Improvement of Salt Tolerance in Rice Plants by Arbuscular Mycorrhizal Symbiosis

  1. Ruiz-Lozano, Juan Manuel 1
  2. Porcel, Rosa 12
  3. Calvo-Polanco, Mónica 3
  4. Aroca, Ricardo 1
  1. 1 Departamento de Microbiología del Suelo y Sistemas SimbióticosEstación Experimental del Zaidín (CSIC), Granada, Spain
  2. 2 Instituto Universitario de Conservación y Mejora de la Agrodiversidad Valenciana (COMAV), Universidad Politécnica de Valencia, Valencia, Spain
  3. 3 Biochimie et Physiologie Moléculaire des Plantes, SupAgro/INRA UMR 5004, Montpellier Cedex 2, France
Libro:
Root Biology
  1. Bhoopander Giri (coord.)
  2. Ram Prasad (coord.)
  3. Ajit Varma (coord.)

Editorial: Srpinger

ISSN: 1613-3382 2196-4831

ISBN: 9783319759098 9783319759104

Año de publicación: 2018

Páginas: 259-279

Tipo: Capítulo de Libro

DOI: 10.1007/978-3-319-75910-4_10 GOOGLE SCHOLAR lock_openAcceso abierto editor

Resumen

Rice (Oryza sativa L.) is the most important source of food for more than half of the world population, with salinity having a remarkable negative impact on its productivity worldwide. An important challenge for researchers is to achieve strategies to make rice plants more tolerant and to improve its productivity under salinity, in order to cope with reduced food production due to soil salinization. Several studies have shown that the arbuscular mycorrhizal (AM) symbiosis can alleviate salt stress in different host plant species. In this chapter, we summarize results obtained in relation to the amelioration of salt stress tolerance by the AM symbiosis in a crop of such importance for human nourishment as rice. Results showed that AM rice plants had a higher photochemical efficiency for CO2 fixation and solar energy utilization, and this increases plant salt tolerance by preventing the injury to the photosystems reaction centers and by allowing a better utilization of light energy in photochemical processes. On the other hand, in aerial plant tissues, the AM symbiosis may favor Na+ extrusion from cytoplasm, its sequestration into the vacuole, the unloading of Na+ from the xylem, and its recirculation from photosynthetic organs to roots, through regulation of OsSOS1, OsNHX3, OsHKT2;1 and OsHKT1;5 genes. The AM symbiosis also improves root hydraulic conductivity under saline conditions, and this may be due to enhanced symplastic and apoplastic radial water flow in rice roots, mediated by the induction of specific aquaporin isoforms and also by the additional water-absorbing surface of AM fungal hyphae. In addition to the above effects, the antioxidant capacity of rice plants seems to be also enhanced by the AM symbiosis, as evidenced by a reduced oxidative damage to lipids in AM plants subjected to salinity, by the enhanced activity of some antioxidant enzymes, or by the accumulation of antioxidant compounds such as glutathione.

Referencias bibliográficas

  • Aharon R, Shahak Y, Wininger S, Bendov R, Kapulnik Y, Galili G (2003) Overexpression of a plasma membrane aquaporins in transgenic tobacco improves plant vigour under favourable growth conditions but not under drought or salt stress. Plant Cell 15:439–447
  • Alguacil MM, Hernández JA, Caravaca F, Portillo B, Roldán A (2003) Antioxidant enzyme activities in shoots from three mycorrhizal shrub species afforested in a degraded semi-arid soil. Physiol Plant 118:562–570
  • Allen MF (2009) Bidirectional water flows through the soil-fungal-plant mycorrhizal continuum. New Phytol 182:290–293
  • Aroca R, Porcel R, Ruiz-Lozano JM (2007) How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol 173:808–816
  • Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42
  • Augé RM, Toler HD, Saxton AM (2014) Arbuscular mycorrhizal symbiosis and osmotic adjustment in response to NaCl stress: a meta-analysis. Front Plant Sci 5:562
  • Bagheri V, Shamshiri MH, Shirani H, Roosta HR (2011) Effect of mycorrhizal inoculation on ecophysiological responses of pistachio plants grown under different water regimes. Photosynthetica 49:531–538
  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113
  • Bárzana G, Aroca R, Paz JA, Chaumont F, Martinez-Ballesta MC, Carvajal M, Ruiz-Lozano JM (2012) Arbuscular mycorrhizal symbiosis increases relative apoplastic water flow in roots of the host plant under both well-watered and drought stress conditions. Ann Bot 109:1009–1017
  • Bárzana G, Aroca R, Bienert P, Chaumont F, Ruiz-Lozano JM (2014) 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 Interact 27:349–363
  • Bárzana G, Aroca R, Ruiz-Lozano JM (2015) 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 38:1613–1627
  • Bienert GP, Désirée-Bienert M, Jahn TP, Boutry M, Chaumont F (2011) Solanaceae XIPs are plasma membrane aquaporins that facilitate the transport of many uncharged substrates. Plant J 66:306–317
  • Birhane E, Sterck FJ, Fetene M, Bongers F, Kuyper TW (2012) Arbuscular mycorrhizal fungi enhance photosynthesis, water use efficiency, and growth of frankincense seedlings under pulsed water availability conditions. Oecologia 169:895–904
  • Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170:489–504
  • Boursiac Y, Chen S, Luu D-T, Sorieul M, van den Dries N, Maurel C (2005) Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol 139:790–805
  • Cabot C, Sibole JV, Barceló J, Poschenrieder C (2014) Lessons from crop plants struggling with salinity. Plant Sci 226:2–13
  • Callaway E (2014) Domestication: the birth of rice. Nature 514:S58
  • Carvajal M, Cerdá A, Martínez V (2000) Does calcium ameliorate the negative effect of NaCl on melon root water transport by regulating water channel activity? New Phytol 145:439–447
  • Chen Z, Zhou MX, Newman IA, Mendham NJ, Zhang GP, Shabala S (2007) Potassium and sodium relations in salinized barley as a basis of differential salt tolerance. Funct Plant Biol 34:150–162
  • Chen YY, Hu CY, Xiao JX (2014) Effects of arbuscular mycorrhizal inoculation on the growth, zinc distribution and photosynthesis of two citrus cultivars grown in low-zinc soil. Trees 28:1427–1436
  • Cuin TA, Bose J, Stefano G, Jha D, Tester M, Mancuso S, Shabala S (2011) Assessing the role of root plasma membrane and tonoplast Na+/H+ exchangers in salinity tolerance in wheat: in planta quantification methods. Plant Cell Environ 34:947–961
  • Davenport RJ, Muñoz-Mayor A, Jha D, Essah PA, Rus A, Tester M (2007) The Na+ transporter AtHKT1;1 controls retrieval of Na+ from the xylem in Arabidopsis. Plant Cell Environ 30:497–507
  • Duarte B, Santos D, Marques JC, Cacador I (2013) Ecophysiological adaptations of two halo-phytes to salt stress: photosynthesis, PS II photochemistry and anti-oxidant feedback—implications for resilience in climate change. Plant Physiol Biochem 67:178–188
  • Estrada B, Aroca R, Maathuis FJM, Barea JM, Ruiz-Lozano JM (2013) Arbuscular mycorrhizal fungi native from a Mediterranean saline area enhance maize tolerance to salinity through improved ion homeostasis. Plant Cell Environ 36:1771–1182
  • Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280
  • Evelin H, Giri B, Kapoor R (2012) Contribution of Glomus intraradices inoculation to nutrient acquisition and mitigation of ionic imbalance in NaCl-stressed Trigonella foenum-graecum. Mycorrhiza 22:203–217
  • Evelin H, Giri B, Kapoor R (2013) Ultrastructural evidence for AMF mediated salt stress mitigation in Trigonella foenum-graecum. Mycorrhiza 23:71–86
  • FAO (2005) Global network on integrated soil management for sustainable use of salt-affected soils. FAO Land and Plant Nutrition Management Service, Rome, Italy. http://www.fao.org/ag/agl/agll/spush
  • Fukuda A, Nakamura A, Hara N, Toki S, Tanaka Y (2011) Molecular and functional analyses of rice NHX-type Na+/H+ antiporter genes. Planta 233:175–188
  • Galmés J, Medrano H, Flexas J (2007) Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms. New Phytol 175:81–93
  • Garciadeblás B, Senn ME, Banuelos MA, Rodriguez-Navarro A (2003) Sodium transport and HKT transporters: the rice model. Plant J 34:788–801
  • Giri B, Mukerji KG (2004) Mycorrhizal inoculant alleviates salt stress in Sesbania aegyptiaca and Sesbania grandiflora under field conditions: evidence for reduced sodium and improved magnesium uptake. Mycorrhiza 14:307–312
  • Giri B, Kapoor R, Mukerji KG (2007) Improved tolerance of Acacia nilotica to salt stress by arbuscular mycorrhiza, Glomus fasciculatum may be partly related to elevated K/Na ratios in root and shoot tissues. Microb Ecol 54:753–760
  • Goicoechea N, Antolin MC, Sánchez-Díaz M (1997) Gas exchange is related to the hormone balance in mycorrhizal or nitrogen-fixing alfalfa subjected to drought. Physiol Plant 100:989–997
  • Goicoechea N, Baslam M, Erice G, Irigoyen JJ (2014) Increased photosynthetic acclimation in alfalfa associated with arbuscular mycorrhizal fungi (AMF) and cultivated in greenhouse under elevated CO2. J Plant Physiol 171:1774–1781
  • Grondin A, Mauleon R, Vadez V, Henry A (2016) Root aquaporins contribute to whole plant water fluxes under drought stress in rice (Oryza sativa L.) Plant Cell Environ 39:349–365
  • Gupta AB, Sankararamakrishnan R (2009) Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: characterization of XIP subfamily of aquaporins from evolutionary perspective. BMC Plant Biol 9:134
  • Hajiboland R, Aliasgharzadeh N, Laiegh SF, Poschenrieder C (2010) Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331:313–327
  • Hammer E, Nasr H, Pallon J, Olsson P, Wallander H (2011) Elemental composition of arbuscular mycorrhizal fungi at high salinity. Mycorrhiza 21:117–129
  • Harbinson J (2013) Improving the accuracy of chlorophyll fluorescence measurements. Plant Cell Environ 36:1751–1754
  • Jahromi F, Aroca R, Porcel R, Ruiz-Lozano JM (2008) Influence of salinity on the in vitro development of Glomus intraradices and on the in vivo physiological and molecular responses of mycorrhizal lettuce plants. Microbial Ecol 55:45–53
  • Javot H, Maurel C (2002) The role of aquaporins in root water uptake. Ann Bot 90:301–313
  • Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M, Giller KE (2009) Are the rate of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem 41:1233–1244
  • Krajinski F, Biela A, Schubert D, Gianinazzi-Pearson V, Kaldenhoff R, Franken P (2000) Arbuscular mycorrhiza development regulates the mRNA abundance of Mtaqp1 encoding a mercury-insensitive aquaporin of Medicago truncatula. Planta 211:85–90
  • Kumar K, Kumar M, Kim S-R, Ryu H, Cho Y-G (2013) Insights into genomics of salt stress responses in rice. Rice 6:27
  • Lazár D (2015) Parameters of photosynthetic energy partitioning. J Plant Physiol 175:131–147
  • Lehto T, Zwiazek JJ (2011) Ectomycorrhizas and water relations of trees: a review. Mycorrhiza 21:71–90
  • Li T, Hu Y-J, Hao Z-P, Li H, Wang Y-S, Chen B-D (2013) First cloning and characterization of two functional aquaporin genes from an arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 197:617–630
  • Lian H-L, Yu X, Ye Q, Ding X-S, Kitagawa Y, Kwak S-S, Su W-S, Tang Z-C (2004) The role of aquaporin RWC3 in drought avoidance in rice. Plant Cell Physiol 45:481–489
  • Lima-Neto MC, Lobo AKM, Martins MO, Fontenele AV, Albenisio J, Silveira G (2014) Dissipation of excess photosynthetic energy contributes to salinity tolerance: a comparative study of salt-tolerant Ricinus communis and salt-sensitive Jatropha curcas. J Plant Physiol 171:23–30
  • Liu T, Sheng M, Wang CY, Chen H, Li Z, Tang M (2015) Impact of arbuscular mycorrhizal fungi on the growth, water status, and photosynthesis of hybrid poplar under drought stress and recovery. Photosynthetica 53:250–258
  • López D, Venisse J-S, Fumanal B, Chaumont F, Guillot E, Daniels MJ, Gousset-Dupont A (2013) Aquaporins and leaf hydraulics: poplar sheds new light. Plant Cell Physiol 54:1963–1975
  • Maathuis FJM (2014) Sodium in plants: perception, signalling, and regulation of sodium fluxes. J Exp Bot 65:849–858
  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158CrossRefGoogle Scholar Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, London
  • Martínez-Ballesta MC, Martínez V, Carvajal M (2000) Regulation of water channel activity in whole roots and in protoplasts from roots of melon plants grown under saline conditions. Aust J Plant Physiol 27:685–691
  • Masumoto C, Ishii T, Hatanaka T, Uchida N (2005) Mechanisms of high photosynthetic capacity in BC2F4 lines derived from a cross between Oryza sativa and wild relatives O-rufipogon. Plant Prod Sci 8:539–545
  • Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624
  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467
  • Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663
  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
  • Noctor G, Mhamdi A, Foyer CH (2016) Oxidative stress and antioxidative systems: recipes for successful data collection and interpretation. Plant Cell Environ 39:1140–1160
  • Olías R, Eljakaoui Z, Li J, Alvarez De Morales P, Marín-Manzano MC, Pardo JM, Belver A (2009) The plasma membrane Na+/H+ antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na+ between plant organs. Plant Cell Environ 32:904–916
  • Otto B, Kaldenhoff R (2000) Cell-specific expression of the mercury-insensitive plasma-membrane aquaporin NtAQP1 from Nicotiana tabacum. Planta 211:167–172
  • Ouziad F, Wilde P, Schmelzer E, Hildebrandt U, Bothe H (2006) Analysis of expression of aquaporins and Na+/H+ transporters in tomato colonized by arbuscular mycorrhizal fungi and affected by salt stress. Environ Exp Bot 57:177–186
  • Pardo JM, Cubero B, Leidi EO, Quintero FJ (2006) Alkali cation exchangers: roles in cellular homeostasis and stress tolerance. J Exp Bot 57:1181–1199
  • Pinior A, Grunewaldt-Stöcker G, von Alten H, Strasser RT (2005) Mycorrhizal impact on drought stress tolerance of rose plants probed by chlorophyll a fluorescence, proline content and visual scoring. Mycorrhiza 15:596–605
  • Pitman M, Läuchli A (2002) Global impact of salinity and agricultural ecosystems. In: Läuchli A, Lüttge U (eds) Salinity: environment-plants-molecules. Kluwer, Dordrecht, pp 3–20
  • Porcel R, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron Sustain Dev 32:181–200
  • Porcel R, Redondo-Gómez S, Mateos-Naranjo E, Aroca R, Garcia R, Ruiz-Lozano JM (2015) Arbuscular mycorrhizal symbiosis ameliorates the optimum quantum yield of photosystem II and reduces non-photochemical quenching in rice plants subjected to salt stress. J Plant Physiol 185:75–83
  • Porcel R, Aroca R, Azcón R, Ruiz-Lozano JM (2016) Regulation of cation transporter genes by the arbuscular mycorrhizal symbiosis in rice plants subjected to salinity suggests improved salt tolerance due to reduced Na+ root-to-shoot distribution. Mycorrhiza 26:673–684
  • Ramoliya PJ, Patel HM, Pandey AN (2004) Effect of salinization of soil on growth and macro- and micro-nutrient accumulation in seedlings of Salvadora persica (Salvadoraceae). Forest Ecol Manag 202:181–193
  • Ranathunge K, Kotula L, Steudle E, Lafitte R (2004) Water permeability and reflection coefficient of the outer part of young rice roots are differently affected by closure of water channels (aquaporins) or blockage of apoplastic pores. J Exp Bot 55:433–447
  • Redondo-Gómez S, Mateos-Naranjo E, Figueroa ME, Davy AJ (2010) Salt stimulation of growth and photosynthesis in an extreme halophyte, Arthrocnemum macrostachyum. Plant Biol 2010(12):79–87
  • Ren Z-H, Gao J-P, Li L-G et al (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37:1141–1146
  • Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13:309–317
  • Ruiz-Lozano JM, Aroca R (2010) Host response to osmotic stresses: stomatal behaviour and water use efficiency of arbuscular mycorrhizal plants. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function, 2nd edn. Springer, Dordrecht, pp 239–256
  • Ruiz-Lozano JM, Alguacil MM, Bárzana G, Vernieri P, Aroca R (2009) Exogenous ABA accentuates the differences in root hydraulic properties between mycorrhizal and non mycorrhizal maize plants through regulation of PIP aquaporins. Plant Mol Biol 70:565–579
  • Ruiz-Lozano JM, Porcel R, Azcón R, Aroca R (2012) Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. J Exp Bot 63:4033–4044
  • Ruíz-Sánchez M, Aroca R, Munoz Y, Polon R, Ruíz-Lozano JM (2010) The arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. J Plant Physiol 167:862–869
  • Ruíz-Sánchez M, Armada E, Munoz Y, García de Salamone I, Aroca R, Ruíz-Lozano JM, Azcón R (2011) Azospirillum and arbuscular mycorrhizal colonization enhanced rice growth and physiological traits under well-watered and drought conditions. J Plant Physiol 168:1031–1037
  • Sade N, Gebretsadik M, Seligmann R, Schwartz A, Wallach R, Moshelion M (2010) The role of tobacco aquaporin1 in improving water use efficiency, hydraulic conductivity, and yield production under salt stress. Plant Physiol 152:245–254
  • Sannazzaro AI, Ruiz OA, Alberto EO, Menendez AB (2006) Alleviation of salt stress in Lotus glaber by Glomus intraradices. Plant Soil 285:279–287
  • Sanz-Sáez A, Erice G, Aranjuelo I, Aroca R, Ruiz-Lozano JM, Aguirreolea J et al (2013) Photosynthetic and molecular markers of CO2-mediate photosynthetic downregulation in nodulated alfalfa. J Integr Plant Biol 55:721–734
  • Scheibe R, Beck E (2011) Drought, desiccation, and oxidative stress. In: Lüttge U et al (eds) Plant desiccation tolerance, Ecological studies, vol 215. Springer, Berlin, pp 209–231
  • Shao HB, Chu LY, Shao MA, Jaleel CA, Mi HM (2008) Higher plant antioxidants and redox signaling under environmental stresses. Comptes Redue Biolol 331:433–441
  • Sheng M, Tang M, Chen H, Yang B, Zhang F, Huang Y (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18:287–296
  • Shi HZ, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–477
  • Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M (ed) Probing photosynthesis: mechanisms, regulation and adaptation. Taylor & Francis, London, pp 445–483
  • Takai T, Kondo M, Yano M, Yamamoto T (2010) A quantitative trait locus for chlorophyll content and its association with leaf photosynthesis in rice. Rice 3:172–180
  • Talaat NB, Shawky BT (2011) Influence of arbuscular mycorrhizae on yield, nutrients, organic solutes, and antioxidant enzymes of two wheat cultivars under salt stress. J Plant Nutr Soil Sci 174:283–291
  • Uehlein N, Fileschi K, Eckert M, Bienert GP, Bertl A, Kaldenhoff R (2007) Arbuscular mycorrhizal symbiosis and plant aquaporin expression. Phytochemistry 68:122–129
  • Wang WX, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14
  • Wu H, Shabala L, Barry K, Zhou M, Shabala S (2013) Ability of leaf mesophyll to retain potassium correlates with salinity tolerance in wheat and barley. Physiol Plant 149:515–527
  • Zelazny E, Borst JW, Muylaert M, Batoko H, Hemminga MA, Chaumont F (2007) FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localisation. Proc Natl Acad Sci USA 104:12359–12364
  • Zhao C-X, Shao H-B, Chu L-Y (2008) Aquaporin structure-function relationships: water flow through plant living cells. Col Surf B 62:163–172
  • Zhu XQ, Wang CY, Chen H, Tang M (2014) Effects of arbuscular mycorrhizal fungi on photosynthesis, carbon content, and calorific value of black locust seedlings. Photosynthetica 52:247–252
  • Zhu M, Shabala L, Cuin TA, Huang X, Zhou M, Munns R, Shabala S (2016) Nax loci affect SOS1-like Na+/H+ exchanger expression and activity in wheat. J Exp Bot 67:835–844
  • Zuccarini P, Okurowska P (2008) Effects of mycorrhizal colonization and fertilization on growth and photosynthesis of sweet basil under salt stress. J Plant Nutr 31:497–513