CHOLINE TRANSPORTER-LIKE1 is required for sieve plate development to mediate long-distance cell-to-cell communication

Dettmer, Jan; Ursache, Robertas; Campilho, Ana; Miyashima, Shunsuke; Belevich, Ilya; O’Regan, S; Mullendore, Daniel L.; Yadav, Shri Ram; Lanz, Christa; Beverina, Luca; Papagni, Antonio; Schneeberger, Korbinian; Weigel, Detlef; Stierhof, York‐Dieter; Moritz, Thomas; Knoblauch, Michael; Jokitalo, Eija; Helariutta, Yrjö

doi:10.1038/ncomms5276

Cited by 74 publications

(100 citation statements)

References 69 publications

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“…Furthermore, recent work has demonstrated that impairing choline transport, by CHER1 choline transporter inactivation, has an impact on the development of the root vasculature and plasmodesmata in particular (Dettmer et al, 2014;Kraner et al, 2017). In light of the absence of strong architectural alterations and lipid modifications caused by the greatly diminished PCho concentration in our plant lines, the CHER1 mutant phenotype is more likely linked to choline or PtdCho imbalance rather than to lower PCho content (Kraner et al, 2017).…”

Section: Discussionmentioning

confidence: 89%

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: 89%

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

et al. 2018

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“…and Cho (Jost et al, 2009). NMT1 expression is known to be sensitive to feedback inhibition leaves (Dettmer et al, 2014;Kraner et al, 2017). Choline has also long been known to be 582 present in xylem sap (Maizel et al, 1956;Martin et al, 1983).…”

mentioning

confidence: 99%

NMT1 and NMT3 N-Methyltransferase Activity Is Critical to Lipid Homeostasis, Morphogenesis, and Reproduction

et al. 2018

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54Phosphatidylcholine (PC) is a major membrane phospholipid and a precursor for most 55 signalling molecules. Understanding its synthesis is important for improving plant growth, 56 nutritional value and resistance to stress. PC synthesis is complex, involving several 57 interconnected pathways, one of which proceeds from serine-derived phosphoethanolamine 58(PEA) to form phosphocholine (PCho) through three sequential phospho-base methylations 59 catalysed by phosphoethanolamine N-methyltransferases (PEAMTs). The contribution of 60 this pathway to the production of PC and plant growth has been a matter of some debate.

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“…The work in Helariutta lab carefully dissects the mechanisms underlying the formation of sieve pores and the regulation of plasmodesmata aiming to identify opportunities to engineer long distance signaling. Characterization of proteins, such as the putative choline transporter CHER1 [63], involved in the transition from plasmodesmata to mature sieve pores is combined with genetic analysis of plasmodesmata regulation. Identification of mutants activated in callose biosynthesis (via callose synthase 3, CALS3) indicates the importance of this pathway not only for plasmodesmata but also in vascular transport [64].…”

Section: Intercellular Channelsmentioning

confidence: 99%

“…The exocyst tethering complex is very recently and surprisingly implicated, not only in exocytosis, but also autophagy in both animals and plants [45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68]. Previous indication of exocyst engagement in the autophagy initiation in animals and multiplicity of EXO70 paralogs in land plants both imply a possible role for the exocyst complex as a coordinator contributing to the endomembrane dynamics.…”

Section: Unconventional Role Of Proteins Normally Functioning In Cmentioning

confidence: 99%

Unconventional Transport Routes of Soluble and Membrane Proteins and Their Role in Developmental Biology

Pompa

Marchis

Pallotta

et al. 2017

IJMS

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Many proteins and cargoes in eukaryotic cells are secreted through the conventional secretory pathway that brings proteins and membranes from the endoplasmic reticulum to the plasma membrane, passing through various cell compartments, and then the extracellular space. The recent identification of an increasing number of leaderless secreted proteins bypassing the Golgi apparatus unveiled the existence of alternative protein secretion pathways. Moreover, other unconventional routes for secretion of soluble or transmembrane proteins with initial endoplasmic reticulum localization were identified. Furthermore, other proteins normally functioning in conventional membrane traffic or in the biogenesis of unique plant/fungi organelles or in plasmodesmata transport seem to be involved in unconventional secretory pathways. These alternative pathways are functionally related to biotic stress and development, and are becoming more and more important in cell biology studies in yeast, mammalian cells and in plants. The city of Lecce hosted specialists working on mammals, plants and microorganisms for the inaugural meeting on “Unconventional Protein and Membrane Traffic” (UPMT) during 4–7 October 2016. The main aim of the meeting was to include the highest number of topics, summarized in this report, related to the unconventional transport routes of protein and membranes.

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CHOLINE TRANSPORTER-LIKE1 is required for sieve plate development to mediate long-distance cell-to-cell communication

Cited by 74 publications

References 69 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

NMT1 and NMT3 N-Methyltransferase Activity Is Critical to Lipid Homeostasis, Morphogenesis, and Reproduction

Unconventional Transport Routes of Soluble and Membrane Proteins and Their Role in Developmental Biology

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