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Fast moves in arbuscular mycorrhizal symbiotic signalling
Update
TRENDS in Plant Science
Vol.11 No.8
Full text provided by www.sciencedirect.com
Research Focus
Fast moves in arbuscular mycorrhizal symbiotic signalling Sally E. Smith1, Susan J. Barker2 and Yong-Guan Zhu1,3 1
Soil and Land Systems, School of Earth and Environmental Sciences, Waite Campus, DP636, The University of Adelaide, Adelaide, SA 5005, Australia 2 School of Plant Biology M084, University of Western Australia, 35 Stirling Highway, Crawley, WA 6009 Australia 3 Research Center for Eco-environmental Sciences, Chinese Academy of Sciences, China
Exciting research looking at early events in arbuscular mycorrhizal symbioses has shown how the fungus and plant get together. Kohki Akiyama et al. have demonstrated that strigolactones in root exudates are fungal germ tube branching factors, and Arnaud Besserer et al. found that these compounds rapidly induce fungal mitochondrial activity. Andrea Genre et al. have shown that subsequent development of appressoria on host roots induces construction of a transient prepenetration apparatus inside epidermal cells that is reminiscent of nodulation infection. Arbuscular mycorrhiza: a beneficial symbiosis gives up secrets One intriguing question about arbuscular mycorrhizal symbioses (AMS, see Box 1) is how the partnerships between the fungal symbionts and the host roots are established without triggering rejection. Research has been inhibited by some key features of AMS: lack of partner specificity, obligate status of the fungi, highly compatible interactions and non-synchronous development. Here we highlight three articles that have made significant contributions towards our understanding of the early interactions between symbionts. Plant signals stimulate fungal activity and transition to a symbiosis-ready state Kohki Akiyama et al. [1] used a neat and simple bioassay of AM fungal germ tube branching [2] to identify and hence chemically characterize active compounds in root exudates that lead to morphogenetic changes in advance of root colonization. These changes appear crucial in converting germ tubes with limited growth potential into presymbiotic mycelium that has the capacity to initiate colonization of roots, which is a crucial step in the life of an obligate symbiont. The changes (shown earlier with partially purified root exudates and now with purified compounds) involve rapid alterations in gene expression, an increase in mitochondrial activity (shown in vivo with Mitotracker green and also immunologically) as well as respiration rate and, 5 h after stimulation, increased branching [3–5]. The active compounds are strigolactones and are effective at extremely low concentrations. This suggests that they probably act through a signalling pathway that can lead to Corresponding author: Smith, S.E. ([email protected]) Available online 12 July 2006. www.sciencedirect.com
fully effective catabolism of lipids, which are the major carbon currency of AM fungi. Strigolactones have previously been identified because of their importance in stimulating germination of the economically damaging root parasites Striga and Orobanche. The new findings lead the way to controlled investigation of changes in fungal metabolism that occur as AM fungal germ tubes are stimulated, and should allow mycorrhizal researchers to capitalize on knowledge of the molecular interactions involved in the initiation of root parasite infections [6] and the tools that are being developed to combat them, such as labelled molecules to identify strigolactone receptors in Striga itself [7]. What is fascinating is the possibility that the parasitic members of the advanced angiosperm family Scrophulariaceae might have coopted a recognition and developmental pathway that evolved when the earliest land plants interacted with AM fungi. There is already evidence for such cooption by nitrogen-fixing symbioses (NFS). Formation of a special plant structure guiding fungal invasion of roots Andrea Genre et al. [8] targeted plant events during the initial colonization step as symbiosis-ready fungal hyphae contact roots. They showed how epidermal cells assemble a special intracellular structure before any cell penetration occurs. Using Medicago truncatula root clones expressing GFP-labelled markers for plant cytoskeleton and endoplasmic reticulum (ER), they followed, by elegant confocal microscopy, epidermal cell responses to the formation of fungal appressoria and hyphal penetration in living cells over many hours. First the epidermal cell nucleus was repositioned immediately under the appressorium (Figure 1a,b). How that event is triggered remains unknown. Highly regulated events followed, directed by further movements of the cell nucleus, leading to the formation of a special prepenetration apparatus (PPA) within 4–5 h of appressorium formation (Figure 1c). The PPA is formed within a cytoplasmic column; labelling shows a high-density array of microtubules and microfilament bundles running parallel to the column, associated with a region of dense ER cisternae. Once the PPA is formed, fungal entry and growth of hyphae across the cell follow precisely the track defined by the cytoskeletal and ER structures within the column (Figure 1d). Before and during assembly of the PPA, ENOD11 expression is
370
Update
TRENDS in Plant Science
Box 1. Arbuscular mycorrhizal symbioses Arbuscular mycorrhizas are thought to be the most ancient terrestrial symbioses, and plant roots and AM fungi (Glomeromycota) have been coevolving for >450 million years. Arbuscular mycorrhizal symbioses (AMS) pre-date other mycorrhizal types, as well as nitrogen-fixing symbioses (NFS) in legumes. About 80% of present-day terrestrial plants form AMS, distributed in a wide range of habitats, suggesting that these biotrophic and mutualistic associations have selective advantages for both plant and fungal symbionts. The main basis of mutualism is bidirectional nutrient transfer: sugars transfer from plant to fungus, in exchange for mineral nutrients, particularly phosphorus, from the fungus. This exchange occurs across specialized interfaces between the symbionts developed deep in the root cortex [15]. The process of colonization requires a complex signalling network and morphogenetic changes in both symbionts (Figure I). Our understanding of these processes has been greatly enhanced by detailed developmental and molecular studies of symbiotic mutants [10,16].
Figure I. Steps in the colonization of roots by AM fungi. (a) Hyphae (h) on the surface of a root produce a swollen appressorium (ap) from which a penetrating hypha (arrow) traverses the epidermal cell to reach the cortex where intracellular coils (C) develop in Paris-type AM. Abbreviation: V, vesicle. (b) Cortical Arum-type colonization involves the spread of intercellular hyphae (ih) and the development of highly branched intracellular arbuscules (arb). Image (a) S.E. Smith; image (b) reproduced, with permission, from Ref. [17].
initiated in epidermal cells. This gene encodes a protein that is believed to be part of the plant extracellular matrix. Genre et al. [8] suggest that the transient PPA is responsible for the formation of an intracellular symbiotic interface, including a new membrane structure that creates an apoplastic plant compartment separating the invading fungus from the plant. It is tempting to speculate, as the authors do, that the invasion process parallels the way that infection threads ‘lead’ rhizobium through legume root hairs into the root cortex during the establishment of NFS nodules. Plant genetic overlaps between AMS and NFS are well established [9,10] and are strengthened by the demonstration of induction of ENOD11, which is also involved in NFS
Vol.11 No.8
establishment, and by the finding that no PPAs are formed in dmi2 or dmi3 mutants of M. truncatula, which do not become infected by AM fungi or rhizobium. The findings implicate common symbiosis genes in PPA formation, but also indicate that these are not involved in the primary pre-penetration signalling because nuclear movement in the epidermal cells occurs normally in the mutants. The way in which putative ‘myc factors’ are perceived and transduced to facilitate AM penetration via the PPA will be a fascinating line of future research. Coordination and timing of sweet talk between the symbionts AM fungal spores can germinate in the soil in the absence of any plants. The root signals now identified [1,5] alert the fungi to the presence of a potential host and hence a vital source of organic carbon. The papers show that AM-active strigolactones are produced by Lotus and Sorghum and that they induce responses in phylogenetically distinct and distant AM fungi. It seems reasonable to predict that they are extremely widespread plant products. However, Arnaud Besserer et al. [5] caution that other classes of active molecule must not be ruled out. The increased branching of fungal germ tubes probably increases the chances of root contact, and changes in gene expression and respiratory activity convert the fungus to an infection-ready state. When contact is made, fungal morphogenesis changes once more, with the formation of slightly swollen appressoria on the root epidermis (Box 1). Now fungal signals alert the plant, which prepares the way for intracellular penetration and forms the PPA and interfacial structures that lead the fungus inward towards the root cortex [8]. The initial stages of colonization are completed in 10 h. Elucidation of the next stages of development will be more challenging because the intracellular interfaces involved in nutrient transfer between symbionts develop within root cortical cells. We anticipate that formation of intracellular arbuscules and coils will involve highly coordinated cellular processes, similar to those described in epidermal cells, but probably more complicated. The development of cortical interfaces probably takes a further 1–2 days after penetration and involves nuclear repositioning and changes in expression and localization of the membrane and matrix proteins that facilitate nutrient transfers [11]. ENOD11 expression is also induced in these cells, independently of epidermal
Figure 1. Formation of the prepenetration apparatus (PPA) that facilitates passage of AM fungi through epidermal cells. Appressorium formation on the outer surface of the host cell (a) results in initial nuclear movement toward the surface appressorium (b). This is followed by the assembly of the transient PPA within the cytoplasmic column created during the subsequent transcellular nuclear migration (c). Finally, the AM infection hypha crosses the epidermal cell through the apoplastic compartment constructed within the cytoplasmic column (d). Colour coding is as follows: cell nucleus, dark brown; plasma membrane, light brown; microtubules, green; actin bundles, red; ER, white. Reproduced, with permission, from Ref. [8]. www.sciencedirect.com
Update
TRENDS in Plant Science
expression [12]. Intriguing new data also implicate a reactive oxygen species-inactivating system in signal transduction between the symbionts [13] and haemoglobin-encoding gene in suppression of NO-based defence processes during arbuscule formation [14]. Advances in our understanding of these late stages would be greatly facilitated by an extended range of mutants. Developmental diversity? The research discussed here understandably used a limited range of fungi and plants that best suited the technical challenges. But we know that there is considerable developmental and functional diversity and even limited specificity among the symbioses that are formed between the huge array of potential host plants and the 120 or so fungi in the Glomeromycota. Do the root and fungal signals and their receptors carry the necessary information to encompass this diversity in the developmental programmes? And does the limited cortical colonization of some mutants normally blocked at the surface result from bypassing epidermal cell penetration and thus avoiding the requirement for triggered formation of a PPA? This again is for the future. Acknowledgements Our collaborations are funded by the Australian Research Council and the Natural Science Foundation of China (40225002).
References 1 Akiyama, K. et al. (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824–827 2 Nagahashi, G. and Douds, D.D. (1999) Rapid and sensitive bioassay to study signals between root exudates and arbuscular mycorrhizal fungi. Biotechnol. Tech. 13, 893–897 3 Buee, M. et al. (2000) The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol. Plant Microbe Interact. 13, 693–698
Vol.11 No.8
4 Tamasloukht, M. et al. (2003) Root factors induce mitochondrialrelated gene expression and fungal respiration during the developmental switch from asymbiosis to presymbiosis in the arbuscular mycorrhizal fungus Gigaspora rosea. Plant Physiol. 131, 1468–1478 5 Besserer, A. et al. (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol. 4 (7), e226 6 Yoder, J.I. (2001) Host–plant recognition by parasitic Scrophulariaceae. Curr. Opin. Plant Biol. 4, 359–365 7 Reizelman, A. et al. (2003) Synthesis and bioactivity of labelled germination stimulants for the isolation and identification of the strigolactone receptor. Org. Biomol. Chem. 1, 950–959 8 Genre, A. et al. (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17, 3489–3499 9 Kistner, C. et al. (2005) Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell 17, 2217–2229 10 Harrison, M.J. (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu. Rev. Microbiol. 59, 19–42 11 Karandashov, V. and Bucher, M. (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci. 10, 22–29 12 Chabaud, M. et al. (2002) Targeted inoculation of Medicago truncatula in vitro root cultures reveals MtENOD11 expression during early stages of infection by arbuscular mycorrhizal fungi. New Phytol. 156, 265–273 13 Lanfranco, L. et al. (2005) The mycorrhizal fungus Gigaspora margarita possesses a CuZn superoxide dismutase that is up-regulated during symbiosis with legume hosts. Plant Physiol. 137, 1319–1330 14 Vieweg, M.F. et al. (2005) Two genes encoding different truncated hemoglobins are regulated during root nodule and arbuscular mycorrhiza symbioses of Medicago truncatula. Planta 220, 757–766 15 Smith, S.E. and Read, D.J. (1997) Mycorrhizal Symbiosis, (Ed 2). Academic Press 16 Parniske, M. (2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr. Opin. Plant Biol. 7, 414–421 17 Smith, S.E. et al. (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol. 162, 511–524 1360-1385/$ – see front matter ß 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2006.06.008
Plant Science meetings sponsored by Trends in Plant Science Haploids in Higher Plants III 12–15 February 2006 Vienna, Austria http://www.univie.ac.at/gem/conference/haploids/ The Second Symposium on Plant Neurobiology 22–27 May 2006 Beijing, China http://plantneurobiology.ibcas.ac.cn/index.htm 2006 FASEB Summer Research Conference: ‘Mechanisms in Plant Development’ 5–9 August 2006 Vermont Academy, Saxtons River, VT, USA http://src.faseb.org/preliminary.htm www.sciencedirect.com
371
TRENDS in Plant Science
Vol.11 No.8
Full text provided by www.sciencedirect.com
Research Focus
Fast moves in arbuscular mycorrhizal symbiotic signalling Sally E. Smith1, Susan J. Barker2 and Yong-Guan Zhu1,3 1
Soil and Land Systems, School of Earth and Environmental Sciences, Waite Campus, DP636, The University of Adelaide, Adelaide, SA 5005, Australia 2 School of Plant Biology M084, University of Western Australia, 35 Stirling Highway, Crawley, WA 6009 Australia 3 Research Center for Eco-environmental Sciences, Chinese Academy of Sciences, China
Exciting research looking at early events in arbuscular mycorrhizal symbioses has shown how the fungus and plant get together. Kohki Akiyama et al. have demonstrated that strigolactones in root exudates are fungal germ tube branching factors, and Arnaud Besserer et al. found that these compounds rapidly induce fungal mitochondrial activity. Andrea Genre et al. have shown that subsequent development of appressoria on host roots induces construction of a transient prepenetration apparatus inside epidermal cells that is reminiscent of nodulation infection. Arbuscular mycorrhiza: a beneficial symbiosis gives up secrets One intriguing question about arbuscular mycorrhizal symbioses (AMS, see Box 1) is how the partnerships between the fungal symbionts and the host roots are established without triggering rejection. Research has been inhibited by some key features of AMS: lack of partner specificity, obligate status of the fungi, highly compatible interactions and non-synchronous development. Here we highlight three articles that have made significant contributions towards our understanding of the early interactions between symbionts. Plant signals stimulate fungal activity and transition to a symbiosis-ready state Kohki Akiyama et al. [1] used a neat and simple bioassay of AM fungal germ tube branching [2] to identify and hence chemically characterize active compounds in root exudates that lead to morphogenetic changes in advance of root colonization. These changes appear crucial in converting germ tubes with limited growth potential into presymbiotic mycelium that has the capacity to initiate colonization of roots, which is a crucial step in the life of an obligate symbiont. The changes (shown earlier with partially purified root exudates and now with purified compounds) involve rapid alterations in gene expression, an increase in mitochondrial activity (shown in vivo with Mitotracker green and also immunologically) as well as respiration rate and, 5 h after stimulation, increased branching [3–5]. The active compounds are strigolactones and are effective at extremely low concentrations. This suggests that they probably act through a signalling pathway that can lead to Corresponding author: Smith, S.E. ([email protected]) Available online 12 July 2006. www.sciencedirect.com
fully effective catabolism of lipids, which are the major carbon currency of AM fungi. Strigolactones have previously been identified because of their importance in stimulating germination of the economically damaging root parasites Striga and Orobanche. The new findings lead the way to controlled investigation of changes in fungal metabolism that occur as AM fungal germ tubes are stimulated, and should allow mycorrhizal researchers to capitalize on knowledge of the molecular interactions involved in the initiation of root parasite infections [6] and the tools that are being developed to combat them, such as labelled molecules to identify strigolactone receptors in Striga itself [7]. What is fascinating is the possibility that the parasitic members of the advanced angiosperm family Scrophulariaceae might have coopted a recognition and developmental pathway that evolved when the earliest land plants interacted with AM fungi. There is already evidence for such cooption by nitrogen-fixing symbioses (NFS). Formation of a special plant structure guiding fungal invasion of roots Andrea Genre et al. [8] targeted plant events during the initial colonization step as symbiosis-ready fungal hyphae contact roots. They showed how epidermal cells assemble a special intracellular structure before any cell penetration occurs. Using Medicago truncatula root clones expressing GFP-labelled markers for plant cytoskeleton and endoplasmic reticulum (ER), they followed, by elegant confocal microscopy, epidermal cell responses to the formation of fungal appressoria and hyphal penetration in living cells over many hours. First the epidermal cell nucleus was repositioned immediately under the appressorium (Figure 1a,b). How that event is triggered remains unknown. Highly regulated events followed, directed by further movements of the cell nucleus, leading to the formation of a special prepenetration apparatus (PPA) within 4–5 h of appressorium formation (Figure 1c). The PPA is formed within a cytoplasmic column; labelling shows a high-density array of microtubules and microfilament bundles running parallel to the column, associated with a region of dense ER cisternae. Once the PPA is formed, fungal entry and growth of hyphae across the cell follow precisely the track defined by the cytoskeletal and ER structures within the column (Figure 1d). Before and during assembly of the PPA, ENOD11 expression is
370
Update
TRENDS in Plant Science
Box 1. Arbuscular mycorrhizal symbioses Arbuscular mycorrhizas are thought to be the most ancient terrestrial symbioses, and plant roots and AM fungi (Glomeromycota) have been coevolving for >450 million years. Arbuscular mycorrhizal symbioses (AMS) pre-date other mycorrhizal types, as well as nitrogen-fixing symbioses (NFS) in legumes. About 80% of present-day terrestrial plants form AMS, distributed in a wide range of habitats, suggesting that these biotrophic and mutualistic associations have selective advantages for both plant and fungal symbionts. The main basis of mutualism is bidirectional nutrient transfer: sugars transfer from plant to fungus, in exchange for mineral nutrients, particularly phosphorus, from the fungus. This exchange occurs across specialized interfaces between the symbionts developed deep in the root cortex [15]. The process of colonization requires a complex signalling network and morphogenetic changes in both symbionts (Figure I). Our understanding of these processes has been greatly enhanced by detailed developmental and molecular studies of symbiotic mutants [10,16].
Figure I. Steps in the colonization of roots by AM fungi. (a) Hyphae (h) on the surface of a root produce a swollen appressorium (ap) from which a penetrating hypha (arrow) traverses the epidermal cell to reach the cortex where intracellular coils (C) develop in Paris-type AM. Abbreviation: V, vesicle. (b) Cortical Arum-type colonization involves the spread of intercellular hyphae (ih) and the development of highly branched intracellular arbuscules (arb). Image (a) S.E. Smith; image (b) reproduced, with permission, from Ref. [17].
initiated in epidermal cells. This gene encodes a protein that is believed to be part of the plant extracellular matrix. Genre et al. [8] suggest that the transient PPA is responsible for the formation of an intracellular symbiotic interface, including a new membrane structure that creates an apoplastic plant compartment separating the invading fungus from the plant. It is tempting to speculate, as the authors do, that the invasion process parallels the way that infection threads ‘lead’ rhizobium through legume root hairs into the root cortex during the establishment of NFS nodules. Plant genetic overlaps between AMS and NFS are well established [9,10] and are strengthened by the demonstration of induction of ENOD11, which is also involved in NFS
Vol.11 No.8
establishment, and by the finding that no PPAs are formed in dmi2 or dmi3 mutants of M. truncatula, which do not become infected by AM fungi or rhizobium. The findings implicate common symbiosis genes in PPA formation, but also indicate that these are not involved in the primary pre-penetration signalling because nuclear movement in the epidermal cells occurs normally in the mutants. The way in which putative ‘myc factors’ are perceived and transduced to facilitate AM penetration via the PPA will be a fascinating line of future research. Coordination and timing of sweet talk between the symbionts AM fungal spores can germinate in the soil in the absence of any plants. The root signals now identified [1,5] alert the fungi to the presence of a potential host and hence a vital source of organic carbon. The papers show that AM-active strigolactones are produced by Lotus and Sorghum and that they induce responses in phylogenetically distinct and distant AM fungi. It seems reasonable to predict that they are extremely widespread plant products. However, Arnaud Besserer et al. [5] caution that other classes of active molecule must not be ruled out. The increased branching of fungal germ tubes probably increases the chances of root contact, and changes in gene expression and respiratory activity convert the fungus to an infection-ready state. When contact is made, fungal morphogenesis changes once more, with the formation of slightly swollen appressoria on the root epidermis (Box 1). Now fungal signals alert the plant, which prepares the way for intracellular penetration and forms the PPA and interfacial structures that lead the fungus inward towards the root cortex [8]. The initial stages of colonization are completed in 10 h. Elucidation of the next stages of development will be more challenging because the intracellular interfaces involved in nutrient transfer between symbionts develop within root cortical cells. We anticipate that formation of intracellular arbuscules and coils will involve highly coordinated cellular processes, similar to those described in epidermal cells, but probably more complicated. The development of cortical interfaces probably takes a further 1–2 days after penetration and involves nuclear repositioning and changes in expression and localization of the membrane and matrix proteins that facilitate nutrient transfers [11]. ENOD11 expression is also induced in these cells, independently of epidermal
Figure 1. Formation of the prepenetration apparatus (PPA) that facilitates passage of AM fungi through epidermal cells. Appressorium formation on the outer surface of the host cell (a) results in initial nuclear movement toward the surface appressorium (b). This is followed by the assembly of the transient PPA within the cytoplasmic column created during the subsequent transcellular nuclear migration (c). Finally, the AM infection hypha crosses the epidermal cell through the apoplastic compartment constructed within the cytoplasmic column (d). Colour coding is as follows: cell nucleus, dark brown; plasma membrane, light brown; microtubules, green; actin bundles, red; ER, white. Reproduced, with permission, from Ref. [8]. www.sciencedirect.com
Update
TRENDS in Plant Science
expression [12]. Intriguing new data also implicate a reactive oxygen species-inactivating system in signal transduction between the symbionts [13] and haemoglobin-encoding gene in suppression of NO-based defence processes during arbuscule formation [14]. Advances in our understanding of these late stages would be greatly facilitated by an extended range of mutants. Developmental diversity? The research discussed here understandably used a limited range of fungi and plants that best suited the technical challenges. But we know that there is considerable developmental and functional diversity and even limited specificity among the symbioses that are formed between the huge array of potential host plants and the 120 or so fungi in the Glomeromycota. Do the root and fungal signals and their receptors carry the necessary information to encompass this diversity in the developmental programmes? And does the limited cortical colonization of some mutants normally blocked at the surface result from bypassing epidermal cell penetration and thus avoiding the requirement for triggered formation of a PPA? This again is for the future. Acknowledgements Our collaborations are funded by the Australian Research Council and the Natural Science Foundation of China (40225002).
References 1 Akiyama, K. et al. (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824–827 2 Nagahashi, G. and Douds, D.D. (1999) Rapid and sensitive bioassay to study signals between root exudates and arbuscular mycorrhizal fungi. Biotechnol. Tech. 13, 893–897 3 Buee, M. et al. (2000) The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol. Plant Microbe Interact. 13, 693–698
Vol.11 No.8
4 Tamasloukht, M. et al. (2003) Root factors induce mitochondrialrelated gene expression and fungal respiration during the developmental switch from asymbiosis to presymbiosis in the arbuscular mycorrhizal fungus Gigaspora rosea. Plant Physiol. 131, 1468–1478 5 Besserer, A. et al. (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol. 4 (7), e226 6 Yoder, J.I. (2001) Host–plant recognition by parasitic Scrophulariaceae. Curr. Opin. Plant Biol. 4, 359–365 7 Reizelman, A. et al. (2003) Synthesis and bioactivity of labelled germination stimulants for the isolation and identification of the strigolactone receptor. Org. Biomol. Chem. 1, 950–959 8 Genre, A. et al. (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17, 3489–3499 9 Kistner, C. et al. (2005) Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell 17, 2217–2229 10 Harrison, M.J. (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu. Rev. Microbiol. 59, 19–42 11 Karandashov, V. and Bucher, M. (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci. 10, 22–29 12 Chabaud, M. et al. (2002) Targeted inoculation of Medicago truncatula in vitro root cultures reveals MtENOD11 expression during early stages of infection by arbuscular mycorrhizal fungi. New Phytol. 156, 265–273 13 Lanfranco, L. et al. (2005) The mycorrhizal fungus Gigaspora margarita possesses a CuZn superoxide dismutase that is up-regulated during symbiosis with legume hosts. Plant Physiol. 137, 1319–1330 14 Vieweg, M.F. et al. (2005) Two genes encoding different truncated hemoglobins are regulated during root nodule and arbuscular mycorrhiza symbioses of Medicago truncatula. Planta 220, 757–766 15 Smith, S.E. and Read, D.J. (1997) Mycorrhizal Symbiosis, (Ed 2). Academic Press 16 Parniske, M. (2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr. Opin. Plant Biol. 7, 414–421 17 Smith, S.E. et al. (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol. 162, 511–524 1360-1385/$ – see front matter ß 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2006.06.008
Plant Science meetings sponsored by Trends in Plant Science Haploids in Higher Plants III 12–15 February 2006 Vienna, Austria http://www.univie.ac.at/gem/conference/haploids/ The Second Symposium on Plant Neurobiology 22–27 May 2006 Beijing, China http://plantneurobiology.ibcas.ac.cn/index.htm 2006 FASEB Summer Research Conference: ‘Mechanisms in Plant Development’ 5–9 August 2006 Vermont Academy, Saxtons River, VT, USA http://src.faseb.org/preliminary.htm www.sciencedirect.com
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