DORN1/P2K1 and purino-calcium signalling in plants: making waves with extracellular ATP

Abstract

Background and Aims Extracellular ATP governs a range of plant functions, including cell viability, adaptation and cross-kingdom interactions. Key functions of extracellular ATP in leaves and roots may involve an increase in cytosolic free calcium as a second messenger (‘calcium signature’). The main aim here was to determine to what extent leaf and root calcium responses require the DORN1/P2K1 extracellular ATP receptor in Arabidopsis thaliana. The second aim was to test whether extracellular ATP can generate a calcium wave in the root. Methods Leaf and root responses to extracellular ATP were reviewed for their possible links to calcium signalling and DORN1/P2K1. Leaves and roots of wild type and dorn1 plants were tested for cytosolic calcium increase in response to ATP, using aequorin. The spatial abundance of DORN1/P2K1 in the root was estimated using green fluorescent protein. Wild type roots expressing GCaMP3 were used to determine the spatial variation of cytosolic calcium increase in response to extracellular ATP. Key Results Leaf and root ATP-induced calcium signatures differed markedly. The leaf signature was only partially dependent on DORN1/P2K1, while the root signature was fully dependent. The distribution of DORN1/P2K1 in the root supports a key role in the generation of the apical calcium signature. Root apical and sub-apical calcium signatures may operate independently of each other but an apical calcium increase can drive a sub-apical increase, consistent with a calcium wave. Conclusion DORN1 could underpin several calcium-related responses but it may not be the only receptor for extracellular ATP in Arabidopsis. The root has the capacity for a calcium wave, triggered by extracellular ATP at the apex.

Overexpression of phosphatidylserine synthase IbPSS1 affords cellular Na+ homeostasis and salt tolerance by activating plasma membrane Na+/H+ antiport activity in sweet potato roots

“…The nonoverlapping emission spectra between DsRed and green fluorescence-based physiological analyses enable the widespread application of this system through fluorescence microscopy or confocal microscopy, such as imaging Na + accumulation by the use of CoroNa TM Green (this study; Figs. 2 d, 5 e, and 6a ) or recoding cytosolic Ca 2+ dynamics by the use of Ca 2+ fluorescent probes and genetically encoded Ca 2+ sensors (GCaMP3 and GCaMP6) 32 , 33 .…”

Annexin 1 Is a Component of eATP-Induced Cytosolic Calcium Elevation in Arabidopsis thaliana Roots

“…Extracellular ATP (eATP) is implicated as an apoplastic signal molecule in the abiotic and biotic stress responses of plants, their cellular viability, growth and stomatal regulation [ 1 , 2 , 3 , 4 , 5 , 6 ]. In Arabidopsis thaliana , eATP can act as a damage-associated molecular pattern (DAMP) and activates immunity signalling through the plasma membrane purinoreceptor AtDORN1 (Does Not Respond to Nucleotides1, also known as P2K1) [ 7 ].…”

“…eATP-dependent but AtDORN1-independent effects have also been reported [ 9 , 10 ], pointing to the presence of other perception mechanisms. eATP perception triggers increase in root and leaf free cytosolic Ca 2+ ([Ca 2+ ] cyt ) [ 5 ] that can lead to the production of reactive oxygen species (ROS) as further putative signalling agents [ 11 , 12 , 13 , 14 ]. Nitric oxide (NO) production can also be increased [ 2 , 15 , 16 ].…”

“…It is known that eATP-induced [Ca 2+ ] cyt increase in Arabidopsis roots requires plasma membrane Ca 2+ influx channels but the molecular identities of these channels remain unknown, as is also the case for other organs [ 9 , 11 , 14 , 21 , 22 , 23 ]. It has been hypothesized that the Arabidopsis annexin 1 protein (AtANN1) could be involved in mediating plasma membrane Ca 2+ influx [ 5 , 24 ] and recently AtANN4 was found to mediate eATP-induced [Ca 2+ ] cyt increase when expressed in Xenopus oocytes [ 25 ]. AtANN1 is thought to act as a plasma membrane Ca 2+ channel in the root [Ca 2+ ] cyt response to salinity stress, hyperosmotic stress, and oxidative stress [ 26 , 27 , 28 ].…”

New Insight into Plant Signaling: Extracellular ATP and Uncommon Nucleotides

“…This finding suggests new, P2K1-independent responses to eATP, involved among others in the root-bending mechanism [39]. Moreover DORN1 could underpin several calcium-related responses but it may not be the only receptor for eATP in Arabidopsis thaliana [40].…”