Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Negative short-term salt effects on the soybean–Bradyrhizobium japonicum interaction and partial reversion by calcium addition

Nacira Muñoz A B , Marianela Rodriguez A , German Robert A B and Ramiro Lascano A B C
+ Author Affiliations
- Author Affiliations

A Instituto de Fisiología y Recursos Genéticos Vegetales, Centro de Investigaciones Agropecuarias-INTA, Camino a 60 Cuadras Km 5 y ½, Córdoba Argentina.

B Cátedra de Fisiología Vegetal, Facultad de Ciencias Exactas Físicas y Naturales, Universidad Nacional de Córdoba, Av. Vélez Sarsfield 299, Córdoba Argentina.

C Corresponding author. Email: hrlascano@correo.inta.gov.ar

Functional Plant Biology 41(1) 96-105 https://doi.org/10.1071/FP13085
Submitted: 5 September 2012  Accepted: 19 July 2013   Published: 5 September 2013

Abstract

The short-term (2 h) effects of salt stress (50 and 150 mM NaCl) on early events of soybean– Bradyrhizobium japonicum (rhizobia) interaction were analysed, determining the following parameters in root hair with or without calcium addition: deformation, apoplastic superoxide radical production (O2), root hair death and sodium/potassium ion content. We also analysed whether this short-term salt stress influenced later formation of crown and noncrown nodules, determining the number and weight of nodules. The negative effect of salt stress on these characters was attenuated by the addition of 5 mM CaCl2. We also analysed the expression of pathogenesis-related proteins (PRP) genes PR-1, PR-2, PR-3, and four isoforms of PR-5. The expression of PR-2 increased under saline conditions and decreased in osmotic treatment and saline treatment supplemented with calcium in the presence of the symbiont. The changes in PR-2 expression levels, together with the death of root hairs provide a possible mechanism for the inhibition of infection by the symbiont under salinity, and suggests a possible overlap with responses to plant pathogens.

Additional keywords: ionic homeostasis, nodulation, pathogenic-related proteins, symbiotic interaction.


References

Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373–399.
Reactive oxygen species: metabolism, oxidative stress, and signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFeisL0%3D&md5=bb62c10883f0f45b9778cbbe05a12a70CAS | 15377225PubMed |

Ashraf M (1994) Breeding for salinity tolerance in plants. Critical Reviews in Plant Sciences 13, 17–42.

Bernstein L (1975) Effects of salinity and sodicity on plant growth. Annual Review of Phytopathology 13, 295–312.
Effects of salinity and sodicity on plant growth.Crossref | GoogleScholarGoogle Scholar |

Broughton W, Dilworth M (1971) Control of leghaemoglobin synthesis in snake beans. Biochemical journal 125, 1075–1080.

Cárdenas L, Martinez A, Sanchez F, Quinto C (2008) Fast, transient and specific intracellular ROS changes in living root hair cells responding to Nod factors (NFs). The Plant Journal 56, 802–813.
Fast, transient and specific intracellular ROS changes in living root hair cells responding to Nod factors (NFs).Crossref | GoogleScholarGoogle Scholar | 18680562PubMed |

Delgado J, Ligero F, Liuch C (1994) Effects of salt stress on growth and nitrogen fixation by pea, faba-bean, common bean and soybean plant. Soil Biology & Biochemistry 26, 371–376.
Effects of salt stress on growth and nitrogen fixation by pea, faba-bean, common bean and soybean plant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXis12is70%3D&md5=a8278e9db81641c4472249a9fe6e1557CAS |

Demidchik V, Maathuis F (2007) Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytologist 175, 387–404.
Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpvFSqs7w%3D&md5=e6d9d391cb0668058f9488556bf96e8aCAS | 17635215PubMed |

Demidchik V, Shabala S, Davies J (2007) Spatial variation in H2O2 response of Arabidopsis thaliana root epidermal Ca2 + flux and plasma membrane Ca2 + channels. The Plant Journal 49, 377–386.
Spatial variation in H2O2 response of Arabidopsis thaliana root epidermal Ca2 + flux and plasma membrane Ca2 + channels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXisVyisLk%3D&md5=252bc33c2375ea34e20f6298997548cdCAS | 17181775PubMed |

Domínguez F, Cejudo FJ (2006) Identification of a nuclear-localized nuclease from wheat cells undergoing programmed cell death that is able to trigger DNA fragmentation and apoptotic morphology on nuclei from human cells. Biochemical Journal 307, 529–536.

Elsheikh E, Wood M (1995) Nodulation and N2 fixation by soybean inoculated with salt-tolerant rhizobia or salt-sensitive bradyrhizobia in saline soil. Soil Biology & Biochemistry 27, 657–661.
Nodulation and N2 fixation by soybean inoculated with salt-tolerant rhizobia or salt-sensitive bradyrhizobia in saline soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlt12rt7s%3D&md5=cc96fa94177cd480fa161fec9b2ec205CAS |

Fedoroff N (2006) Redox regulatory mechanisms in cellular stress responses. Annals of Botany 98, 289–300.
Redox regulatory mechanisms in cellular stress responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xpt1yltLc%3D&md5=a9fc96e54d0386146e5c79ef9a701fa0CAS | 16790465PubMed |

Leubner-Metzger G, Meins F (1999) Functions and regulation of plant β-1,3-glucanases (PR-2). In: ‘Pathogenesis-related proteins in plants.’ (Eds SK Datta, S Muthukrishnan) pp. 49–76. (CRC Press: Boca Raton, FL, USA)

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) Method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) Method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=cda22da73d6034ad2e4c74827f633baaCAS | 11846609PubMed |

López-Baena J, Monreal JA, Pérez-Montaño F, Guasch-Vidal B, Bellogín R, Vinardell J, Ollero F (2009) The absence of Nops secretion in Sinorhizobium fredii HH103 increases GmPR1 expression in Williams soybean. Molecular Plant-Microbe Interactions 22, 1445–1454.
The absence of Nops secretion in Sinorhizobium fredii HH103 increases GmPR1 expression in Williams soybean.Crossref | GoogleScholarGoogle Scholar |

Mazarei M, Elling AA, Maier TR, Puthoff DP, Baum TJ (2007) GmEREBP1 is a transcription factor activating defense genes in soybean and Arabidopsis. Molecular Plant-Microbe Interactions 20, 107–119.
GmEREBP1 is a transcription factor activating defense genes in soybean and Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVyrsA%3D%3D&md5=0a56cfca1adb6122e58458a111e1bb77CAS | 17313162PubMed |

Mithöfer A (2002) Suppression of plant defence in rhizobia–legume symbiosis. Trends in Plant Science 7, 440–444.
Suppression of plant defence in rhizobia–legume symbiosis.Crossref | GoogleScholarGoogle Scholar | 12399178PubMed |

Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends in Plant Science 9, 490–498.
Reactive oxygen gene network of plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotF2msrg%3D&md5=f784349d5767e5607415f067ce056dcbCAS | 15465684PubMed |

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqtrw%3D&md5=0ce1f7aad22c73fffb329d4603f0e836CAS | 18444910PubMed |

Muñoz N, Robert G, Melchiorre M, Racca R, Lascano R (2012) Saline and osmotic stress differentially affects apoplastic and intracellular reactive oxygen species production, curling and death of root hair during Glycine max L.–Bradyrhizobium japonicum interaction. Environmental and Experimental Botany 78, 76–83.
Saline and osmotic stress differentially affects apoplastic and intracellular reactive oxygen species production, curling and death of root hair during Glycine max L.–Bradyrhizobium japonicum interaction.Crossref | GoogleScholarGoogle Scholar |

Onishi M, Tachi H, Kojima T, Shiraiwa M, Takahara H (2006) Molecular cloning and characterization of a novel salt-inducible gene encoding an acidic isoform of PR-5 protein in soybean (Glycine max (L.) Merr.). Plant Physiology and Biochemistry 44, 574–580.
Molecular cloning and characterization of a novel salt-inducible gene encoding an acidic isoform of PR-5 protein in soybean (Glycine max (L.) Merr.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1Cmt7vP&md5=02e942f72962752e1f8c3e2ce08caffcCAS | 17070691PubMed |

Rengel Z (1992) The role of calcium in salt toxicity. Plant, Cell & Environment 15, 625–632.
The role of calcium in salt toxicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmtlSjtL4%3D&md5=2dd1977b1ba9e329b4156423baec7757CAS |

Sagi M, Fluhr R (2001) Superoxide production by plant homologues of the gp91phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiology 126, 1281–1290.
Superoxide production by plant homologues of the gp91phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFemt7s%3D&md5=ff39ba69af81fbbff142fcd4365aba99CAS | 11457979PubMed |

Shabala S, Cuin T (2008) Potassium transport and plant salt tolerance. Physiologia Plantarum 133, 651–669.
Potassium transport and plant salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXps1Oit70%3D&md5=b00298e506b7189fc2da0a5277d6448aCAS | 18724408PubMed |

Shabala S, Demidchik V, Shabala L, Cuin T, Smith J, Miller A, Davies J, Newman I (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels. Plant Physiology 141, 1653–1665.
Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKitbo%3D&md5=9cf8fa017b3c4ebb820d7488c42c9af4CAS | 16798942PubMed |

Shao H, Song Z, Liu L (1986) Preliminary studies on the evaluation of salt tolerance in soybean varieties. Acta Agronomic Science 6, 30–35.

Shao H, Wan C, Chang R, Chen Y (1993) Preliminary study on the damage of plasma membrane caused by salt stress. Crops 1, 39–40.

Singleton P, Bohlool B (1984) Effect of salinity on nodule formation by soybean. Plant Physiology 74, 72–76.
Effect of salinity on nodule formation by soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXot1yksw%3D%3D&md5=b5a8baa8d26d348fb8411e93da5ad066CAS | 16663389PubMed |

Tachi H, Yamada K, Kojima T, Shiraiwa M, Takahara H (2009) Molecular characterization of a novel soybean gene encoding a neutral PR-5 protein induced by high-salt stress. Plant Physiology and Biochemistry 47, 73–79.
Molecular characterization of a novel soybean gene encoding a neutral PR-5 protein induced by high-salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFamtbbP&md5=536f14d1c24e636cd2042aa63b76042dCAS | 19010689PubMed |

Toné S, Sugimoto K, Tanda K, Suda T, Uehira K, Kanouchi H, Samejima K, Minatogawa Y, Earnshaw W (2007) Three distinct stages of apoptotic nuclear condensation revealed by time-lapse imaging, biochemical and electron microscopy analysis of cell-free apoptosis. Experimental Cell Research 313, 3635–3644.
Three distinct stages of apoptotic nuclear condensation revealed by time-lapse imaging, biochemical and electron microscopy analysis of cell-free apoptosis.Crossref | GoogleScholarGoogle Scholar | 17643424PubMed |

van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annual Review of Phytopathology 44, 135–162.
Significance of inducible defense-related proteins in infected plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVylsLnK&md5=d541a733cfd42d90d8b1c378e280288eCAS | 16602946PubMed |

Vasse J, de Billy F, Truchet G (1993) Abortion of infection during the Rhizobium meliloti-alfalfa symbiotic interaction is accompanied by a hypersensitive reaction. The Plant Journal 4, 555–566.
Abortion of infection during the Rhizobium meliloti-alfalfa symbiotic interaction is accompanied by a hypersensitive reaction.Crossref | GoogleScholarGoogle Scholar |

Vincent J (1970) ‘A manual for the practical study of the root-nodule bacteria.’ (Blackwell Scientific Publications: Oxford)

Yamada T, Ichimura K, Van Doorn WG (2006) DNA degradation and nuclear degeneration during programmed cell death in Antirrhinum, Argyranthemum and Petunia. Journal of Experimental Botany 57, 3543–3552.
DNA degradation and nuclear degeneration during programmed cell death in Antirrhinum, Argyranthemum and Petunia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlCnsLvF&md5=ab16873e9bbd0f26131005d07de4d009CAS | 16957019PubMed |

Zamioudis C, Pieterse C (2012) Modulation of host immunity by beneficial microbes. Molecular Plant-Microbe Interactions 25, 139–150.
Modulation of host immunity by beneficial microbes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFWisbc%3D&md5=0df5f89b667b9615d22b885fe3fde06fCAS | 21995763PubMed |

Zdor R, Pueppke S (1988) Early infection and competition for nodulation of soybean by Bradyrhizobium japonicum 123 and 138. Applied and Environmental Microbiology 54, 1996–2002.

Zhu JK (2001) Plant salt tolerance. Trends in Plant Science 6, 66–71.
Plant salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFyjtLs%3D&md5=36de2a21d4f2c605397e01ce5240d467CAS | 11173290PubMed |