Introduction to a Virtual Special Issue on calcium signalling in plants

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Key words: electronic journal, not-for-profit, online journal, plant

science, print to online transition, scientific publishing.

Introduction to a VirtualSpecial Issue on calciumsignalling in plants

The complex roles played by Ca2+ in the regulation of amultitude of processes in eukaryotes and algae havebecome widely accepted and better understood over thepast two decades. A number of seminal studies extendingback half a century or more laid the foundation for thesemore detailed investigations though our understanding ofplant Ca2+ signalling progressed at a slower pace comparedwith the rapid advances in animal Ca2+ signalling researchin the 1980s and 1990s. This has been due, at least inpart, to the difficulties in measuring plant cytosolic Ca2+

concentrations. Notable early advances indicating roles forCa2+ as a regulator of cellular function in plants camefrom studies of ionic currents associated with morpho-genesis in fucoid algae (Robinson & Jaffe, 1973), andphytochrome responses in giant algae such as Nitella (e.g.Weisenseel & Ruppert, 1977). It was at least a decadelater that the first measurements of cytosolic Ca2+ weremade in plant and algal cells. Since then the field of Ca2+

signalling in plants has advanced rapidly on a number offronts (reviewed in Rudd & Franklin-Tong, 2001;McAinsh & Pittman, 2009). The development of modelsystems for studying Ca2+ signalling, such as the stomatalguard cell and the application of cell physiology to modelhigher plant cells (for example, De Silva et al., 1985;Brownlee, 1994), along with advances in moleculargenetic and genomics approaches are providing increas-ingly clearer pictures of both the similarities and

substantial differences between the ways animals, algaeand plants use Ca2+ to relay information within andbetween cells.

This Virtual Special Issue (VSI ) (www.newphytologist.com/virtualissues) presents a number of recent researcharticles and reviews that address some key features of signaltransduction (stimulus perception, generation of anddecoding information from Ca2+ signatures; and interac-tions with other signals and messengers) in plants and algae.The articles provide a snapshot of this rapidly advancingfield and point to requirements for future research.

Ca2+ and stimulus perception in bioticinteractions

Four articles bring new insights into the roles of cytosolicCa2+ in the perception of a range of biotic and abiotic stim-uli. Chabaud et al. (2011) made use of a nuclear encodedtransgenic ‘cameleon’ Ca2+ reporter to study the signallingbetween mycorrhizal fungi and the root cells that theyinfect. In comparing nuclear Ca2+ spiking patterns in rootcells of carrot and Medicago, they showed that contact withboth mycorrhizal hyphae and fungal spore exudate couldelicit spiking that involves a putative Ca2+-permeable cationchannel and a leucine-rich-receptor (LRR)-like kinase ascomponents of the signalling pathway. Ca2+ signalling haslong been known to be pivotal in the responses of legumi-nous root cells to nod factors produced by the symbioticRhizobium bacterium. Further insights into nodulationsignalling are to be found in a review by Capoen et al.(2010), which describes the roles of Ca2+ signatures in cellsof Medicago and semiaquatic plants such as Sesbania rostratain response to different infection strategies used by theinfecting bacterium. Rhizobium, in turn, has been shown torespond to diffusible flavonoid factors produced by legumi-nous plant roots. Moscatiello et al. (2010) shed new lighton the signalling processes in Rhizobium in this interactionby showing that flavonoids induce selective Ca2+ signals inthe Rhizobium cells, opening up a new perspective in ourunderstanding of this symbiotic interaction. Continuing thetheme of plant–microbial interactions, Ma & Berkowitz(2011) review the evidence that cyclic nucleotide-gated ionchannels underlie the elevation of cytosolic Ca2+ and thatthis leads to downstream generation of other messengerssuch as nitric oxide (NO) and activation of calmodulin(CaM), Ca2+-dependent protein kinases (CDPKs) andCa2+-activated transcription factors in the pathogenresponse signal transduction cascade.

Generation of Ca2+ signals and Ca2+

homeostasis

Ca2+ signalling requires that resting amounts of cellularCa2+ are maintained within very strictly defined limits. The

Papers included in this Virtual Special Issue are indicated by theircitations set in bold type (www.newphytologist.com/virtualissues)

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topic of Ca2+ homeostasis is given close attention in thisVSI with research articles and reviews covering the roles ofdifferent cellular compartments in the regulation of cyto-solic Ca2+. The role of chloroplasts in the regulation ofcytosolic Ca2+ is exemplified by Weinl et al. (2008), whoshow the requirement of a chloroplast Ca2+-sensing receptor(CAS) involved in Ca2+-regulated stomatal responses,providing new evidence that the chloroplast-localizedprotein plays a role in regulation of cytosolic Ca2+. The roleof the chloroplasts in regulating Ca2+ signalling is furtherdiscussed in a commentary by Webb (2008), which empha-sizes that recent findings ‘suggest that a totally novelpathway that is central to Ca2+ signalling in plants awaitsdiscovery’. Mitochondria, as well as chloroplasts play keyroles in cytosolic Ca2+ homeostasis and signalling. Scott &Logan (2008) showed that oxidative stress or heat shockinduced morphological changes in mitochondria (mito-chondrial morphology transition) – a necessary componentof the cell death pathway. This transition was shown to beaccompanied by altered Ca2+ homeostasis. Mazars et al.(2009) also consider Ca2+ homeostasis in a spatial contextfocusing on nuclear Ca2+. They present accumulating evi-dence that plant nuclei are able to generate Ca2+ signalsindependently of other cellular compartments and thatthese may also regulate biochemical activity and geneexpression. A comprehensive review by McAinsh &Pittman (2009) discusses the various pathways by whichthe spatiotemporal patterns of cytosolic Ca2+ elevationsmay provide signatures that may encode specificity in sig-nalling processes. This review emphasizes the complexity ofCa2+ signalling pathways, the multiple origins of Ca2+

elevations and the roles of Ca2+ channels and efflux trans-porters in bringing about different patterns of Ca2+

elevation in cellular Ca2+.

The expanding roles of Ca2+ channels

In recent years, substantial progress has been made inunderstanding the roles of Ca2+ channels in signalling andCa2+ uptake. A number of reports, combining cell physiol-ogy, molecular biology and genomics, exemplify some ofthe key findings in this field. A key emerging feature ofplant Ca2+ signalling is that distinct types of Ca2+ channels,defined by their physiological attributes, differ markedlyfrom certain canonical animal-type Ca2+ channels.Moreover, a number of channel types that are widespreadamongst other eukaryotes, including many algae, appear tobe absent from the genomes of higher plants and mosses(embryophytes). These include the four-domain voltage-dependent Ca2+ channels and the InsP3 (inositol 1,4,5trisphosphate) receptors (Verret et al., 2010).

Genomic studies also reveal expansion of particular chan-nel gene families in embryophytes, most notably the cyclicnucleotide-gated channels (CNGCs) and the glutamate

receptor-like channels (GLRs). This is mirrored in severalarticles in the VSI that describe the roles of CNGCs in anumber of processes. Ma & Berkowitz (2011) review evi-dence for interactions between CNGCs and otherdownstream signalling components, including NO, CaM,CDPKs and CaM-binding transcription factors in pathogendefence signal transduction cascades. A study byChaiwongsar et al. (2009) using Arabidopsis mutantsdefective in CNGC2, showed that they have reduced fertil-ity, which was ascribed to reduced pollen tube growth inhigh-Ca2+ environments. The complexity of signallinginvolving channel-mediated Ca2+ fluxes in pollen tubegrowth is exemplified by two further reports. The occur-rence of hyperpolarization-activated Ca2+ channels in thepollen tube apex is described by Qu et al. (2007), whileWu et al. (2007) provide evidence that signal transductionvia a heterotrimeric G-protein is mediated via hyperpolar-ization-activated Ca2+-permeable channels (HACCs) inpollen. Physiological evidence also supports the roles ofCa2+-permeable channels that are activated by membranepotential depolarization (depolarization-activated calciumchannels, DACCs) (White, 2009) and patch clamp experi-ments with Arabidopsis root hairs reveals the coexistence ofboth HACCs and DACCs in the same cell (Miedemaet al., 2008). How the activities of these channel types arecoordinated and their precise roles in the generation ormodulation of Ca2+ signals remain to be determined.Physiological studies also point to widespread roles of non-selective cation channels in mediating Ca2+ influx into thecytosol (Demidchik & Maathuis, 2007). A possible role ofthe multifunctional membrane-binding proteins of theannexin family in Ca2+ signalling is explored by Laohavisit& Davies (2011). In this review the authors present theinteresting hypothesis that certain annexins may be respon-sible for the reactive oxygen-stimulated Ca2+ conductancein root hairs and other plant cell types.

Decoding and interactions with other signals

One of the least understood aspects of Ca2+ signalling ishow spatiotemporal changes in the concentrations of Ca2+

in different cellular compartments can be translated intospecific, often complex adaptive and developmentalresponses that involve a host of other signal transductionnetworks. A number of reviews and articles address thisissue. One of the best studied decoding networks is the cal-cineurin-B-like (CBL)-interacting kinases (CIPKs)pathway, which is given a thorough and comprehensivetreatment in a review by Weinl & Kudla (2009), present-ing novel aspects relating to the evolution of Ca2+ signallingin plants. A similarly comprehensive review of nuclear pro-tein kinases (Dahan et al., 2010) presents the hypothesisthat these key regulatory proteins play pivotal roles indecoding nuclear Ca2+ signals.

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The interaction of Ca2+ with other messengers, includingNO, in the regulation of extracellular Ca2+ fluxes and actinorganization in Pinus pollen tubes (Wang et al., 2009) andthe involvement of VILLIN4 in regulation of actin in aCa2+-dependent manner in root hairs (Zhang et al., 2011)further exemplify the complexity of interactions of Ca2+

signals with other messengers. An important, albeit indi-rect, link between Ca2+ signalling, NO and external ATPsignalling was demonstrated by Sueldo et al. (2010),showing that exogenous ATP induced formation of the sig-nalling lipid phosphatidic acid in suspension culturedtomato cells which involved the action of phospholipases Dand C and Ca2+ influx. A direct activation of Ca2+ channelsby ethylene is suggested by an electrophysiological study byZhao et al. (2007). Finally, the involvement of Ca2+-CaMoxidative stress signalling with roles both upstream anddownstream of H2O2 production was suggested to play akey role in ABA-induced antioxidant defence (Hu et al.,2007).

Conclusions

The field of Ca2+ signalling research is developing fast. Weare discovering that the complexity of Ca2+ signalling net-works, their multiple interactions with other signallingpathways and unexpected features of the components ofthese networks reflect the close integration of environmentalperception and metabolic and developmental control inplants and algae. The evolutionary drivers that underliesome of the startling differences between plant, algal andanimal Ca2+ signalling components remain to be fullyexplored.

Colin Brownlee and Alistair Hetherington

Editors, New [email protected]

[email protected]

References

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Capoen W, Oldroyd G, Goormachtig S, Holsters M. 2010. Sesbaniarostrata: a case study of natural variation in legume nodulation. NewPhytologist 186: 340–345.

Chabaud M, Genre A, Sieberer BJ, Faccio A, Fournier J, Novero M,

Barker DG, Bonfante P. 2011. Arbuscular mycorrhizal hyphopodia and

germinated spore exudates trigger Ca2+ spiking in the legume and

nonlegume root epidermis. New Phytologist 189: 347–355.

Chaiwongsar S, Strohm AK, Roe JR, Godiwalla RY, Chan CWM. 2009.

A cyclic nucleotide-gated channel is necessary for optimum fertility in

high calcium environments. New Phytologist 183: 76–87.

Dahan J, Wendehenne D, Ranjeva R, Pugin A, Bourque S. 2010. Nuclear

protein kinases: still enigmatic components in plant cell signalling. NewPhytologist 185: 355–368.

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Qu H-Y, Shang Z-L, Zhang S-L, Liu L-M, Wu J-Y. 2007. Identification

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modulation of a plasmamembrane hyperpolarization-activated Ca2+-

permeable channel. New Phytologist 176: 550–559.

Zhang Y, Xiao Y, Du F, Cao L, Dong H, Ren H. 2011. ArabidopsisVILLIN4 is involved in root hair growth through regulating actin

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Key words: biotic and abiotic interactions, calcium, CDPK, channels,

decoding, homeostasis, nodulation signalling, signalling.

Commentary

Wetlands and the globalcarbon cycle: what mightthe simulated past tell usabout the future?

Wetlands play an important role in the global carbon (C)cycle. Flooded or saturated conditions in these ecosystemslimit the availability of oxygen to soil microbes and decom-position of organic matter proceeds slowly under the water-logged conditions (Megonigal et al., 2004). As a result ofslow rates of anaerobic decomposition, wetlands haveaccumulated c. 500 Pg of C in their soils globally (approxi-mately one-third of the terrestrial soil C), with the majorityof this C stored in peatland soils, which are characterized by> 40 cm of surface organic matter (Bridgham et al., 2006).Anaerobic soil conditions also result in the production ofmethane (CH4) by methanogenic microbes, and wetlandsare responsible for 15% to 40% of current global CH4

emissions (Denman et al., 2007). Given that CH4 is apotent glasshouse gas with 25-times the global warmingpotential of CO2 (Forster et al., 2007), changes in wetlandCH4 emissions can have important implications for the glo-bal climate. Indeed, modeling approaches have linkedwetland CH4 fluxes to past changes in climate (e.g.Loulergue et al., 2011), and a great deal of current researchis exploring how wetland CH4 dynamics will respond tofuture global changes, including increases in atmospheric[CO2] (summarized in van Groenigen et al., 2011). Recentwork by Boardman et al., in this issue of New Phytologist(pp. 898–911), adds an exciting new perspective to thisimportant research area by experimentally demonstratingfor the first time that lower atmospheric [CO2] during theLast Glacial Maximum (LGM) could suppress CH4 fluxfrom some wetlands. Their results help provide a potentialexplanation for the lower atmospheric [CH4] observedduring glacial maxima; moreover, these findings have

implications for our understanding of current and futurewetland CH4 dynamics.

‘… the response of wetland CH4 dynamics to global

change is not straightforward …’

In contrast to most terrestrial ecosystems where decompo-sition of organic matter can be carried out by a singlemicroorganism using oxygen as a terminal electron acceptorfor respiration, decomposition in anaerobic wetland envi-ronments relies on a number of complementary andcompeting microbial processes (Megonigal et al., 2004;Fig. 1). As in upland ecosystems, biopolymers (e.g. plantdetritus) are initially hydrolyzed by exoenzymes to simplermonomers. In wetlands, however, these monomers are sub-sequently broken down through a series of sequentialfermentation reactions that ultimately generate low molecu-lar weight alcohols, fatty acids (including acetate), H2 andCO2. Methanogens are able to use these fermentation endproducts – primarily acetate, H2 and CO2 – to produceCH4. However, the C sources that fuel methanogens canalso be used by a number of competing microbial processesthat use a variety of terminal electron acceptors (TEAs),including: nitrate ions (NO3

)), manganese(III, IV), iron(III),oxidized humic substances, and sulfate ions (SO4

2)) tocomplete respiration. These alternative TEAs are moreenergetically favorable than methanogenesis and can sup-press the production of CH4 in many wetland ecosystems.Following methanogenesis, CH4 can leave the systemthrough a combination of ebullition (bubble formation),diffusion across the water–air interface and flux throughemergent vegetation. CH4 lost via diffusion is subject to oxi-dation to CO2 by methanotrophic bacteria using oxygen (orperhaps other TEAs), while CH4 lost via ebullition andthrough plants largely bypasses this methanotrophic activity.Thus, the controls on CH4 emission from wetlands are

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Introduction to a Virtual Special Issue on calcium signalling in plants