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Available online at www.sciencedirect.com Cellular programs for arbuscular mycorrhizal symbiosis Maria J Harrison In arbuscular mycorrhizal (AM) symbiosis, AM fungi colonize root cortical cells to obtain carbon from the plant, while assisting the plant with the acquisition of mineral nutrients from the soil. Within the root cells, the fungal hyphae inhabit membrane-bound compartments that the plant establishes to accommodate the fungal symbiont. Recent data provide new insights into the events associated with development of the symbiosis including signaling for the formation of a cellular apparatus that guides hyphal growth through the cell. Plant genes that play key roles in a cellular program for the accommodation of microbial symbionts have been identified. In the inner cortical cells, tightly regulated changes in gene expression accompanied by a transient reorientation of secretion, enables the cell to build and populate the periarbuscular membrane with its unique complement of transporter proteins. Similarities between the cellular events for development of the periarbuscular membrane and cell plate formation are emerging. Address Boyce Thompson Institute for Plant Research, Tower Road, Ithaca, NY 14853, USA Corresponding author: Harrison, Maria J. ([email protected]) Current Opinion in Plant Biology 2012, 15:691–698 This review comes from a themed issue on Cell biology Edited by Keiko U Torii and Masao Tasaka For a complete overview see the Issue and the Editorial Available online 1st October 2012 1369-5266/$ – see front matter, # 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.pbi.2012.08.010 Introduction The arbuscular mycorrhizal (AM) symbiosis is formed by plants and fungi from the Glomeromycota. The ability to form AM symbiosis occurred early in the plant lineage and was retained in many plant families. As a result of its widespread distribution, AM symbiosis has a global impact on plant phosphorus nutrition and on the carbon cycle [1]. AM symbiosis is an endosymbiosis, that is, a symbiosis where one organism lives within the cells of another. During AM symbiosis, the fungus enters the root through the epidermal cells and grows into the cortex where it establishes highly branched hyphae called arbuscules within the cortical cells. At all stages of development, the hyphae that grow through, or differentiate within, plant cells are always surrounded by a plant membrane. www.sciencedirect.com This is referred to as the perifungal membrane around intracellular hyphae or the periarbuscular membrane (PAM) around the arbuscule. The arbuscule is the site of phosphate delivery to the plant and phosphate transporters in the PAM capture phosphate released from the arbuscule and transport it into the cortical cell [2–5]. The site of carbon transfer to the fungus is still unclear but analysis of an AM fungal hexose transporter implicates the arbuscule in this process [6]. Diffusible signals initiate the symbiosis before physical contact between the symbionts. Strigolactones, secreted from the roots of phosphate-deprived plants [7], activate AM fungal metabolism and this results in hyphal branching in proximity to the root [8,9]. Following contact with the root surface, the fungus forms a hyphopodium through which it penetrates the epidermis. Entry into the epidermal cell and subsequently the root cortex, is controlled by a plant signaling pathway, referred to as the common symbiosis signaling pathway (CSSP), so named because in legumes, this pathway is required also for the formation of symbiosis with rhizobia (Box 1). In CSSP loss-of-function mutants, the AM fungus is unable to enter epidermal or cortical cells. The current understanding of signaling through the CSSP has been obtained mostly from analyses of the rhizobium-legume symbiosis (RLS) (Box 1). Here, rhizobial Nod factors are perceived by LysM-domain receptor kinases and downstream signaling through the CSSP activates calcium spiking in root cells and gene expression changes necessary for RLS [10,11]. Calcium spiking and transient increases in cytosolic calcium levels also occur in root cells treated with exudates from AM fungi [12–14], and it was shown recently that AM fungi secrete a mixture of sulphated and non-sulphated lipochitooligosaccharides (referred to as Myc-LCOs) with structures very similar to Nod factors [15]. This suggests that activation of the CSSP for AM symbiosis may occur in a similar manner to activation by Nod factors. Currently, the full complement of receptors for Myc-LCOs is unknown. In Medicago truncatula, lateral root branching, which is one of the activities stimulated by Myc-LCOs is mediated partly through a Nod factor receptor, NFP [15], and in Parasponia, the ortholog of NFP is required for RLS and for arbuscule formation in AM symbiosis [16]. However, nfp and L. japonicus Nod factor receptor mutants nfr1 and nfr5, all form AM symbiosis [17,18], therefore in legumes, additional receptors must be involved in Myc-LCO perception for AM symbiosis. In M. truncatula the LysM-domain receptor family contains at least 17 members [19], one of which is induced during AM symbiosis [20] and any of which could be Myc-LCO receptors. Current Opinion in Plant Biology 2012, 15:691–698 692 Cell biology Box 1 Common symbiosis signaling pathway (CSSP) The CSSP is a signaling pathway required for AM symbiosis and rhizobium-legume symbiosis (RLS) and several recent reviews provide in depth coverage of this pathway [10,11]. As the AM symbiosis is the older of the two symbioses, it is assumed that the CSSP arose for AM symbiosis and was later coopted for RLS. Components of the CSSP were identified largely through genetic analyses of RLS. The pathway is comprised of a receptor kinase (SYMRK in L. japonicus, DMI2 in M. truncatula), ion channel(s) (CASTOR and POLLUX in L. japonicus, DMI1 in M. truncatula), a calcium calmodulin-dependent protein kinase (CCaMK), three components of the nuclear pore complex (NUP85, NUP135 and NENA in L. japonicus), a nuclear protein of unknown function (CYCLOPS in L. japonicus, IPD3 in M. truncatula) and a transcription factor, NSP2 of M. truncatula. It is assumed that for each symbiosis, signals perceived by unique receptors activate the signaling pathway and a combination of outputs, common to both symbioses and unique to each individual symbiosis, are obtained via signaling through different sets of transcription factors. A detailed understanding of signaling through the pathway has been obtained from analyses of RLS. In RLS, rhizobial lipochitooligosaccharide molecules called Nod factors are perceived by LysM-domain receptor kinases (NFR1, NFR5 in L. japonicus, NFP and LYK3 in M. truncatula) which then activate signaling through the CSSP. Calcium spiking is a central component of the CSSP and the spiking signal is likely decoded by CCaMK to activate NSP2 and also transcription factors unique to RLS, to result in changes in gene expression and RLS. The ion channels, receptor kinases and nuclear pore components are required to enable calcium spiking. Recently a sarco/endoplasmic reticulum calcium ATPase required for spiking was identified that is potentially another component of the CSSP [58]. develops around the nucleus and under the contact site. Subsequently, the nucleus migrates to the opposite side of the epidermal cell and a broad cytoplasmic column, containing the PPA, links the nucleus with its original position below the hyphopodium. FM4-64 labeling suggests that plasma membrane invagination occurs under the hyphopodium contact point and the penetrating hypha then grows across the cell, following the path defined by the PPA. Live cell imaging and electron microscopy analyses indicated that Golgi bodies were abundant under the hyphopodium and in the vicinity of the penetrating hypha, as were trans-Golgi networks (TGN). In addition, EXO-84, a marker of the exocytotic pathway, and VAMP proteins that mark secretory vesicles, accumulated in the vicinity of the hyphopodium, and around the growing hyphal tip [25]. These data point to substantial secretory activity in the PPA, likely associated with the synthesis of the perifungal membrane and matrix that envelop the hypha as it grows through the cell (Figure 1). A similar reorganization of the ER and nuclear migration was observed in the outer cortical cells before hyphal growth through the cell and also in the inner cortical cells preparing for arbuscule formation [14,22,25,26,27] (Box 2). Calcium signaling and hyphal growth through epidermal and cortical cells Which genes and which cellular processes are activated by the CSSP, or by other signaling pathways, to enable AM symbiosis? Here, recent advances that lead to our current understanding of the cellular programs used to accommodate fungal symbionts during AM symbiosis are reviewed. Some aspects of the programs are controlled by the CSSP and fall within the remit of a general accommodation program for endosymbionts, proposed originally by Parniske several years ago [21]. Cellular events during hyphal penetration of epidermal and cortical cells Two striking aspects of AM symbiosis are the extent to which root cells reorganize their internal structure to accommodate the fungal symbiont and the fact that the first changes occur before intracellular growth of the fungal hypha, suggesting that the cells prepare for infection [22,23]. As observed previously for pre-infection threads formed during RLS [24], the cellular reorganization defines the future path of hyphal growth through the cell. By using fluorescent protein fusions and confocal microscopy, the cellular alterations that occur in preparation for AM symbiosis have been analyzed in detail, particularly in epidermal cells in contact with a hyphopodium [23]. Here it was observed that the nucleus of the epidermal cell moves toward the hyphopodium contact site and a dense assemblage of ER, actin and microtubules, named the prepenetration apparatus (PPA), Current Opinion in Plant Biology 2012, 15:691–698 What induces PPA formation? PPAs were not observed in the CSSP mutants dmi2 or dmi3 [23] and constitutive expression of a gain-of-function CCaMK variant induces cytoplasmic aggregates which appear similar to PPAs [27]. Consequently, PPA formation is induced in response to signaling through the CSSP. In RLS, the analogous structure, the pre-infection thread, can be induced by Nod factors [24]. Analyses of calcium spiking during the pre-infection phase and also during hyphal growth through epidermal and outer cortical cells, revealed differences in the spiking signatures during these two phases. Epidermal cells in contact with a hyphopodium showed calcium spiking, as did the underlying outer cortical cells and in both cases, spiking was associated with nuclear migration toward the contact site and cytoplasmic aggregation [14,26]. A distinct increase in the frequency of the calcium spikes was observed as the fungus penetrated the cells. Detailed observations of outer cortical cells indicated that highfrequency spiking occurred only in the penetrated cell and was no longer detected once hyphal growth through the cell was complete (Figure 1). Similar analyses of RLS showed that growth of the infection thread across the outer cortical cells is also associated with high-frequency calcium spiking and the spiking signature was the same as that observed in root hair cells treated with Nod factors. Furthermore, the spiking signature observed in the outer www.sciencedirect.com Cellular programs for AM symbiosis Harrison 693 Figure 1 hypha Hyphopodium Penetrating PPA Golgi CSSP ER Vapryin/PAM1 punctate bodies TGN TGN CCaMK Hypothetical Myc-LCO receptor TG N Myc-LCO gene expression (VAPYRIN) Ca2+ Current Opinion in Plant Biology Growth of a fungal hypha through an epidermal cell is guided by the plant pre-penetration apparatus (PPA) that spans the cell. The PPA consists of cytoplasm containing a dense assemblage of ER, cytoskeletal components (not shown) and organelles of the secretory system. It functions to guide the hypha through the cell and secretion of the peri-fungal membrane (shown as an orange dotted line) and a matrix with composition similar to a primary cell wall (white space between the peri-fungal membrane and the penetrating hypha) is achieved through the secretory organelles within the PPA. The PPA forms in the cells underlying hyphopodia, before hyphal growth through the cell and its formation is triggered by signaling through the common symbiosis signaling pathway (CSSP). Although not yet shown directly, it is likely that Myc-LCOs produced by the fungus, induce formation of the PPA. Receptors that perceive Myc-LCOs and activate the CSSP for PPA formation have not been identified and are shown as ‘hypothetical receptors’. cortical cells during infection thread growth was the same as that observed during transcellular hyphal growth [26]. Consequently, it is likely that spiking in these cells is induced by Nod factors and Myc-LCOs produced by the respective symbionts. Do low-frequency and high-frequency calcium spiking induce different changes in gene expression associated with the preparative and penetration events? This is unknown but previous studies suggested that a minimum number of calcium spikes is necessary to induce gene expression changes [28], which would be most readily attained by high-frequency calcium spiking. A calcium spiking signature common www.sciencedirect.com to both symbioses can be expected to induce similar gene expression changes but how are gene expression patterns specific to each inducer [17] achieved? Currently, the answer to this is unclear but CCaMK may provide some specificity as this multi-domain protein does not function identically in the two symbioses [29,30]. Thus, a high-frequency calcium spiking signal induced by Nod factors and Myc-LCOs, may activate CCaMK and lead to both common and unique changes in gene expression depending on the environment. Additionally, specificity may arise from signaling independent of the CSSP [31–34]. Current Opinion in Plant Biology 2012, 15:691–698 694 Cell biology Box 2 Prepenetration apparatus (PPA) formation in the inner cortical cells PPA-like structures are also observed in the inner cortical cells before arbuscule formation and their morphology varies depending on the morpho-type of the mycorrhiza. In Arum-type symbioses, the PPA develops below the hyphal contact point and the nucleus migrates to the middle of the cell where it remains during arbuscule branching. In the Paris-type symbioses, where the fungal hyphae take an intracellular path through the inner cortical cells, the PPAs are particularly striking. As many as 5 cells ahead of the advancing hyphae show a polarized organization with a broad aggregation of ER that links the potential contact point to a centrally located nucleus and furthermore connects to the opposite side of the cell where the hypha will exit the cell. Time lapse imaging demonstrated that these PPAs define the path of hyphal growth as the fungus passed through each cell, sometimes forming large coils within the cell. These results suggest that either a diffusible signal or cell-to-cell communication ahead of the growing hypha initiates PPA formation [22,25]. PPA formation in the cortical cells is associated with significant enlargement of the nuclei [22,59] which may be necessary for the significant transcriptional activity that occurs during arbuscule development, or alternatively a reflection of endoreduplication [59,60]. The latter provides further support for the hypothesis of recruitment of the cell division program to enable periarbuscular membrane formation, as discussed later in this review. Vapyrin/PAM1, a gene induced by Myc-LCOs that is required for hyphal entry into cells While links between signaling and preparative cellular events have been made, we know relatively little about genes activated by the CSSP that function in cellular processes for the accommodation of the fungus. The Vapyrin gene of M. truncatula and its ortholog, PAM1 of Petunia hybrida are required for both AM symbiosis and RLS and may be the first candidate [35,36,37]. During AM symbiosis, Vapyrin is induced transiently in epidermal cells and then in cortical cells during hyphal growth into the cell [35]. It is likely that this occurs via MycLCOs as Vapryin transcripts are elevated in roots exposed to Myc-LCOs [17] and induction requires the CSSP [36]. However, Vapyin expression is not restricted to the penetrated cell but occurs also in adjacent cells, so if it is induced by the high-frequency calcium spiking, the signal must be further transduced to the neighboring cells. In Vapryin RNAi lines, 50% of the hyphopodia fail to penetrate epidermal cells [35,36] and hyphae that gain access to the inner cortex are unable to enter the cortical cells, so arbuscule formation is abolished. The phenotype of pam1 is similar, although some hyphae manage to penetrate cortical cells but fail to develop arbuscules [37]. The minor differences in phenotypes in M. truncatula and Petunia may result from differences in the fungal symbionts or environmental conditions. Currently, it is unclear how Vapyrin/PAM1 functions to enable hyphal penetration of cells. The Vapyrin/PAM1 protein is a novel combination of two previously described protein domains, a VAMP Associated Protein (VAP)/major sperm protein (MSP) domain and an ankyrin repeat domain; both domains are generally involved in protein–protein interactions. Vapyrin/PAM-GFP fusions Current Opinion in Plant Biology 2012, 15:691–698 revealed that the protein was present mostly as small puncta some of which move rapidly in the cell and it is possible that Vapyrin/PAM1 associates with proteins on vesicles involved in building the perimicrobial membranes [35,37]. Alternatively, MSP domains are known to self-oligomerize and Vapyrin puncta may be aggregates, possibly with a role in the development of the PPA. Currently, it is not known if PPAs form correctly in vapryin/pam1 mutants. Cellular activities in the inner cortical cells; accommodation of the arbuscule and development of the periarbuscular membrane The prepenetration apparatus and the phenotype of vapryin/pam1 mutants indicate a cellular program common to epidermal and cortical cells that enables hyphal growth into cells. However, in the inner cortical cells, additional events are necessary to enable arbuscule development including a substantial reorganization of cellular components and expression of a unique transcriptional program [38,39], which is not activated directly via the CCSP [27]. Currently, signals and regulators of this specific cortical cell program are unknown and only a few genes with potential roles in this program are known. In addition to Vapryin/PAM1, an ABC transporter STR/STR2 [40,41] and a secreted subtilisin protease, SbtM1 that localizes in the periarbuscular space [42], are required to enable arbuscule development. In both cases, their substrates and their exact roles are unknown. During arbuscule formation, the hypha enters the inner cortical cells and is guided to the middle of the cell by a PPA where arbuscule branching commences [22]. The signal that induces branching and terminal differentiation of the fungus is currently unknown. During arbuscule branching, the ER envelops the developing arbuscule and cytoskeletal components reorganize and bundle around the arbuscule branches [22,43–45]. Golgi bodies, which are particularly numerous, are positioned adjacent to arbuscule branch nodes [44], and markers suggest exocytosis at the hyphal tips [25]. Again, this arrangement of the cytoskeleton, organelles and markers point to secretory activities, likely associated with development of the PAM and matrix in the periarbuscular space. The PAM has two broad domains: the domain around the arbuscule trunk, which shares protein markers with the plasma membrane of the cell and a domain around the arbuscule branches, which contains a unique set of proteins including symbiotic phosphate transporters such as M. truncatula MtPT4 and rice OsPT11 [3,44]. The striking polarity of MtPT4 prompted investigations of the mechanism underlying its targeting to the branch-domain of the PAM. This led to an unexpected finding that several different plasma membrane-resident phosphate transporter and carbohydrate transporter proteins could www.sciencedirect.com Cellular programs for AM symbiosis Harrison 695 be targeted to the PAM if expressed ectopically from the MtPT4 promoter [46]. Subsequent analyses revealed that the final destination of these membrane proteins depended on the time at which they were expressed relative to arbuscule formation; expression before arbuscule formation resulted in location in the plasma membrane while expression coincident with arbuscule formation resulted in location in the PAM. These results suggested that during arbuscule formation the secretory pathway is redirected to the developing PAM [46] a finding that is also consistent with the positioning of the majority of the secretory organelles [25,44] Thus, the cell simultaneously builds and populates the PAM by reorienting secretory flow in the cell and activating transcription of genes encoding PAM-resident proteins. Additionally, alterations in the ER of colonized cells further controls which proteins enter the secretory system [46]. Currently, it is unclear when default secretion to the plasma membrane is reestablished but this probably occurs once PAM development is complete. Although the cell builds the PAM by redirecting secretion, there is still a requirement for some specific vesicle trafficking components. In M. truncatula, two SNAREs Figure 2 Arbuscule TGN N TGN TGN Vapryin/PAM1 punctate bodies MtPT4 Vesicles containing VAMP 721d and e Periarbuscular membrane STR/STR2 Layer of ER-rich cytoplasm Golgi TGN TGN Arrows indicate the direction of secretion Current Opinion in Plant Biology During arbuscule development, a layer of cytoplasm containing ER, cytoskeleton (not shown) and the tonoplast (not shown) surrounds the arbuscule (for detailed images of cytoskeleton and tonoplast, see [43,44,61]). Golgi bodies are abundant and locate at the branch nodes. Vapyrin/PAM1 punctate mobile bodies are abundant in the cell; Vapyrin/PAM1 is required for arbuscule formation but its cellular function is unknown. Vesicles containing VAMP721d/e are located around the hyphal branches. VAMP721d/e likely function in SNARE-mediated vesicle fusion to the periarbuscular membrane. The periarbuscular membrane is physically continuous with the plasma membrane of the cell but the domain around the arbuscule branches contains a unique set of proteins including phosphate transporters (MtPT4, OsPT11) and ABC transporters (STR/STR2) that are not present in the plasma membrane. Vapyrin/PAM1 punctate mobile bodies are abundant in the colonized cells; their function is unknown. During arbuscule branching, the default secretory pathway, which is normally directed to the plasma membrane, is reoriented to the periarbuscular membrane. www.sciencedirect.com Current Opinion in Plant Biology 2012, 15:691–698 696 Cell biology (soluble N-ethylmaleimide sensitive factor attachment protein receptor), VAMP721d and VAMP721e, likely play a role in periarbuscular membrane development [47]. The VAMP72 family of vSNAREs, of which VAMP721d/e are members, are located on the membranes of exocytotic vesicles and together with tSNAREs located on the target membrane; they mediate the fusion of vesicles and target membranes. VAMP721d/e are expressed in the inner cortical cells and knockdown via RNAi resulted in aberrant arbuscules with a trunk and very few short branches. GFPVAMP721 fusion proteins were visible in the vicinity of the arbuscule and it seems likely that they are located on vesicles where they mediate fusion to the PAM. Potential cargo of the VAMP721d/e vesicles would include PAMresident proteins, MtPT4 [48], an ABC transporter, STR/ STR2 [40,41] and a secreted subtilisin protease, SbtM1 [42]. VAMP721d/e are required also for symbiosome formation during RLS [47] indicating commonalities in exocytotic events in these two endosymbioses (Figure 2). and rhizobia-legume symbiosis continue to emerge, supporting the idea of a basic cellular program for the accommodation of endosymbionts [21], with individual specializations. The arbuscule is a transient structure and the PAM and matrix are rapidly built and later deconstructed as the cortical cell returns to its original state [49]. Development of the PAM has several parallels with cell plate formation during cytokinesis. In both cases, polarized secretion of large amounts of membrane occurs in a short space of time and this is achieved through the transient reorientation of default secretory flow [46,50,51]. Consistent with this, reorganization of the cytoskeleton and proliferation of Golgi, and secretory machinery are features common to both processes [25,45,52,53]. VAMP721 proteins are required in both of these processes [54] and the M. truncatula VAMP 721d/e proteins localize to the cell plate in meristematic cells [47]. Additionally, both processes require a transient reduction in vacuole volume and morphology [44,55,56]. Given these emerging similarities, it seems possible that some aspects of the program for accommodation of the arbuscule may have evolved from the cellular program for cell plate formation. A similar proposal has been made for infection thread growth during RLS, which is coupled to cell cycle reactivation and cell division processes [57]. Summary and conclusions In summary, the cellular programs for AM symbiosis are beginning to be revealed. The current data suggest that the fungal symbiont activates the CSSP to induce complex cellular changes necessary to enable its growth into the epidermal and cortical cells. In the cortical cells, an additional cellular program operates to accommodate the arbuscule and signals that activate this program are unknown. So far, only a handful of proteins that operate in these cellular accommodation programs have been identified and in most cases, their precise roles are unclear. It may be useful to turn to other cellular programs, such as cell plate formation, for additional clues. Commonalities in the cellular programs for AM symbiosis Current Opinion in Plant Biology 2012, 15:691–698 Acknowledgements Financial support was provided by the National Science Foundation IOS0842720 and IOS-0820005. Figures 1 and 2 were drawn by M. Swartwood Towne. References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as: of special interest of outstanding interest 1. Parniske M: Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 2008, 6:763-775. 2. Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ: A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 2007, 104:1720-1725. 3. Kobae Y, Hata S: Dynamics of periarbuscular membranes visualized with a fluorescent phosphate transporter in arbuscular mycorrhizal roots of rice. Plant Cell Physiol 2010, 51:341-353. 4. Paszkowski U, Kroken S, Roux C, Briggs SP: Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 2002, 99:13324-13329. 5. Maeda D, Ashida K, Iguchi K, Chechetka S, Hijikata A, Okusako Y, Deguchi Y, Izui K, Hata S: Knockdown of an arbuscular mycorrhiza-inducible phosphate transporter gene of Lotus japonicus suppresses mutualistic symbiosis. Plant Cell Physiol 2006, 47:807-817. 6. Helber N, Wippel K, Sauer N, Schaarschmidt S, Hause B, Requena N: A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp. is crucial for the symbiotic relationship with plants. Plant Cell 2011, 23:3812-3823. 7. Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M, Bachelier JB, Reinhardt D, Bours R, Bouwmeester HJ, Martinoia E: A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 2012, 483:341-344. The identification of an ABC transporter responsible for the efflux of strigolactones, the initial signals for AM symbiosis, from plant roots. The transporter is induced by phosphate-starvation and during AM symbiosis and transporter mutants have a reduced ability to form AM symbiosis. 8. Akiyama K, Matsuzaki K-I, Hayashi H: Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 2005, 435:824-827. 9. Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais JC, Roux C, Bécard G, SéjalonDelmas N: Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 2006, 4:1239-1247. 10. Oldroyd GED, Murray JD, Poole PS, Downie JA: The rules of engagement in the legume-rhizobial symbiosis. In Annual Review of Genetics, vol. 45. Edited by Bassler BL, Lichten M, Schupbach G. 2011:119-144. 11. Popp C, Ott T: Regulation of signal transduction and bacterial infection during root nodule symbiosis. Curr Opin Plant Biol 2011, 14:458-467. 12. Kosuta S, Hazledine S, Sun J, Miwa H, Morris RJ, Downie JA, Oldroyd GED: Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc Natl Acad Sci U S A 2008, 105:9823-9828. 13. Navazio L, Moscatiello R, Genre A, Novero M, Baldan B, Bonfante P, Mariani P: A diffusible signal from arbuscular www.sciencedirect.com Cellular programs for AM symbiosis Harrison 697 mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells. Plant Physiol 2007, 144:673-681. 14. Chabaud M, Genre A, Sieberer BJ, Faccio A, Fournier J, Novero M, Barker DG, Bonfante P: Arbuscular mycorrhizal hyphopodia and germinated spore exudates trigger Ca(2+) spiking in the legume and nonlegume root epidermis. New Phytol 2011, 189:347-355. 24. Vanbrussel AAN, Bakhuizen R, Vanspronsen PC, Spaink HP, Tak T, Lugtenberg BJJ, Kijne JW: Induction of preinfection thread structures in the leguminous host plant by mitogenic lipooligosaccharides of rhizobium. Science 1992, 257:70-72. 25. Genre A, Ivanov S, Fendrych M, Faccio A, Zarsky V, Bisseling T, Bonfante P: Multiple exocytotic markers accumulate at the sites of perifungal membrane biogenesis in arbuscular mycorrhizas. Plant Cell Physiol 2012, 53:244-255. 15. Maillet F, Poinsot V, Andre O, Puech-Pages V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A et al.: Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 2011, 469:58-64. The authors demonstrate that AM fungi secrete sulphated and nonsulphated lipochitooligosaccharide molecules with structures similar to those of Nod factors produced by rhizobia. This has many implications, for example, activation of the common symbiosis signaling pathway for AM symbiosis will likely occur in a manner similar to activation by Nod factors, that is, through Lys-M domain receptor kinases. Additionally, root branching induced by Myc-LCOs occurs partially through the Nod factor receptor NFP and requires the GRAS transcription factor, NSP2. 26. Sieberer BJ, Chabaud M, Fournier J, Timmers AC, Barker DG: A switch in Ca2+ spiking signature is concomitant with endosymbiotic microbe entry into cortical root cells of Medicago truncatula. Plant J 2012, 69:822-830. The authors use chameleon to monitor calcium signatures before, and during, hyphal growth across epidermal and outer cortical cells. Low frequency calcium spiking is associated with preparative cellular events that are reversible. The frequency of spiking changes during intracellular growth of the hypha. In addition, the calcium signatures during transcellular growth of infection threads during nodulation are the same as those observed during hyphal growth. 16. den Camp RO, Streng A, De Mita S, Cao QQ, Polone E, Liu W, Ammiraju JSS, Kudrna D, Wing R, Untergasser A et al.: LysM-type mycorrhizal receptor recruited for rhizobium symbiosis in nonlegume parasponia. Science 2011, 331:909-912. In Parasponia, downregulation of the ortholog of NFP by RNAi results in a failure to form arbuscules during AM symbiosis. This suggests the involvement of the Nod factor receptors (Lys-M domain receptor kinases) in AM symbiosis. This implies that in the legumes, where the Lys-M domain receptor gene family has expanded redundancy may mask the roles of the Nod factor receptors in AM symbiosis. 27. Takeda N, Maekawa T, Hayashi M: Nuclear-localized and deregulated calcium- and calmodulin-dependent protein kinase activates rhizobial and mycorrhizal responses in Lotus japonicus. Plant Cell 2012, 24:810-822. A gain-of-function CCAMK mutant induces gene expression changes and cytoplasmic aggregates similar to PPAs in root cells. This provides further evidence that signaling through the common symbiosis signaling pathway induces PPA formation. Additionally, they provide evidence for differences for the requirements in CCAMK in AM symbiosis and rhizobium-legume symbiosis. 17. Czaja L, Hogekamp C, Lamm P, Maillet F, Martinez E, Samain E, Denarie J, Kuster H, Hohnjec N: Transcriptional responses towards diffusible signals from symbiotic microbes reveal MtNFP and MtDMI3-dependent reprogramming of host gene expression by AM fungal LCOs. Plant Physiol 2012, 159:1671-1685. Array data provide a large-scale description of the gene expression patterns induced by Nod factors and Myc-LCOs. The data indicate that despite their similar structures, these molecules induce both overlapping, and distinct, sets of genes. 28. Miwa H, Sun J, Oldroyd GED, Downie JA: Analysis of calcium spiking using a cameleon calcium sensor reveals that nodulation gene expression is regulated by calcium spike number and the developmental status of the cell. Plant J 2006, 48:883-894. 18. Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, Gronlund M, Sato S, Nakamura Y, Tabata S, Sandal N et al.: Plant recognition of symbiotic bacteria requires two LysM receptorlike kinases. Nature 2003, 425:585-592. 19. Arrighi JF, Barre A, Ben Amor B, Bersoult A, Soriano LC, Mirabella R, de Carvalho-Niebel F, Journet EP, Ghérardi M, Huguet T et al.: The Medicago truncatula lysine motif-receptorlike kinase gene family includes NFP and new noduleexpressed genes. Plant Physiol 2006, 142:265-279. 20. Gomez SK, Javot H, Deewatthanawong P, Torrez-Jerez I, Tang Y, Blancaflor EB, Udvardi MK, Harrison MJ: Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol 2009, 9:1-19. 21. Parniske M: Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease? Curr Opin Plant Biol 2000, 3:320-328. In this review, the author considered the commonalities between endosymbioses and first proposed that plants might possess a program used generally for the accommodation of endosymbionts. This astute prediction was made before the identification of the common symbiosis signaling pathway. 22. Genre A, Chabaud M, Faccio A, Barker DG, Bonfante P: Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungus within the root cortex of both Medicago truncatula and Daucus carota. Plant Cell 2008, 20:1407-1420. 23. Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG: Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 2005, 17:3489-3499. This classic paper was the first to describe the cellular reorganization (the prepenetration apparatus) that occurs in root epidermal cells in contact with hyphopodia, before cellular penetration of the fungal hypha. The authors demonstrated that the pre-penetration apparatus defines the future path of hyphal growth through the cell and formation of this apparatus required the common symbiosis signaling pathway. www.sciencedirect.com 29. Hayashi T, Banba M, Shimoda Y, Kouchi H, Hayashi M, ImaizumiAnraku H: A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts. Plant J 2010, 63:141-154. 30. Shimoda Y, Han L, Yamazaki T, Suzuki R, Hayashi M, Imaizumi Anraku H: Rhizobial and fungal symbioses show different requirements for calmodulin binding to calcium calmodulindependent protein kinase in Lotus japonicus. Plant Cell 2012, 24:304-321. The authors show different requirements for CCAMK in AM symbiosis and rhizobium-legume symbiosis. For example, the CAM binding domain is not necessary for AM symbiosis. The data provide evidence that specificity in signaling through the common symbiosis signaling pathway can occur at CCAMK. 31. Kistner C, Winzer T, Pitzschke A, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Webb KJ et al.: Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell 2005, 17:2217-2229. 32. Gutjahr C, Banba M, Croset V, An K, Miyao A, An G, Hirochika H, Imaizumi-Anraku H, Paszkowski U: Arbuscular mycorrhizaspecific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell 2008, 20:2989-3005. 33. Kuhn H, Kuster H, Requena N: Membrane steroid-binding protein 1 induced by a diffusible fungal signal is critical for mycorrhization in Medicago truncatula. New Phytol 2010, 185:716-733. 34. Mukherjee A, Ane JM: Germinating spore exudates from arbuscular mycorrhizal fungi: molecular and developmental responses in plants and their regulation by ethylene. Mol PlantMicrobe Interact 2011, 24:260-270. 35. Pumplin N, Mondo SJ, Topp S, Starker CG, Gantt JS, Harrison MJ: Medicago truncatula Vapyrin is a novel protein required for arbuscular mycorrhizal symbiosis. Plant J 2010, 61:482-494. This paper by and papers by Murray et al. [36] and Fedderman et al. [37] report the identification of a gene of unknown function, Vapyrin of M. truncatula and PAM1 of Petunia hybrida, that is required for hyphal growth into epidermal and cortical cells, and also for arbuscule development. Vapyrin/PAM1 is the first protein required for the accommodation of Current Opinion in Plant Biology 2012, 15:691–698 698 Cell biology endosymbionts that likely has function other than signaling. Currently this function is unknown. 36. Murray JD, Muni RRD, Torres-Jerez I, Tang YH, Allen S, Andriankaja M, Li GM, Laxmi A, Cheng XF, Wen JQ et al.: Vapyrin, a gene essential for intracellular progression of arbuscular mycorrhizal symbiosis, is also essential for infection by rhizobia in the nodule symbiosis of Medicago truncatula. Plant J 2011, 65:244-252. See comments for Pumplin et al. [35] In addition, the authors demonstrate that Vapryin is required also for infection thread growth through the epidermal cells during rhizobium-legume symbiosis. 37. Feddermann N, Muni RRD, Zeier T, Stuurman J, Ercolin F, Schorderet M, Reinhardt D: The PAM1 gene of petunia, required for intracellular accommodation and morphogenesis of arbuscular mycorrhizal fungi, encodes a homologue of VAPYRIN. Plant J 2010, 64:470-481. See comments for Pumplin et al. [36] In Petunia, the PAM 1 phenotype is slightly different to that of vapyrin mutants and the fungal hyphal penetrate the cortical cells but arbuscule formation is severely impaired. This is significant because it provides evidence for an ongoing role for PAM1 during the arbuscule branching phase of arbuscule development. 38. Hogekamp C, Arndt D, Pereira PA, Becker JD, Hohnjec N, Kuster H: Laser microdissection unravels cell-type-specific transcription in arbuscular mycorrhizal roots including CAATbox transcription factor gene expression correlating with fungal contact and spread. Plant Physiol 2011, 157:2023-2043. 39. Gaude N, Bortfeld S, Duensing N, Lohse M, Krajinski F: Arbuscule-containing and non-colonized cortical cells of mycorrhizal roots undergo extensive and specific reprogramming during arbuscular mycorrhizal development. Plant J 2012, 69:510-528. 40. Zhang Q, Blaylock LA, Harrison MJ: Two Medicago truncatula half-ABC transporters are essential for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Cell 2010, 22:1483-1497. 41. 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Pumplin N, Harrison MJ: Live-cell imaging reveals periarbuscular membrane domains and organelle location in Medicago truncatula roots during arbuscular mycorrhizal symbiosis. Plant Physiol 2009, 151:809-819. 45. Blancaflor EB, Zhao LM, Harrison MJ: Microtubule organization in root cells of Medicago truncatula during development of an arbuscular mycorrhizal symbiosis with Glomus versiforme. Protoplasma 2001, 217:154-165. 46. Pumplin N, Zhang X, Noar RD, Harrison MJ: Polar localization of a symbiosis-specific phosphate transporter is mediated by a transient reorientation of secretion. Proc Natl Acad Sci U S A 2012, 109:E665-E672 http://dx.doi.org/10.1073/ pnas.1110215109. Current Opinion in Plant Biology 2012, 15:691–698 The authors investigate targeting of a symbiotic phosphate transporter, MtPT4, to the periarbuscular membrane. Unexpectedly, the data reveal that during arbuscule formation, the default secretory pathway of the colonized cortical cell is reoriented to the periarbuscular membrane. Consequently expression of MtPT4 coincident with arbuscule/periarbuscular membrane formation is sufficient to result in location in the periarbuscular membrane. 47. Ivanov S, Fedorova EE, Limpens E, De Mita S, Genre A, Bonfante P, Bisseling T: Rhizobium-legume symbiosis shares an exocytotic pathway required for arbuscule formation. Proc Natl Acad Sci U S A 2012, 109:8316-8321. Knockdown of two VAMP proteins of the VAMP721 family prevents arbuscule formation during AM symbiosis and symbiosome formation during nodulation. The VAMP proteins are located in the vicinity of the developing arbuscule and are likely required for building the periarbuscular membrane. 48. 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