYB‐like transcription factor NoPSR1 is crucial for membrane lipid remodeling under phosphate starvation in the oleaginous microalga Nannochloropsis oceanica

et al. 2020

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Edited by Ulf-Ingo Fl€ ugge Membrane lipid remodeling under phosphate (Pi) limitation, a process that replaces structural membrane phospholipids with nonphosphorus lipids, is a widely observed adaptive response in plants and algae. Here, we identified the transcription factor phosphorus starvation response 1 (NoPSR1) as an indispensable player for regulating membrane lipid conversion during Pi starvation in the microalga Nannochloropsis oceanica. Knocking out NoPSR1 scarcely perturbed membrane lipid composition under Pi-sufficient conditions but significantly impaired dynamic alteration in membrane lipids during Pi starvation. In contrast, the absence of NoPSR1 led to no obvious change in cell proliferation or storage lipid accumulation under either nutrient-sufficient or Pi-deficient conditions. Our results demonstrate a key factor controlling the membrane lipid profile during the Pi starvation response in N. oceanica.

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Sensing, signaLling, and CONTROL of phosphate starvation in plants: molecular players and applications

Scheible¹,

Rojas-Triana²

2015

Annual Plant Reviews Volume 48

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The transcription factor PHR1 regulates lipid remodeling and triacylglycerol accumulation in Arabidopsis thaliana during phosphorus starvation

Abstract: HighlightThis study reveals that the transcription factor PHR1 controls phospholipid/glycolipid substitution during P starvation, and that Arabidopsis accumulates triacylglycerol during P starvation. In roots this phenotype is also under control of PHR1.

Cited by 138 publications

References 71 publications

The Phosphate Fast-Responsive Genes PECP1 and PPsPase1 Affect Phosphocholine and Phosphoethanolamine Content

The Phosphate Fast-Responsive Genes PECP1 and PPsPase1 Affect Phosphocholine and Phosphoethanolamine Content

MYB‐like transcription factor NoPSR1 is crucial for membrane lipid remodeling under phosphate starvation in the oleaginous microalga Nannochloropsis oceanica

Sensing, signaLling, and CONTROL of phosphate starvation in plants: molecular players and applications

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