PLANT SIGNALING & BEHAVIOR 2016, VOL. 11, NO. 7, e1197468 (3 pages) http://dx.doi.org/10.1080/15592324.2016.1197468
ARTICLE ADDENDUM
Arbuscular mycorrhizal symbiosis-mediated tomato tolerance to drought Walter Chitarra, Biancaelena Maserti, Giorgio Gambino, Emilio Guerrieri, and Raffaella Balestrini Institute for Sustainable Plant Protection (IPSP)–CNR, Torino, Italy
ABSTRACT
ARTICLE HISTORY
A multidisciplinary approach, involving eco-physiological, morphometric, biochemical and molecular analyses, has been used to study the impact of two different AM fungi, i.e. Funneliformis mosseae and Rhizophagus intraradices, on tomato response to water stress. Overall, results show that AM symbiosis positively affects the tolerance to drought in tomato with a different plant response depending on the involved AM fungal species.
Received 16 May 2016 Accepted 27 May 2016
During the last decades, a variety of strategies have been deployed to improve stress tolerance in crops, including traditional selection methods and genetic engineering. The use of root-associated microbial communities to enhance plant tolerance to abiotic stresses has been explored in recent years.1 An important role as bio-fertilizing microorganisms is played by arbuscular mycorrhizal (AM) fungi thanks to their ability to establish mutualistic symbioses with the roots of most crops.2 These symbiotic fungi are considered to be essential elements for plant nutrition, while they receive the products of photosynthesis in turn. Their hyphae can extend for many meters in the soil, helping the host plant to reach water and nutrients.2 Furthermore, these fungi have been described to improve plant tolerance to important abiotic environmental conditions such as drought, salt stress and cold.3,4,5,6,7 We have used a multidisciplinary approach, involving eco-physiological, morphometric, biochemical and molecular analyses, to study the impact of 2 different AM fungi, i.e., Funneliformis mosseae and Rhizophagus intraradices, on tomato response to water stress.8 The cooperation in AM interactions is related to the partners involved in the symbiosis, and depends on several factors, including environmental conditions and functional diversity.9 Overall, our experimental results show that AM symbiosis positively affects the tolerance to drought in tomato (e.g., improving intrinsic water use efficiency, iWUE) and that R. intraradices seems to be more efficient in the induction of resilience to water stress (WS), at least in the considered tomato cultivar. One noteworthy result regards the role of abscisic acid (ABA), which is an important hormone that regulates plant growth and development and responses to abiotic stresses, such as drought and high salinity.10 We observed that under severe WS (-1.3 MPa),
KEYWORDS
AM fungi; aquaporins; abiotic stress tolerance; abscisic acid (ABA); iWUE; stomatal density; water stress
AM-colonized tomato (AM+) showed a significant lower level of ABA both in roots and leaves compared with uncolonized plants (AM-), suggesting that non-mycorrhizal plants probably faced more intense drought stress than mycorrhizal ones, and produce/accumulate more ABA. To deeply understand the role of ABA in our conditions, the expression of ABA-related genes has also been analyzed, i.e., the ABA-biosynthetic gene LeNCED1 and 3 genes (LePYL9, LePP2C, LeSnR2K) related to ABA signaling mechanisms (Fig. 1). Although this aspect has to be further investigated, taken together, our results suggest that in AM + plants upon WS the stomata closing is probably not regulated by ABA-mediated mechanisms, but it could be rather induced by passive hydraulic-mediated mechanisms. In woody plants, such as grapevine, it has been demonstrated that stomata closure can be driven by both active (ABAmediated) and/or passive (hydraulic-mediated) mechanisms.11 Moreover, in addition to opening and closing the stomata, plants may exert control over their gas exchange rates by varying stomata density in new leaves.12 We have demonstrated that the presence of AM fungi determines a higher stomatal density, especially in plants colonized by R. intraradices.8 Since a higher stomatal density can increase the plant CO2 absorption capacity, these data are in agreement with the significantly higher photosynthetic rates (AN) measured in AM+ plants both under not stressed (NS) and WS conditions in respect to uncolonized plants, which are also directly correlated with their relative iWUE values.8 In order to further clarify these aspects, we also evaluated the expression in new developing tomato leaves, of genes putatively involved in stomatal development regulation (Fig. 1), showing that they are differentially expressed in the presence of the AM fungi. Since the physiological responses of
CONTACT Raffaella Balestrini [email protected] IPSP-CNR, Torino Unit, Viale Mattioli Torino, Italy Addendum to: Chitarra W, Pagliarani C, Maserti B, Lumini E, Siciliano I, Cascone P, Schubert A, Gambino G, Balestrini R, Guerrieri E (2016) Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. Plant Physiology 171:1009-1023; http://dx.doi.org/10.1104/pp.16.00307. © 2016 Taylor & Francis Group, LLC
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W. CHITARRA ET AL.
Figure 1. Modulation of the expression of selected genes induced by AM symbiosis in tomato plants subjected to water stress conditions with respect to uncolonised (AM-) plants (adapted from Chitarra et al. 2016).
plants to drought stress are also regulated by the expression of genes encoding aquaporins (AQPs),13 the expression of several plants and fungal AQPs was considered. It has been already reported that AM symbiosis may regulate the expression of AQP genes, improving root hydraulic conductivity, plant water status and drought tolerance.14,15,16,17,18 Under WS, our recent results show that LeNIP3.1 was significantly more expressed in AM fungal-colonized roots (Fig. 1), with higher values in the presence of R. intraradices. This results is in agreement with the specifically expression of a NIP aquaporin gene (LjNIP1) in the root cells containing arbuscules, which represent the key structure of a functional symbiosis, as previously reported in Lotus japonicus.16 Since AM fungal aquaporin can also have a role in drought tolerance stimulated by AM symbiosis,19,20 the expression of 2 R. intraradices AQP genes have also been evaluated, showing a significant up-regulation for one of the 2 considered genes (GintAQPF2), in agreement with previous data.20 This contemporaneous induction of both fungal and plant AQP genes in these experiments is a confirmation that the 2 symbionts strictly cooperate to regulate the mycorrhizal drought-stress response. Furthermore, a role of host transpiration and fungal AQP in long-distance fungal polyphosphate (polyP) translocation, and consequently on fungal phosphate (Pi) delivery, has been recently proposed.21 The data obtained in our recent publication,8 showing a change in plant performance in the presence of the AM fungi under WS, offer new insights for understanding the molecular and physiological mechanisms underlying the tomato tolerance to drought as mediated by the AM fungi. Together with experiments performed by several researchers in the last years, they also open new perspectives in the exploitation of AM symbiosis to enhance crop
tolerance to abiotic stress in a scenario of climate change. The evaluation of the nutrient use efficiency, and the regulation of the genes involved in nutrient transport, under drought conditions could represent further steps of this research.
Disclosure of potential confllicts of interest No potential conflicts of interest were disclosed.
Funding This work was supported by the AQUA Project (Progetto Premiale CNR).
References 1. Coleman-Derr D, Tringe SG. Building the crops of tomorrow: advantages of symbiont-based approaches to improving abiotic stress tolerance. Front Microbiol 2014; 5:283; PMID:24936202; http://dx.doi.org/ 10.3389/fmicb.2014.00283 2. Bucher M, Hause B, Krajinski F, K€ uster H. Through the doors of perception to function in arbuscular mycorrhizal symbioses. New Phytol 2014; 204:833-840; PMID:25414918; http://dx.doi.org/10.1111/ nph.12862 3. Rapparini F, Pe~ nuelas J. Mycorrhizal fungi to alleviate drought stress on plant growth. In: Use of microbes for the alleviation of soil stresses: Springer, New York. Miransari M (ed), Vol 1; 2014 4. Estrada B, Aroca R, Maathuis FJM, Barea JM, Ruiz-Lozano JM. Arbuscular mycorrhizal fungi native from a Mediterranean saline area enhance maize tolerance to salinity through improved ion homeostasis. Plant Cell Environ 2013; 36: 1771-1782; PMID:23421735; http:// dx.doi.org/10.1111/pce.12082 5. Estrada B, Aroca R, Barea JM, Ruiz-Lozano JM. Native arbuscular mycorrhizal fungi isolated from a saline habitat improved maize antioxidant systems and plant tolerance to salinity. Plant Sci
PLANT SIGNALING & BEHAVIOR
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2013; 201-202:42-51; PMID:23352401; http://dx.doi.org/10.1016/j. plantsci.2012.11.009 Pedranzani H, Tavecchio N, Gutierrez M, Garbero M, Porcel R, RuizLozano JM. Differential effects of cold stress on the antioxidant response of mycorrhizal and non-mycorrhizal Jatropha curcas (L.) plants. J Agr Sci 2015; 7:35-43; http/dx.doi.org/10.5539/jas.v7n8pxx Pedranzani H, Rodrıguez-Rivera M, Gutierrez M, Porcel R, Hause B, Ruiz-Lozano JM. Arbuscular mycorrhizal symbiosis regulates physiology and performance of Digitaria eriantha plants subjected to abiotic stresses by modulating antioxidant and jasmonate levels. Mycorrhiza 2016; 26:141-52; PMID:26184604; http://dx.doi.org/10.1007/s00572015-0653-4 Chitarra W, Pagliarani C, Maserti B, Lumini E, Siciliano I, Cascone P, Schubert A, Gambino G, Balestrini R, Guerrieri E. Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. Plant Physiol 2016; 171:1-15; PMID:27208301; http://dx. doi.org/10.1104/pp.16.003079 Walder F, van der Heijden, MGA. Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nat Plants 2015; 1:15159; PMID:27251530; http://dx.doi.org/10.1038/nplants.2015.159 Lim CW, Baek W, Jung J, Kim J-H, Lee SC. Function of ABA in stomatal defense against biotic and drought stresses. Int J Mol Sci 2015; 16:1525170; PMID:26154766; http://dx.doi.org/10.3390/ijms16071525111 Tombesi S, Nardini A, Frioni T, Soccolini M, Zadra C, Farinelli D, Poni S, Palliotti A. Stomatal closure is induced by hydraulic signals and maintained by ABA in drought-stressed grapevine. Sci Rep 2015; 5:12449; PMID:26207993;http://dx.doi.org/10.1038/srep12449 Casson S, Gray JE. Influence of environmental factors on stomatal development. New Phytol 2008; 178:9-23; PMID:18266617; http://dx. doi.org/10.1111/j.1469-8137.2007.02351.x Maurel C, Boursiac Y, Luu DT, Santoni V, Shahzad Z, Verdoucq L. Aquaporins in plants. Physiol Rev 2015; 95:1321-58; PMID:26336033; http://dx.doi.org/10.1152/physrev.00008.2015 Ruiz-Lozano JM, Alguacil MM, Barzana G, Vernieri P, Aroca R. Exogenous ABA accentuates the differences in root hydraulic properties between mycorrhizal and non mycorrhizal maize plants
15.
16.
17.
18.
19.
20.
21.
e1197468-3
through regulation of PIP aquaporins. Plant Mol Biol 2009; 70:565-79; PMID:19404751; http://dx.doi.org/10.1007/s11103-0099492-z Aroca R, Porcel R, Ruiz-Lozano JM. Regulation of root water uptake under abiotic stress conditions. J Exp Bot 2012; 63:43-57; PMID:21914658; http://dx.doi.org/10.1093/jxb/err26616 Giovannetti M, Balestrini R, Volpe V, Guether M, Straub D, Costa A, Ludewig U, Bonfante P. Two putative-aquaporin genes are differentially expressed during arbuscular mycorrhizal symbiosis in Lotus japonicus. BMC Plant Biol 2012; 12:186; PMID:23046713; http://dx. doi.org/10.1186/1471-2229-12-186 Barzana G, Aroca R, Bienert GP, Chaumont F, Ruız-Lozano JM. New insights into the regulation of aquaporins by the arbuscular mycorrhizal symbiosis in maize plants under drought stress and possible implications for plant performance. Mol Plant Microbe Interct 2014; 27:349-63; PMID:24593244; http://dx.doi.org/10.1094/MPMI-09-130268-R Barzana G, Aroca R, Ruiz-Lozano JM. Localized and non-localized effects of arbuscular mycorrhizal symbiosis on accumulation of osmolytes and aquaporins and on antioxidant systems in maize plants subjected to total or partial root drying. Plant Cell Environ 2015; 38:1613-27; PMID:25630435; http://dx.doi.org/10.1111/pce.12507 Aroca R, Bago A, Sutka M, Paz JA, Cano C, Amodeo G, Ruiz-Lozano JM. Expression analysis of the first arbuscular mycorrhizal fungi aquaporin described reveals concerted gene expression between salt-stressed and nonstressed mycelium. Mol Plant Microbe Interact 2009; 22:116978; PMID:19656051; http://dx.doi.org/10.1094/MPMI-22-9-1169 Li T, Hu YJ, Hao ZP, Li H, Wang YS, Chen BD. First cloning and characterization of two functional aquaporin genes from an arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 2013; 197:617-30; PMID:23157494; http://dx.doi.org/10.1111/nph.12011 Kikuchi Y, Hijikata N, Ohtomo R, Handa Y, Kawaguchi M, Saito K, Masuta C, Ezawa T. Aquaporin-mediated long-distance polyphosphate translocation directed towards the host in arbuscular mycorrhizal symbiosis: application of virus-induced gene silencing. New Phytol 2016; http://dx.doi.org/10.1111/nph.14016
ARTICLE ADDENDUM
Arbuscular mycorrhizal symbiosis-mediated tomato tolerance to drought Walter Chitarra, Biancaelena Maserti, Giorgio Gambino, Emilio Guerrieri, and Raffaella Balestrini Institute for Sustainable Plant Protection (IPSP)–CNR, Torino, Italy
ABSTRACT
ARTICLE HISTORY
A multidisciplinary approach, involving eco-physiological, morphometric, biochemical and molecular analyses, has been used to study the impact of two different AM fungi, i.e. Funneliformis mosseae and Rhizophagus intraradices, on tomato response to water stress. Overall, results show that AM symbiosis positively affects the tolerance to drought in tomato with a different plant response depending on the involved AM fungal species.
Received 16 May 2016 Accepted 27 May 2016
During the last decades, a variety of strategies have been deployed to improve stress tolerance in crops, including traditional selection methods and genetic engineering. The use of root-associated microbial communities to enhance plant tolerance to abiotic stresses has been explored in recent years.1 An important role as bio-fertilizing microorganisms is played by arbuscular mycorrhizal (AM) fungi thanks to their ability to establish mutualistic symbioses with the roots of most crops.2 These symbiotic fungi are considered to be essential elements for plant nutrition, while they receive the products of photosynthesis in turn. Their hyphae can extend for many meters in the soil, helping the host plant to reach water and nutrients.2 Furthermore, these fungi have been described to improve plant tolerance to important abiotic environmental conditions such as drought, salt stress and cold.3,4,5,6,7 We have used a multidisciplinary approach, involving eco-physiological, morphometric, biochemical and molecular analyses, to study the impact of 2 different AM fungi, i.e., Funneliformis mosseae and Rhizophagus intraradices, on tomato response to water stress.8 The cooperation in AM interactions is related to the partners involved in the symbiosis, and depends on several factors, including environmental conditions and functional diversity.9 Overall, our experimental results show that AM symbiosis positively affects the tolerance to drought in tomato (e.g., improving intrinsic water use efficiency, iWUE) and that R. intraradices seems to be more efficient in the induction of resilience to water stress (WS), at least in the considered tomato cultivar. One noteworthy result regards the role of abscisic acid (ABA), which is an important hormone that regulates plant growth and development and responses to abiotic stresses, such as drought and high salinity.10 We observed that under severe WS (-1.3 MPa),
KEYWORDS
AM fungi; aquaporins; abiotic stress tolerance; abscisic acid (ABA); iWUE; stomatal density; water stress
AM-colonized tomato (AM+) showed a significant lower level of ABA both in roots and leaves compared with uncolonized plants (AM-), suggesting that non-mycorrhizal plants probably faced more intense drought stress than mycorrhizal ones, and produce/accumulate more ABA. To deeply understand the role of ABA in our conditions, the expression of ABA-related genes has also been analyzed, i.e., the ABA-biosynthetic gene LeNCED1 and 3 genes (LePYL9, LePP2C, LeSnR2K) related to ABA signaling mechanisms (Fig. 1). Although this aspect has to be further investigated, taken together, our results suggest that in AM + plants upon WS the stomata closing is probably not regulated by ABA-mediated mechanisms, but it could be rather induced by passive hydraulic-mediated mechanisms. In woody plants, such as grapevine, it has been demonstrated that stomata closure can be driven by both active (ABAmediated) and/or passive (hydraulic-mediated) mechanisms.11 Moreover, in addition to opening and closing the stomata, plants may exert control over their gas exchange rates by varying stomata density in new leaves.12 We have demonstrated that the presence of AM fungi determines a higher stomatal density, especially in plants colonized by R. intraradices.8 Since a higher stomatal density can increase the plant CO2 absorption capacity, these data are in agreement with the significantly higher photosynthetic rates (AN) measured in AM+ plants both under not stressed (NS) and WS conditions in respect to uncolonized plants, which are also directly correlated with their relative iWUE values.8 In order to further clarify these aspects, we also evaluated the expression in new developing tomato leaves, of genes putatively involved in stomatal development regulation (Fig. 1), showing that they are differentially expressed in the presence of the AM fungi. Since the physiological responses of
CONTACT Raffaella Balestrini [email protected] IPSP-CNR, Torino Unit, Viale Mattioli Torino, Italy Addendum to: Chitarra W, Pagliarani C, Maserti B, Lumini E, Siciliano I, Cascone P, Schubert A, Gambino G, Balestrini R, Guerrieri E (2016) Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. Plant Physiology 171:1009-1023; http://dx.doi.org/10.1104/pp.16.00307. © 2016 Taylor & Francis Group, LLC
e1197468-2
W. CHITARRA ET AL.
Figure 1. Modulation of the expression of selected genes induced by AM symbiosis in tomato plants subjected to water stress conditions with respect to uncolonised (AM-) plants (adapted from Chitarra et al. 2016).
plants to drought stress are also regulated by the expression of genes encoding aquaporins (AQPs),13 the expression of several plants and fungal AQPs was considered. It has been already reported that AM symbiosis may regulate the expression of AQP genes, improving root hydraulic conductivity, plant water status and drought tolerance.14,15,16,17,18 Under WS, our recent results show that LeNIP3.1 was significantly more expressed in AM fungal-colonized roots (Fig. 1), with higher values in the presence of R. intraradices. This results is in agreement with the specifically expression of a NIP aquaporin gene (LjNIP1) in the root cells containing arbuscules, which represent the key structure of a functional symbiosis, as previously reported in Lotus japonicus.16 Since AM fungal aquaporin can also have a role in drought tolerance stimulated by AM symbiosis,19,20 the expression of 2 R. intraradices AQP genes have also been evaluated, showing a significant up-regulation for one of the 2 considered genes (GintAQPF2), in agreement with previous data.20 This contemporaneous induction of both fungal and plant AQP genes in these experiments is a confirmation that the 2 symbionts strictly cooperate to regulate the mycorrhizal drought-stress response. Furthermore, a role of host transpiration and fungal AQP in long-distance fungal polyphosphate (polyP) translocation, and consequently on fungal phosphate (Pi) delivery, has been recently proposed.21 The data obtained in our recent publication,8 showing a change in plant performance in the presence of the AM fungi under WS, offer new insights for understanding the molecular and physiological mechanisms underlying the tomato tolerance to drought as mediated by the AM fungi. Together with experiments performed by several researchers in the last years, they also open new perspectives in the exploitation of AM symbiosis to enhance crop
tolerance to abiotic stress in a scenario of climate change. The evaluation of the nutrient use efficiency, and the regulation of the genes involved in nutrient transport, under drought conditions could represent further steps of this research.
Disclosure of potential confllicts of interest No potential conflicts of interest were disclosed.
Funding This work was supported by the AQUA Project (Progetto Premiale CNR).
References 1. Coleman-Derr D, Tringe SG. Building the crops of tomorrow: advantages of symbiont-based approaches to improving abiotic stress tolerance. Front Microbiol 2014; 5:283; PMID:24936202; http://dx.doi.org/ 10.3389/fmicb.2014.00283 2. Bucher M, Hause B, Krajinski F, K€ uster H. Through the doors of perception to function in arbuscular mycorrhizal symbioses. New Phytol 2014; 204:833-840; PMID:25414918; http://dx.doi.org/10.1111/ nph.12862 3. Rapparini F, Pe~ nuelas J. Mycorrhizal fungi to alleviate drought stress on plant growth. In: Use of microbes for the alleviation of soil stresses: Springer, New York. Miransari M (ed), Vol 1; 2014 4. Estrada B, Aroca R, Maathuis FJM, Barea JM, Ruiz-Lozano JM. Arbuscular mycorrhizal fungi native from a Mediterranean saline area enhance maize tolerance to salinity through improved ion homeostasis. Plant Cell Environ 2013; 36: 1771-1782; PMID:23421735; http:// dx.doi.org/10.1111/pce.12082 5. Estrada B, Aroca R, Barea JM, Ruiz-Lozano JM. Native arbuscular mycorrhizal fungi isolated from a saline habitat improved maize antioxidant systems and plant tolerance to salinity. Plant Sci
PLANT SIGNALING & BEHAVIOR
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2013; 201-202:42-51; PMID:23352401; http://dx.doi.org/10.1016/j. plantsci.2012.11.009 Pedranzani H, Tavecchio N, Gutierrez M, Garbero M, Porcel R, RuizLozano JM. Differential effects of cold stress on the antioxidant response of mycorrhizal and non-mycorrhizal Jatropha curcas (L.) plants. J Agr Sci 2015; 7:35-43; http/dx.doi.org/10.5539/jas.v7n8pxx Pedranzani H, Rodrıguez-Rivera M, Gutierrez M, Porcel R, Hause B, Ruiz-Lozano JM. Arbuscular mycorrhizal symbiosis regulates physiology and performance of Digitaria eriantha plants subjected to abiotic stresses by modulating antioxidant and jasmonate levels. Mycorrhiza 2016; 26:141-52; PMID:26184604; http://dx.doi.org/10.1007/s00572015-0653-4 Chitarra W, Pagliarani C, Maserti B, Lumini E, Siciliano I, Cascone P, Schubert A, Gambino G, Balestrini R, Guerrieri E. Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. Plant Physiol 2016; 171:1-15; PMID:27208301; http://dx. doi.org/10.1104/pp.16.003079 Walder F, van der Heijden, MGA. Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nat Plants 2015; 1:15159; PMID:27251530; http://dx.doi.org/10.1038/nplants.2015.159 Lim CW, Baek W, Jung J, Kim J-H, Lee SC. Function of ABA in stomatal defense against biotic and drought stresses. Int J Mol Sci 2015; 16:1525170; PMID:26154766; http://dx.doi.org/10.3390/ijms16071525111 Tombesi S, Nardini A, Frioni T, Soccolini M, Zadra C, Farinelli D, Poni S, Palliotti A. Stomatal closure is induced by hydraulic signals and maintained by ABA in drought-stressed grapevine. Sci Rep 2015; 5:12449; PMID:26207993;http://dx.doi.org/10.1038/srep12449 Casson S, Gray JE. Influence of environmental factors on stomatal development. New Phytol 2008; 178:9-23; PMID:18266617; http://dx. doi.org/10.1111/j.1469-8137.2007.02351.x Maurel C, Boursiac Y, Luu DT, Santoni V, Shahzad Z, Verdoucq L. Aquaporins in plants. Physiol Rev 2015; 95:1321-58; PMID:26336033; http://dx.doi.org/10.1152/physrev.00008.2015 Ruiz-Lozano JM, Alguacil MM, Barzana G, Vernieri P, Aroca R. Exogenous ABA accentuates the differences in root hydraulic properties between mycorrhizal and non mycorrhizal maize plants
15.
16.
17.
18.
19.
20.
21.
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through regulation of PIP aquaporins. Plant Mol Biol 2009; 70:565-79; PMID:19404751; http://dx.doi.org/10.1007/s11103-0099492-z Aroca R, Porcel R, Ruiz-Lozano JM. Regulation of root water uptake under abiotic stress conditions. J Exp Bot 2012; 63:43-57; PMID:21914658; http://dx.doi.org/10.1093/jxb/err26616 Giovannetti M, Balestrini R, Volpe V, Guether M, Straub D, Costa A, Ludewig U, Bonfante P. Two putative-aquaporin genes are differentially expressed during arbuscular mycorrhizal symbiosis in Lotus japonicus. BMC Plant Biol 2012; 12:186; PMID:23046713; http://dx. doi.org/10.1186/1471-2229-12-186 Barzana G, Aroca R, Bienert GP, Chaumont F, Ruız-Lozano JM. New insights into the regulation of aquaporins by the arbuscular mycorrhizal symbiosis in maize plants under drought stress and possible implications for plant performance. Mol Plant Microbe Interct 2014; 27:349-63; PMID:24593244; http://dx.doi.org/10.1094/MPMI-09-130268-R Barzana G, Aroca R, Ruiz-Lozano JM. Localized and non-localized effects of arbuscular mycorrhizal symbiosis on accumulation of osmolytes and aquaporins and on antioxidant systems in maize plants subjected to total or partial root drying. Plant Cell Environ 2015; 38:1613-27; PMID:25630435; http://dx.doi.org/10.1111/pce.12507 Aroca R, Bago A, Sutka M, Paz JA, Cano C, Amodeo G, Ruiz-Lozano JM. Expression analysis of the first arbuscular mycorrhizal fungi aquaporin described reveals concerted gene expression between salt-stressed and nonstressed mycelium. Mol Plant Microbe Interact 2009; 22:116978; PMID:19656051; http://dx.doi.org/10.1094/MPMI-22-9-1169 Li T, Hu YJ, Hao ZP, Li H, Wang YS, Chen BD. First cloning and characterization of two functional aquaporin genes from an arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 2013; 197:617-30; PMID:23157494; http://dx.doi.org/10.1111/nph.12011 Kikuchi Y, Hijikata N, Ohtomo R, Handa Y, Kawaguchi M, Saito K, Masuta C, Ezawa T. Aquaporin-mediated long-distance polyphosphate translocation directed towards the host in arbuscular mycorrhizal symbiosis: application of virus-induced gene silencing. New Phytol 2016; http://dx.doi.org/10.1111/nph.14016
