Abstract
Main conclusion
AM symbiosis did not strongly affect Arundo donax performances under salt stress, although differences in the plants inoculated with two different fungi were recorded.
The mechanisms at the basis of the improved tolerance to abiotic stresses by arbuscular mycorrhizal (AM) fungi have been investigated mainly focusing on food crops. In this work, the potential impact of AM symbiosis on the performance of a bioenergy crop, Arundo donax, under saline conditions was considered. Specifically, we tried to understand whether AM symbiosis helps this fast-growing plant, often widespread in marginal soils, withstand salt. A combined approach, involving eco-physiological, morphometric and biochemical measurements, was used and the effects of two different AM fungal species (Funneliformis mosseae and Rhizophagus irregularis) were compared. Results indicate that potted A. donax plants do not suffer permanent damage induced by salt stress, but photosynthesis and growth are considerably reduced. Since A. donax is a high-yield biomass crop, reduction of biomass might be a serious agronomical problem in saline conditions. At least under the presently experienced growth conditions, and plant–AM combinations, the negative effect of salt on plant performance was not rescued by AM fungal colonization. However, some changes in plant metabolisms were observed following AM-inoculation, including a significant increase in proline accumulation and a trend toward higher isoprene emission and higher H2O2, especially in plants colonized by R. irregularis. This suggests that AM fungal symbiosis influences plant metabolism, and plant–AM fungus combination is an important factor for improving plant performance and productivity, in presence or absence of stress conditions.
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Abbreviations
- AM:
-
Arbuscular mycorrhizal
- A N :
-
Photosynthesis
- g s :
-
Stomatal conductance
- iWUE:
-
Intrinsic water use efficiency
- MDA:
-
Malondialdehyde
- P5CS:
-
Δ1-Pyrroline-5-carboxylate synthase
References
Ahrar M, Doneva D, Koleva D et al (2015) Isoprene emission in the monocot Arundineae tribe in relation to functional and structural organization of the photosynthetic apparatus. Environ Exp Bot 119:87–95
Angelini LG, Ceccarini L, Nassi o Di Nasso N, Bonari E (2009) Comparison of Arundo donax L. and Miscanthus × giganteus in a long-term field experiment in Central Italy: analysis of productive characteristics and energy balance. Biomass Bioenergy 33:635–643
Antoniou C, Filippou P, Mylona P, Fasoula D, Ioannides I, Polidoros A, Fotopoulos V (2013) Developmental stage- and concentration-specific sodium nitroprusside application results in nitrate reductase regulation and the modification of nitrate metabolism in leaves of Medicago truncatula plants. Plant Sign Behav 8:9
Armada E, Azcón R, López-Castillo OM, Calvo Polanco M, Ruiz-Lozano JM (2015) Autochthonous arbuscular mycorrhizal fungi and Bacillus thuringiensis from a degraded Mediterranean area can be used to improve physiological traits and performance of a plant of agronomic interest under drought conditions. Plant Physiol Biochem 90:64–74
Augé RM, Toler HD, Saxton AM (2015) Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza 25:13–24
Azcón-Aguilar C, Barea JM (1997) Applying mycorrhiza biotechnology to horticulture: significance and potentials. Sci Hortic 68:1–24
Balestrini R, Chitarra W, Fotopoulos V, Ruocco M (2017a) Potential role of beneficial soil microorganisms in plant tolerance to abiotic stress. In: Lukac M, Gamboni M, Grenni P (eds) Soil biological communities and ecosystem resilience. Sustainability in plant and crop protection. Springer, New York, pp 269–283. ISBN 978-3-319-63335-0
Balestrini R, Salvioli A, Dal Molin A, Novero M, Gabelli G, Paparelli E, Marroni F, Bonfante P (2017b) Impact of an arbuscular mycorrhizal fungus versus a mixed microbial inoculum on the transcriptome reprogramming of grapevine roots. Mycorrhiza 27:417–430
Baraza E, Tauler M, Romero-Munar A, Cifre J, Gulias J (2016) Mycorrhiza-based biofertilizer application to improve the quality of Arundo donax L. plantlets. In: Barth S, Murphy-Bokern D, Kalinina O, Taylor G, Jones M (eds) Perennial biomass crops for a resource-constrained world. Springer, New York
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Beckett M, Loreto F, Velikova V, Brunetti C, Di Ferdinando M, Tattini M, Calfapietra C, Farrant JM (2012) Photosynthetic limitations and volatile and non-volatile isoprenoids in the poikilochlorophyllous resurrection plant Xerophyta humilis during dehydration and rehydration. Plant, Cell Environ 35:2061–2074
Bongi G, Loreto F (1989) Gas-exchange properties of salt-stressed olive (Olea europaea L) leaves. Plant Physiol 90:1408–1416
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254
Brilli F, Tsonev T, Mahmood T, Velikova V, Loreto F, Centritto M (2013) Ultradian variation of isoprene emission, photosynthesis, mesophyll conductance and optimum temperature sensitivity for isoprene emission in water-stressed Eucalyptus citriodora saplings. J Exp Bot 64:519–528
Brugnoli E, Björkman O (1992) Chloroplast movements in leaves: Influence on chlorophyll fluorescence and measurements of light-induced absorbance changes related to ΔpH and zeaxanthin formation. Photosyn Res 32:23–35
Chandrasekaran M, Kim K, Krishnamoorthy R, Walitang D, Sundaram S, Joe MM, Selvakumar G, Hu S, Oh S-H, Sa T (2016) Mycorrhizal symbiotic efficiency on C3 and C4 plants under salinity stress—a meta-analysis. Front Microbiol 7:1246
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 Physiol 171:1009–1023
Christou A, Manganaris GA, Papadopoulos I, Fotopoulos V (2013) Hydrogen sulfide induces systemic tolerance to salinity and non-ionic osmotic stress in strawberry plants through modification of reactive species biosynthesis and transcriptional regulation of multiple defense pathways. J Exp Bot 64:1953–1966
Coleman-Derr D, Tringe SG (2014) Building the crops of tomorrow: advantages of symbiont-based approaches to improving abiotic stress tolerance. Front Microbiol 5:283
Dahnke WC, Whitney DA (1988) Measurement of soil salinity. In: Recommended soil chemical test procedures for the North Central Region. North Central Regional Research Publication No. 221 (Revised). North Dakota Agricultural Experiment Station Bulletin 499, Fargo, pp 32–34
Dai A (2013) Increasing drought under global warming in observations and models. Nat Clim Change 3:52–58
Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379
Delfine S, Alvino A, Villani MC, Loreto F (1999) Restrictions to carbon dioxide conductance and photosynthesis in spinach leaves recovering from salt stress. Plant Physiol 119:1101–1106
Di Martino C, Delfine S, Pizzuto R, Loreto F, Fuggi A (2003) Free amino acids and glycine betaine in leaf osmoregulation of spinach responding to increasing salt stress. New Phytol 158:455–463
Dick WA, Tabatabai MA (1977) Hydrolisis of organic and inorganic phosphorus compounds added to soil. Geoderma 21:175–182
Elhindi KM, El-Din AS, Elgorban AM (2017) The impact of arbuscular mycorrhizal fungi in mitigating salt-induced adverse effects in sweet basil (Ocimum basilicum L). Saudi J Biol Sci 24:170–179
Estrada B, Aroca R, Maathuis FJM, Barea JM, Ruiz-Lozano JM (2013a) Arbuscular mycorrhizal fungi native from a Mediterranean saline area enhance maize tolerance to salinity through improved ion homeostasis. Plant, Cell Environ 36:1771–1782
Estrada B, Aroca R, Barea JM, Ruiz-Lozano JM (2013b) Native arbuscular mycorrhizal fungi isolated from a saline habitat improved maize antioxidant systems and plant tolerance to salinity. Plant Sci 201–202:42–51
Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280
Feller U, Kingston-Smith AH, Centritto M (2017) Editorial: Abiotic stresses in agroecology: a challenge for whole plant physiology. Front Environ Sci 5:13. https://doi.org/10.3389/fenvs201700013
Filippou P, Antoniou C, Yelamanchili S, Fotopoulos V (2012) NO loading: efficiency assessment of five commonly used application methods of sodium nitroprusside in Medicago truncatula plants. Plant Physiol Biochem 60:115–118
Filippou P, Bouchagier P, Skotti E et al (2014) Proline and reactive oxygen/nitrogen species metabolism is involved in the tolerant response of the invasive plant species Ailanthus altissima to drought and salinity. Environ Exp Bot 97:1–10
Fineschi S, Loreto F (2012) Leaf volatile isoprenoids: an important defensive armament in forest tree species. iForest 5:13–17
Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92
Giberti S, Funck D, Forlani G (2014) Δ1-Pyrroline-5-carboxylate reductase from Arabidopsis thaliana: stimulation or inhibition by chloride ions and feedback regulation by proline depend on whether NADPH or NADH acts as co-substrate. New Phytol 202:911–919
Haworth M, Cosentino LS, Marino G, Brunetti C, Scordia D, Testa G, Riggi E, Avola G, Loreto F, Centritto M (2017a) Physiological responses of Arundo donax ecotypes to drought: a common garden study. GCB Bioenergy 9:132–143
Haworth M, Catola S, Marino G, Brunetti C, Michelozzi M, Riggi E, Avola G, Cosentino SL, Loreto F, Centritto M (2017b) Moderate drought stress induces increased foliar dimethylsulphoniopropionate (DMSP) concentration and isoprene emission in two contrasting ecotypes of Arundo donax. Front Plant Sci 8:1016. https://doi.org/10.3389/fpls201701016
Juniper S, Abbott LK (2006) Soil salinity delays germination and limits growth of hyphae from propagules of arbuscular mycorrhizal fungi. Mycorrhiza 16:371–379
Lenoir I, Fontaine J, Sahraoui ALH (2016) Arbuscular mycorrhizal fungal responses to abiotic stresses: a review. Phytochemistry 123:4–15
Lesk C, Rowhani P, Ramankutty N (2016) Influence of extreme weather disasters on global crop production. Nature 529:84–87
Lewandowski I, Scurlock JMO, Lindvall E, Christou M (2003) The development and current status of perennial rhizomatous grasses as energy crops in the US and Europe. Biomass Bioenergy 25:335–361
Loreto F, Delfine S (2000) Emission of isoprene from salt-stressed Eucalyptus globulus leaves. Plant Physiol 123:1605–1610
Loreto F, Schnitzler JP (2010) Abiotic stresses and induced BVOCs. Trends Plant Sci 15:154–166
Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol 127:1781–1787
Loreto F, Centritto M, Chartzoulakis K (2003) Photosynthetic limitations in olive cultivars with different sensitivity to salt stress. Plant, Cell Environ 26:595–601
Marino G, Brunetti C, Tattini M, Romano A, Biasioli F, Tognetti R, Loreto F, Ferrini F, Centritto M (2017) Dissecting the role of isoprene and stress-related hormones, ABA and ethylene, signaling in split-root Populus nigra exposed to water stress. Tree Physiol. https://doi.org/10.1093/treephys/tpx083
Merlos MA, Zitka O, Vojtech A, Azcón-Aguilar C, Ferrol N (2016) The arbuscular mycorrhizal fungus Rhizophagus irregularis differentially regulates the copper response of two maize cultivars differing in copper tolerance. Plant Sci 253:68–73
Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell Environ 25:239–250
Munns R, Gilliham M (2015) Salinity tolerance of crops—what is the cost? New Phytol 208:668–673
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36
Nackley LL, Kim S-H (2015) A salt on the bioenergy and biological invasions debate: salinity tolerance of the invasive biomass feedstock Arundo donax. GCB Bioenergy 7:752–762
Navarro JM, Pérez-Tornero O, Morte A (2014) Alleviation of salt stress in citrus seedlings inoculated with arbuscular mycorrhizal fungi depends on the rootstock salt tolerance. J Plant Physiol 171:76–85
Olowu RA, Adewuyi GO, Onipede OJ, Lawal OA, Sunday OM (2015) Concentration of heavy metals in root, stem and leaves of Acalypha indica and Panicum maximum jacq from three major dumpsites in Ibadan Metropolis, South West Nigeria. Am J Chem 5:40–48
Pompeiano A, Landi M, Meloni G, Vita F, Guglielminetti L, Guidi L (2017) Allocation pattern, ion partitioning, and chlorophyll a fluorescence in Arundo donax L in responses to salinity stress. Plant Biosyst. https://doi.org/10.1080/11263504.2016.1187680
Porcel R, Aroca R, Ruíz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron Sustain Dev 32:181–200
Porras-Soriano A, Soriano-Martín ML, Porras-Piedra A, Azcón R (2009) Arbuscular mycorrhizal fungi increased growth, nutrient uptake and tolerance to salinity in olive trees under nursery conditions. J Plant Physiol 166:1350–1359
Quiroga G, Erice G, Aroca R, Chaumont F, Ruiz-Lozano JM (2017) Enhanced drought stress tolerance by the arbuscular mycorrhizal symbiosis in a drought-sensitive maize cultivar is related to a broader and differential regulation of host plant aquaporins than in a drought-tolerant cultivar. Front Plant Sci 8:1056. https://doi.org/10.3389/fpls201701056
Romero-Munar A, Del-Saz NF, Ribas-Carbó M, Flexas J, Baraza E, Florez-Sarasa I, Fernie AR, Gulías J (2017) Arbuscular mycorrhizal symbiosis with Arundo donax decreases root respiration and increases both photosynthesis and plant biomass accumulation. Plant, Cell Environ 40:1115–1126
Sánchez E, Scordia D, Lino G, Arias C, Cosentino SL, Nogués S (2015) Salinity and Water stress effects on biomass production in different Arundo donax L clones. Bioenerg Res 8:1461
Savvides A, Ali S, Tester M, Fotopoulos V (2016) Chemical priming against multiple abiotic stresses: mission possible? Trends Plant Sci 21:329–340
Smart RE, Bingham GE (1974) Rapid estimates of relative water content. Plant Physiol 53:258–260
Strizhov N, Abraham E, Okresz L, Blickling S, Zilberstein A, Schell J et al (1997) Differential expression of two P5CS genes controlling proline accumulation during salt-stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis. Plant J 12:557–569
Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97
Tattini M, Loreto F, Fini A, Guidi L, Brunetti C, Velikova V, Gori A, Ferrini F (2015) Isoprenoids and phenylpropanoids are part of the antioxidant defense orchestrated daily by drought-stressed Platanus × acerifolia plants during Mediterranean summers. New Phytol 37:1950–1964
Tauler M, Baraza E (2015) Improving the acclimatization and establishment of Arundo donax L plantlets, a promising energy crop, using a mycorrhiza-based biofertilizer. Ind Crop Prod 66:99–304
Tedeschi A, Zong L, Huang CH, Vitale L, Volpe MG, Xue X (2017) Effect of salinity on growth parameters, soil water potential and ion composition in Cucumis melo cv Huanghemi in North-Western China. J Agro Crop Sci 203:41–55
Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Estimation of VA mycorrhizal infection levels Research for methods having a functional significance. Proceedings of the first European symposium, physiological and genetical aspects of mycorrhizae. Dijon Centre National de la Recherche Scientifique, Dijon; Institut National de la Recherche Agronomique, Dijon; Station d’Amelioration des Plantes, Paris, pp 217–221
Unno H, Maeda Y, Yamamoto S, Okamoto M, Takenaga H (2002) Relationship between salt tolerance and Ca2+ retention among plant species. Jpn J Soil Sci Plant Nutr 73:715–718
Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5:283–291
Walder F, van der Heijden MGA (2015) Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nat Plants. https://doi.org/10.1038/nplants2015159
Wang W-G, Li R, Liu B et al (2011) Effects of low nitrogen and drought stresses on proline synthesis of Jatropha curcas seedling. Acta Physiol Plant 33:1591–1595
Yang S, Zhang Z, Xue Y et al (2014) Arbuscular mycorrhizal fungi increase salt tolerance of apple seedlings. Bot Stud 55:70. https://doi.org/10.1186/s40529-014-0070-6
Yooyongwech S, Samphumphuang T, Tisarum R, Theerawitaya C, Cha-um S (2016) Arbuscular mycorrhizal fungi (AMF) improved water deficit tolerance in two different sweet potato genotypes involves osmotic adjustments via soluble sugar and free proline. Sci Hortic 198:107–117
Zall DM, Fisher D, Garner MQ (1956) Photometric determination of chlorides in water. Anal Chem 28:1655–1668
Acknowledgements
This work was funded by Progetto Premiale 2012 CNR-Biofuels and third-generation biorefinery integrated with the territory. The authors thank Maria Teresa della Beffa for the help during plant preparation and growth.
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425_2017_2808_MOESM1_ESM.jpg
Supplementary material 1 Fig. S1 A comparative picture of A. donax plants non-inoculated (C) and inoculated with two different AM fungal species (Fm or Ri, i.e., F. mosseae and R. irregularis) under non-stressed (NS) and salt-stressed condition (SS), 4 months after AM-inoculation and 25 days after beginning the NaCl treatment (JPEG 161 kb)
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Pollastri, S., Savvides, A., Pesando, M. et al. Impact of two arbuscular mycorrhizal fungi on Arundo donax L. response to salt stress. Planta 247, 573–585 (2018). https://doi.org/10.1007/s00425-017-2808-3
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DOI: https://doi.org/10.1007/s00425-017-2808-3