Advertisement

Planta

pp 1–9 | Cite as

Rhizobial symbiosis modifies root hydraulic properties in bean plants under non-stressed and salinity-stressed conditions

  • Vinicius Ide Franzini
  • Rosario Azcón
  • Juan Manuel Ruiz-Lozano
  • Ricardo ArocaEmail author
Original Article

Abstract

Main conclusion

Rhizobial symbiosis improved the water status of bean plants under salinity-stress conditions, in part by increasing their osmotic root water flow.

One of the main problems for agriculture worldwide is the increasing salinization of farming lands. The use of soil beneficial microorganisms stands up as a way to tackle this problem. One approach is the use of rhizobial N2-fixing, nodule-forming bacteria. Salinity-stress causes leaf dehydration due to an imbalance between water lost through stomata and water absorbed by roots. The aim of the present study was to elucidate how rhizobial symbiosis modulates the water status of bean (Phaseolus vulgaris) plants under salinity-stress conditions, by assessing the effects on root hydraulic properties. Bean plants were inoculated or not with a Rhizobium leguminosarum strain and subjected to moderate salinity-stress. The rhizobial symbiosis was found to improve leaf water status and root osmotic water flow under such conditions. Higher content of nitrogen and lower values of sodium concentration in root tissues were detected when compared to not inoculated plants. In addition, a drop in the osmotic potential of xylem sap and increased amount of PIP aquaporins could favour higher root osmotic water flow in the inoculated plants. Therefore, it was found that rhizobial symbiosis may also improve root osmotic water flow of the host plants under salinity stress.

Keywords

Aquaporins Nitrogen Phaseolus vulgaris Rhizobium Root water flux Sodium 

Notes

References

  1. Akramkhanov A, Martius C, Park SJ, Hendrickx JMH (2011) Environmental factors of spatial distribution of soil salinity on flat irrigated terrain. Geoderma 163:55–62CrossRefGoogle Scholar
  2. Aroca R, Amodeo G, Fernández-Illescas S, Herman EM, Chaumont F, Chrispeels MJ (2005) The role of aquaporin and membrane damage in chilling and hydrogen peroxide induced changes in the hydraulic conductance of maize roots. Plant Physiol 137:341–353CrossRefGoogle Scholar
  3. 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 173:808–816CrossRefGoogle Scholar
  4. Aroca R, Porcel R, Ruiz-Lozano JM (2012) Regulation of root water uptake under abiotic stress conditions. J Exp Bot 63:43–57CrossRefGoogle Scholar
  5. Asanuma K-I, Bayorbor TB, Kogure K, Ofosu-Anim J, Suzuki N (1992) Studies on the response of nodulated soybean to nitrogen fertilizer. I. On the carbon dioxide exchange of shoots and underground organs. Jpn J Crop Sci 61:433–438CrossRefGoogle Scholar
  6. Benabdellah K, Ruiz-Lozano JM, Aroca R (2009) Hydrogen peroxide effects on root hydraulic properties and plasma membrane aquaporin regulation in Phaseolus vulgaris. Plant Mol Biol 70:647–661CrossRefGoogle Scholar
  7. Benidire L, Lahrouni M, El Khalloufi F, Gottfert M, Oufdou K (2017) Effets of rhizobium leguminosarum inoculation on growth, nitrogen uptake and mineral assimilation in Vicia faba plants under salinity. J Agric Sci Technol 19:889–901Google Scholar
  8. Calvo-Polanco M, Sánchez-Romera B, Aroca R (2014) Mild salt stress conditions induce differences responses in root hydraulic conductivity of Phaseolus vulgaris over-time. PLoS One 9:e90631CrossRefGoogle Scholar
  9. Calvo-Polanco M, Sánchez-castro I, Cantos M, García JL, Azcón R, Ruiz-Lozano JM, Beuzón CR, Aroca R (2016) Effects of different arbuscular mycorrhizal fungal backgrounds and soils on olive plants growth and water relation properties under well-watered and drought conditions. Plant, Cell Environ 39:2498–2514CrossRefGoogle Scholar
  10. Carter AM, Tegeder M (2016) Increasing nitrogen fixation and seed development in Soybean requires complex adjustments of nodule nitrogen metabolism and partitioning processes. Curr Biol 26:2044–2051CrossRefGoogle Scholar
  11. Catalano CM, Lane WS, Sherrier DJ (2004) Biochemical characterization of symbiosome membrane proteins from Medicago truncatula root nodules. Electrophoresis 25:519–531CrossRefGoogle Scholar
  12. Chaumont F, Barrieu F, Jung R, Chrispeels MJ (2000) Plasma membrane intrinsic proteins from maize cluster in two sequences subgroups with differential aquaporin activity. Plant Physiol 122:1025–1034CrossRefGoogle Scholar
  13. Chaumont F, Moshelion M, Daniels MJ (2005) Regulation of plant aquaporin activity. Biol Cell 97:749–764CrossRefGoogle Scholar
  14. Cordovilla MP, Ocaña A, Ligero F, Lluch C (1996) Growth and symbiotic performance of faba bean inoculated with Rhizobium leguminosarum biovar. viciae strains tolerant to salt. Soil Sci Plant Nutr 42:133–140CrossRefGoogle Scholar
  15. Craig GF, Atkins CA, Bell DT (1991) Effect of salinity on growth of four strains of rhizobium and their infectivity and effectiveness on two species of Acacia. Plant Soil 133:253–262CrossRefGoogle Scholar
  16. Da Ines O, Graf W, Franck KI, Albert A, Winkler JB, Schreb H, Stichler W, Schäffner AR (2010) Kinetic analyses of plant water relocation using deuterium as tracer—reduced water flux of Arabidopsis pip2 aquaporin knockout mutants. Plant Biol 12:129–139CrossRefGoogle Scholar
  17. Dean RM, Rivers RL, Zeidel ML, Roberts DM (1999) Purification and functional reconstitution of soybean nodulin 26. An aquaporin with water and glycerol transport properties. Biochemistry 38:347–353CrossRefGoogle Scholar
  18. Fetter K, Van Wilder V, Moshelion M, Chaumont F (2004) Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16:215–228CrossRefGoogle Scholar
  19. Fiascorano ML, Gogorcena Y, Muñoz F, Andueza D, Sánchez-Díaz M, Antolín MC (2012) Effects of nitrogen source and water availability on stem carbohydrates and cellulosic bioethanol traits of alfalfa plants. Plant Sci 191–192:16–23Google Scholar
  20. Figueira EMAP, Caldeira GCN (2005) Effect of nitrogen nutrition on salt tolerance of Pisum sativum during vegetative growth. J Plant Nutr Soil Sci 168:359–363CrossRefGoogle Scholar
  21. Franzini VI, Azcón R, Méndes FL, Aroca R (2010) Interaction between Glomus species and Rhizobium strains affect the nutritional physiology of drought-stressed legume hosts. J Plant Physiol 167:614–619CrossRefGoogle Scholar
  22. Franzini VI, Azcón R, Méndes FL, Aroca R (2013) Different interaction among Glomus and Rhizobium species on Phaseolus vulgaris and Zea mays plant growth, physiology and symbiotic development under moderate drought stress conditions. Plant Growth Regul 70:265–273CrossRefGoogle Scholar
  23. Frechilla S, González EM, Royuela M, Arrese-Igor C, Lamsfus C, Aparicio-Tejo PM (1999) Source of nitrogen nutrition affects pea growth involving changes in stomatal conductance and photorespiration. J Plant Nutr 22:911–926CrossRefGoogle Scholar
  24. García-Sánchez F, Carvajal M, Sánchez-Pina MA, Martínez V, Cerda A (2000) Salinity resistance of Citrus seedlings in relation to hydraulic conductance, plasma membrane ATPase and anatomy of the roots. J Plant Physiol 156:724–730CrossRefGoogle Scholar
  25. Garg N, Geetanjali (2007) Symbiotic nitrogen fixation in legume nodules: process and signaling. A review. Agron Sustain Dev 27:59–68CrossRefGoogle Scholar
  26. Gil-Serrano A, Sánchez del Junco A, Tejero-Mateo P, Megías M, Caviedes MA (1990) Structure of the extracellular polysaccharide secreted by Rhizobium leguminosarum var. phaseoli CIAT 899. Carbohydr Res 204:103–107CrossRefGoogle Scholar
  27. Guo S, Shen Q, Brueck H (2007) Effects of local nitrogen supply on water uptake of bean plants in a split root system. J Integr Plant Biol 49:472–480CrossRefGoogle Scholar
  28. Gyenge JE, Fernández ME, Schlichter TM (2003) Water relations of ponderosa pines in Patagonia Argentina: implications for local water resources and individual growth. Trees Struct Funct 17:417–423CrossRefGoogle Scholar
  29. Kay R, Chan A, Daly M, McPherson J (1987) Duplication of CaMV 35S promoter sequences creates a strong enhancer for plant genes. Science 236:1299–1302CrossRefGoogle Scholar
  30. Kim YX, Ranathunge K, Lee S, Lee Y, Lee D, Sung J (2018) Composite transport model and water solute transport across plant roots: an update. Front Plant Sci 9:193CrossRefGoogle Scholar
  31. Knipfer T, Fricke W (2011) Water uptake by seminal and adventitious roots in relation to whole-plant water flow in barley (Hordeum vulgare L.). J Exp Bot 62:717–733CrossRefGoogle Scholar
  32. Lee SH, Chung GC, Jang JY, Ahn SJ, Zwiazek JJ (2012) Overexpression of PIP2;5 aquaporin alleviates effects of low root temperature on cell hydraulic conductivity and growth in Arabidopsis. Plant Physiol 159:479–488CrossRefGoogle Scholar
  33. Li Y, Shao M (2003) Responses of radial and axial hydraulic resistances in maize roots to nitrogen availability. J Plant Nutr 26:821–834CrossRefGoogle Scholar
  34. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408CrossRefGoogle Scholar
  35. Marulanda A, Azcón R, Chaumont F, Ruiz-Lozano JM, Aroca R (2010) Regulation of plasma membrane aquaporins by inoculation with a Bacillus megaterium strain in maize (Zea mays L.) under unstressed and salt-stressed conditions. Planta 232:533–543CrossRefGoogle Scholar
  36. Matre P, Morillon R, Barrieu F, North GB, Nobel PS, Chrispeels MJ (2002) Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiol 130:2101–2110CrossRefGoogle Scholar
  37. Maurel C, Santoni V, Luu DT, Wudick MM, Verdoucq L (2009) The cellular dynamics of plant aquaporin expression and functions. Curr Opin Plant Biol 12:690–698CrossRefGoogle Scholar
  38. Mrema AF, Granhall U, Sennerby-Forsse L (1997) Plant growth, leaf water potential, nitrogenase activity and nodule anatomy in Leucaena leucocephala as affected by water stress and nitrogen availability. Trees Struct Funct 12:42–48Google Scholar
  39. Nedjimi B, Daoud Y (2009) Effcets of calcium chloride on growth, membrane permeability and root hydraulic conductivity in two Atriplex species grown at high (sodium chloride) salinity. J Plant Nutr 32:1818–1830CrossRefGoogle Scholar
  40. North GB, Nobel PS (1991) Changes in hydraulic conductivity and anatomy caused by drying and rewetting roots of Agave deserti (Agavaceae). Am J Bot 78:906–915CrossRefGoogle Scholar
  41. Perrone I, Gambino G, Chitarra W, Vitali M, Pagliarani C, Riccomagno N, Ballestrini R, Kaldenhoff R, Uehlein N, Gribaudo I, Schubert A, Lovisolo C (2012) The grapevine root-specific aquaporin VvPIP2;4N controls root hydraulic conductance and leaf gas exchange under well-watered conditions but not under water stress. Plant Physiol 160:965–977CrossRefGoogle Scholar
  42. Porcel R, Aroca R, Azcón R, Ruiz-Lozano JM (2006) PIP aquaporin gene expression in arbuscular mycorrhizal Glycine max and Lactuca sativa plants in relation to drought stress tolerance. Plant Mol Biol 60:389–404CrossRefGoogle Scholar
  43. Pucciariello C, Innoncenti G, Van de Velde W, Lambert A, Hopkins J, Clement M, Ponchet M, Pauly N, Goormachtig S, Holsters M, Puppo A, Frendo P (2009) (Homo)glutathione depletion modulates host gene expression during symbiotic interaction between Medicago truncatula and Sinorhizobium meliloti. Plant Physiol 151:1186–1196CrossRefGoogle Scholar
  44. Quiroga G, Erice G, Aroca R, Zamarreño AM, García-Mina JM, Ruiz-Lozano JM (2018) Arbuscular mycorrhizal symbiosis and salicylic acid regulate aquaporins and root hydraulic properties in maize plants subjected to drought. Agric Water Manage 202:271–284CrossRefGoogle Scholar
  45. Ramana GV, Padhy SP, Chaitanya KV (2012) Diffrential responses of four soybean (Glycine max L.) cultivard to salinity stress. Legume Res 35:185–193Google Scholar
  46. Rewald B, Leuschner C, Wiesman Z, Ephrath JE (2011) Influence of salinity on root hydraulic properties of three olive varieties. Plant Biosystems 145:12–22CrossRefGoogle Scholar
  47. Rincon CA, Raper CD, Patterson RP (2003) Genotypic differences in root anatomy affecting water movement through roots of soybean. Int J Plant Sci 164:543–551CrossRefGoogle Scholar
  48. Sánchez-Romera B, Ruiz-Lozano JM, Li G, Luu DT, Martínez-Ballesta MC, Carvajal M, Zamarreño AM, García-Mina JM, Maurel C, Aroca R (2014) Enhancement of root hydraulic conductivity by methyl jasmonate and the role of calcium and abscisic acid in this process. Plant Cell Environ 37:995–1008CrossRefGoogle Scholar
  49. Sánchez-Romera B, Ruiz-Lozano JM, Zamarreño AM, García-Mina JM, Aroca R (2016) Arbuscular mycorrhizal symbiosis and methyl jasmonate avoid the inhibition of root hydraulic conductivity caused by drought. Mycorrhiza 26:111–122CrossRefGoogle Scholar
  50. Sánchez-Romera B, Porcel R, Ruiz-Lozano JM, Aroca R (2018a) Arbuscular mycorrhizal symbiosis modifies the effects of a nitric oxide donor (sodium nitroprusside; SNP) and a nitric oxide synthesis inhibitor (Nω-nitro-l-arginine methyl ester; l-NAME) on lettuce plants under well watered and drought conditions. Symbiosis 74:11–20CrossRefGoogle Scholar
  51. Sánchez-Romera B, Calvo-Polanco M, Ruiz-Lozano JM, Zamarreño AM, Arbona V, García-Mina JM, Gómez-Cadenas A, Aroca R (2018b) Involvement of the def-1 mutation in the response of tomato plants to arbuscular mycorrhizal symbiosis under well-watered and drought conditions. Plant Cell Physiol 59:248–261CrossRefGoogle Scholar
  52. Silva C, Martínez V, Carvajal M (2008) Osmotic versus toxic effects of NaCl on pepper plants. Biol Plant 52:72–79CrossRefGoogle Scholar
  53. Staiger D, Zecca L, Kirk DAW, Apel K, Eckstein L (2003) The circadian clock regulated RNA-binding protein AtGRP7 autoregulates its expression by influencing alternative splicing of its own pre-mRNA. Plant J 33:361–371CrossRefGoogle Scholar
  54. Steudle E, Brinckmann E (1989) The osmometer model of the root: water ans solute relations of Phaseolus coccineus. Bot Acta 102:85–95CrossRefGoogle Scholar
  55. Steudle E, Peterson CA (1998) How does water get through roots? J Exp Bot 49:755–788Google Scholar
  56. Temmei Y, Uchida S, Hoshino D, Kanzawa N, Kuwahara M, Sasaki S, Tsuchiya T (2005) Water channel activities of Mimosa pudica plasma membrane intrinsic proteins are regulated by direct interaction and phosphorylation. FEBS Lett 579:4417–4422CrossRefGoogle Scholar
  57. Thrall PH, Bever JD, Slattery JF (2008) Rhizobial mediation of Acacia adaptation to soil salinity: evidence of underlying trade-offs and tests of expected plants. J Ecol 96:746–755CrossRefGoogle Scholar
  58. Vance CP, Boylan KLM, Maxwell CA, Heichel GH, Hardman LL (1985) Transport and partitioning of CO2 fixed by root nodules of ureide and amide producing legumes. Plant Physiol 78:774–778CrossRefGoogle Scholar
  59. Vicente CSL, Pérez-Fernández MA, Pereira G, Tavares de Sousa MM (2012) Biological nitrogen fixation of Biserrula pelecinus L. under water deficit. Plant Soil Environ 58:360–366CrossRefGoogle Scholar
  60. Wang HS, Jia GS (2012) Satellite-based monitoring of decadal soil salinization and climate effects in a semi-arid region of China. Adv Atmos Sci 29:1089–1099CrossRefGoogle Scholar
  61. Wen K, St Segin P, St-Arnaud M, Jabaji-Hare S (2005) Real-time quantitative RT-PCR of defense-associated gene transcripts of Rhizoctonia solani-infected seedlings in response to inoculation with a nonpathogenic binucleate Rhizoctonia isolate. Phytopathology 95:345–353CrossRefGoogle Scholar
  62. Wienkoop S, Saalbach G (2003) Proteome analysis. Novel proteins identified at the peribacteroid membrane from Lotus japonicus root nodules. Plant Physiol 131:1080–1090CrossRefGoogle Scholar
  63. Zaman-Allah M, Sifi B, Issoufou M, El Aouni MH (2005) Salt tolerance of a common bean (Phaseolus vulgaris L.) cultivar as affected by rhizobia. Symbiosis 40:17–22Google Scholar
  64. Zelazny E, Miecielica U, Borst JW, Memminga MA, Chaumont F (2009) An N-terminal diacidic motif is required for the trafficking of maize aquaporins ZmPIP2;4 and ZmPIP2;5 to the plasma membrane. Plant J 57:346–355CrossRefGoogle Scholar
  65. Zhang DY, Ali Z, Wang CB, Xu L, Yi JX, Xu ZL, Liu XQ, He XL, Huang YH, Khan IA, Trethowan RM, Ma HX (2013) Genome-wide sequence characterization and expression analysis of major intrinsic proteins in Soybean (Glycine max L.). PloS One 8:e56312CrossRefGoogle Scholar
  66. Zhang Z-L, Liu G-D, Zhang F-C, Zheng C-X, Ni F-Q, Kang Y-H, Zeng Y (2014) Effects of nitrogen content on growth and hydraulic characteristics of peach (Prunus persica L.) seedlings under different soil moisture conditions. J For Res 25:365–375CrossRefGoogle Scholar
  67. Zheng QS, Liu ZP, Chen G, Gao YZ, Li Q, Wang JY (2010) Comparison of osmotic regulation in dehydration- and salinity-stressed sunflower seedlings. J Plant Nutr 33:966–981CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Soil Microbiology and Symbiotic SystemEstación Experimental del Zaidín (CSIC)GranadaSpain

Personalised recommendations