Submitted Successfully!
Thank you for your contribution! You can also upload a video entry or images related to this topic.
Ver. Summary Created by Modification Content Size Created at Operation
1 -- 2647 2023-06-16 05:43:01 |
2 update reference Meta information modification 2647 2023-06-16 06:00:47 |

Video Upload Options

Do you have a full video?

Confirm

Are you sure to Delete?
Cite
If you have any further questions, please contact Encyclopedia Editorial Office.
Goyal, R.K.; Goyal, R.; Habtewold, J.Z. Legume–Rhizobial Symbiotic Interactions Beyond Nitrogen Fixation. Encyclopedia. Available online: https://encyclopedia.pub/entry/45697 (accessed on 07 December 2023).
Goyal RK, Goyal R, Habtewold JZ. Legume–Rhizobial Symbiotic Interactions Beyond Nitrogen Fixation. Encyclopedia. Available at: https://encyclopedia.pub/entry/45697. Accessed December 07, 2023.
Goyal, Ravinder K., Ravinder Goyal, Jemaneh Z. Habtewold. "Legume–Rhizobial Symbiotic Interactions Beyond Nitrogen Fixation" Encyclopedia, https://encyclopedia.pub/entry/45697 (accessed December 07, 2023).
Goyal, R.K., Goyal, R., & Habtewold, J.Z.(2023, June 16). Legume–Rhizobial Symbiotic Interactions Beyond Nitrogen Fixation. In Encyclopedia. https://encyclopedia.pub/entry/45697
Goyal, Ravinder K., et al. "Legume–Rhizobial Symbiotic Interactions Beyond Nitrogen Fixation." Encyclopedia. Web. 16 June, 2023.
Legume–Rhizobial Symbiotic Interactions Beyond Nitrogen Fixation
Edit

Plants often experience unfavorable conditions during their life cycle that impact their growth and sometimes their survival. A temporary phase of such stress, which can result from heavy metals, drought, salinity, or extremes of temperature or pH, can cause mild to enormous damage to the plant depending on its duration and intensity. Besides environmental stress, plants are the target of many microbial pathogens, causing diseases of varying severity. In plants that harbor mutualistic bacteria, stress can affect the symbiotic interaction and its outcome.

abiotic and biotic stress legume rhizobia stress tolerance symbiosis rhizosphere

1. Introduction

In simplistic terms, a favorable environment of temperature, light, and nutrient availability is among the key factors that promote plant growth and their geographical distribution. Nonetheless, the territorialization of plants was an evolutionary process that started with the establishment of a set of plant species, followed by the diversification of another group of plants. Among the four phases of plant radiation [1], the last phase involved the diversification of angiosperms, which are the most dominant plant species and represent a vast ecological differentiation [2]. With over 350,000 species, angiosperms comprise about 90% of the total unique plant species [3][4]. What led to the success of angiosperms goes beyond the mutually beneficial animal–plant relationships to annual growth form, homeotic gene effects, asexual and sexual reproduction, a propensity for hybrid polyploidy, and an apparent high tolerance to extinction [3]. Many hypotheses have been formulated to explain the speciation and diversification of angiosperms. There is an uneven geographic distribution of plants, which could be due to the differential rate of diversification. It is believed that the key innovations, which are associated with plant morphological, physiological and behavior attributes, along with ecological opportunities, are the important determinants of a diversification rate [3][5].
With a count of 22,360 species [6], legumes are among the largest group of angiosperms, representing the outcome of a high diversification rate. Their adaptation to new climates and/or ecological niches, which are among the important factors promoting rapid diversification [7]), seems to have contributed to their occupancy in diverse habitats. By using the example of phaseoloid legumes that contain many commercial legumes, Li et al. [8] gathered more evidence favoring the interplay of ecological opportunities and key innovations in triggering diversification. While big climatic changes in the past shaped the diversification of plants, the current conditions of the environment determine their growth and distribution, especially of food and forage crops. Heavy metal toxicity, high and low temperatures, drought, salinity, extreme pH, pests, and pathogens all exert significant adverse impacts on the plant’s survival and productivity. Although plants have developed different mechanisms to cope with stress, those that fail become extinct in that environment.
Legumes develop a symbiotic interaction with rhizobia, which take the form of bacteroides and reside inside the nodular structures on the host roots. In exchange for carbon nutrients from the host, the rhizobial bacteria convert atmospheric nitrogen into its usable form, thus making the plant self-sufficient in nitrogen requirements [9]. Nitrogen is one of the macronutrients linked with plant growth and productivity. In non-leguminous crops, nitrogen is often supplemented in the form of synthetic fertilizers, which are now becoming an issue of environmental pollution and a threat to agricultural sustainability. The rhizobial symbiotic interactions evolved over time to provide the host with nitrogen and adaptability to varying environmental conditions and ecosystems [10][11]. It appears that nitrogen fixation is not the only driver of evolution, but host–symbiont genotype interactions and other factors do play an important role [12][13]. While rhizobial interactions have a direct positive impact on plants’ adaptability to both abiotic and biotic stresses, they can also have an indirect impact through the modification of the rhizosphere microbiome. The excretion of compounds (e.g., nodulation factors and exopolysaccharides) influences the structure of the rhizosphere, including non-symbiotic microbial communities, which in turn can alleviate stress and promote plant growth [14]. Hence, symbiotic relationships benefit legumes greatly, not only through nitrogen fixation but also through other benefits that aid the host’s survival and diversity in unfavorable settings.

2. Heavy Metal Stress Tolerance

Soil is a reservoir of several heavy metals that are required in microquantities to meet plants’ nutritional needs. Many of these metals, when present in higher concentrations due to either anthropogenic sources [15][16][17][18] or geological distribution, negatively affect plant growth and development. The metal stress leads to the formation of reactive oxygen species, which interfere with the structure and function of macromolecules, including lipids, proteins, and nucleic acids [19]. The metals in their high concentrations can also limit the rhizobial interaction with the host, resulting in a reduction of nodule number and nitrogen-fixating activity [20][21][22][23][24][25][26][27][28]. A constant threat to mutualism seems to have led to the development of metal-tolerating strategies in rhizobia. The bacteria isolated from heavy-metal soils often tend to tolerate relatively higher levels of the metals [29]. Numerous studies suggest that such rhizobia provide hosts with the ability to tolerate stress caused by many toxic metals, such as cadmium (Cd), nickel (Ni), mercury (Hg), chromium (Cr), arsenic (As), aluminum (Al), copper (Cu), lead (Pb), etc. (Table 1). There was a significant improvement in growth, development, and yield in several leguminous crops under heavy metal regimes when inoculated with appropriate rhizobial species. A symbiotic opportunity for legumes with naturally occurring metal-tolerating rhizobia allows them to take roots, thus promoting their diversification in such environments [30].
The genetic mechanism of the metal-tolerating ability of symbionts indicates an intricate network of multiple genes that relate to biosorption, localized accumulation, detoxification, RNA methylation, expression of antioxidant genes, hormone synthesis, and improving membrane stability. The presence of an efflux system, which reduces accumulation, has been a common strategy used by the rhizobia against several heavy metals. Some rhizobial symbionts have high Ni biosorption and storage capabilities, limiting their mobility in the plant [31][32]. A strong positive relationship between low concentrations of As in the shoots of Medicago truncatula and reduced expression of the plant’s NRT3.1-like gene, which is a nitrate transporter, has been reported [33]. The expression of this transporter gene was induced by abscisic acid, but ammonium, which is the fixed form of nitrogen in Rhizobium, had an antagonistic effect. The Bradyrhizobium canariense L-7AH strain that was isolated from a metal mining site effectively formed a symbiotic relationship with the legume Lupinus albus at high concentrations of Hg (up to 102 mg kg−1 vermiculite) with no apparent reduction in photosynthesis or nitrogenase activities [34]. The tolerance mechanism of the strain is not clear; however, in another study, the Ensifer medicae strain mediated an increase in mercuric reductase activity in M. truncatula nodules to convert the highly toxic mercuric cation to a less toxic volatile mercury metal [35]. A positive correlation between Rhizobium-induced differential methylation and expression of m6A RNA in soybean plants under Cd stress indicates a different mechanism of metal toxicity remediation [36]. Rhizobia-induced accumulation of Cu in M. sativa roots and increased expression of antioxidants have also been observed [37]. Another mechanism of excess Cu tolerance involves Cu homeostasis catalyzed by the multicopper oxidase CuO and a copper chaperone [38]. Legumes that can grow successfully in Al-stressed soil have evolved specific tolerance mechanisms such as prevention of metal uptake through the cell membrane and increased production of extracellular exopolysaccharides [39]. In a recent study, the differentially expressed genes under Al stress were linked to extracellular EPS, biofilm formation and cell membrane-stabilizing proteins in Rhizobium phaseoli [40].
With the recent advances in recombinant technology, genetic improvements in the symbiotic rhizobia for improved metal stress tolerance in legumes may be a way forward. In this context, the intrinsic abilities of rhizobial and non-rhizobial species that can tolerate metal-induced stresses may be considered as resources for the exploitation of novel metal-tolerant factors that can be used in different legumes and perhaps non-legume plants. For instance, genetically improved Rhizobium pusense KG2, a Cd2+ immobilizing strain, exhibited a substantial reduction in Cd absorption while enhancing root and shoot length, biomass, nitrogen contents, and superoxide dismutase activity [41]. After transferring the arsenite S-adenosylmethionine methyltransferase gene from Chlamydomonas reinhardtii into Rhizobium leguminosarum, there was an enhanced As tolerance in the Rhizobium, which methylated and volatilized the heavy metal [42]. This is an example that provides a sustainable remediation strategy for As-contaminated soils. Thus, recombinant DNA technology-based exploitation of metal resistance genes from other organisms, such as Cr resistance genes from Akaligenes eutrophus [43], is a promising technology for developing tolerant legumes of agricultural and ecological importance.
Table 1. A list of some symbiotic rhizobia that confers stress metal stress tolerance to legumes.

3. Tolerance to Drought, Salinity, and pH

Stresses caused by environmental factors such as drought, salinity, heat, and extremes of pH are among the major factors affecting plant growth and development. These environmental factors may exacerbate with the changing climate, thereby causing an adverse impact on agricultural production. The rhizobial symbionts that can confer legumes with tolerance against different types of stresses have been summarized in Table 2.
Drought reduces transpiration and water movement in legumes, thus restricting the circulation of nitrogen fixation products and inhibiting nitrogenase activity [57][58][59][60]. It also reduces biomass and chlorophyll contents and accumulates reactive oxygen species that can disrupt the functioning of different biomolecules including DNA [61][62][63]. Production of antioxidants (e.g., superoxide dismutase, catalase, ascorbic acid, and glutathione) and osmoprotectants (molecules that maintain the balance of osmotic potential in cells) are among the common responses to drought stress in most legumes [62]. There are many examples of rhizobial symbionts that confer drought tolerance to legumes, such as B. diazoefficiens SEMIA 5080 in soybean R01-581F, Mesorhizobium huakuii 7653R in Astragalus sinicus L., and S. medicae or S. meliloti in M. truncatula [64][65][66]. Inoculation of R. meliloti in kidney bean, black bean, mung bean, and chickpea increased the number of nodules and improved photosynthesis under water-deficient conditions [67]. Similarly, S. fredii strain SMH12 was shown to improve the number of nodules and the water potentials in soybean grown under drought stress [68]. Rhizobium-induced increases in antioxidant enzyme production [69], accumulation of osmoprotectants including proline and soluble sugars in nodules and roots [70], or genes that encode enzymes involved in trehalose synthesis [71] were associated with drought stress.
Soil salinity, which is strongly related to drought and gets intensified with the use of saline water for irrigation [72][73][74][75], is among the key factors affecting the efficiency of legume–rhizobia symbiosis [76]. It causes the accumulation of toxic ions in soil [77] and is correlated with poor-quality flavonoids in the root exudates of legumes, which affect the production of nod factors [78]. By influencing the early stage of legume–rhizobia interaction involving chemical communication and colonization or infection of root hairs, salt stress can result in poor establishment of legume–rhizobia symbiosis. The reduction in rhizobial infections under salt stress was observed in many legumes such as bean [79], soybean [80], pea [81], and chickpea [82], which resulted in reduced nitrogen fixation [83]. Some rhizobia are able to modulate the host’s response to salinity by inducing indole-3-acetic acid production and accumulation of osmoprotectant molecules [84], increasing root osmotic water flow via reducing xylem osmotic potential and increasing the amount of aquaporins [85], and changing the protein profile of the host plant [86]. It is unclear if the production of nod factors under high salt conditions would be as effective as in the normal situation although some similarities have been noticed [87].
pH is known to influence soil properties and nutrient availability, and hence the functioning of the soil microbial community. Most soil microbes including root-nodulating rhizobia prefer a near-neutral pH, whereas a large proportion of the global arable land is either acidic or alkaline [88]. Extreme pH conditions can affect the establishment of legume–rhizobia symbiosis [89], as a delay in nodulation under acidic conditions has been observed in many legume plants [90]. The fact that supplementation of molecules such as genistein, a nod gene inducer that reverses the effects of acidic conditions on the establishment of legume–rhizobia symbiosis [91], suggests that expression of symbiosis signals is influenced by pH [92][93][94]. Soil pH can also influence the structure of the rhizosphere community [95], which can have a significant influence on plant roots [96][97]. The legumes thriving in acidic soils have evolved tolerance mechanisms for soil acidic conditions through the production of nod factors that are different from those produced under neutral pH conditions [98]. The studies indicate a role for the rhizobia-specific genes actA, typA, atvA, lpiA, and ubiF in improving acid stress tolerance and symbiotic competitiveness [99][100][101][102]. R. tropici CIAT899, a highly acid-tolerant strain [103], induces the production of glutathione [104]. The bacterium could produce more (~1.8-fold) Nod factors in acidic than neutral growth conditions, and about half of them were different from the normal profile [98]. The rhizobial strains have displayed tolerance to conditions ranging from highly acidic [105][106] to highly alkaline [107]. The defense response to high pH includes an increase in antioxidants, organic acid production, and changes in certain proteins [108].
Species that are naturally tolerant to environmental stress could be exploited for developing tolerant rhizobial strains. Alternatively, a genetic engineering route could be adopted for strain improvement, as has been demonstrated through overproduction of cytokinin, trehalose-6-phosphate synthase, 1-aminocyclopropane-1-carboxylic acid deaminase, high-affinity cytochrome cbb3-type oxidase, indole-3 acetic acid, and flavodoxin [109][110][111][112][113][114].
Table 2. Symbiotic rhizobia that confer environmental stress tolerance to legumes.
Symbiotic Rhizobia Co-Inoculants Legume Host Stress Beneficial Effects on the Plant Reference
Mesorhizobium huakuii strain 7653R   Astragalus sinicus Drought Improved N fixation and NH4+ assimilation [65]
Sinorhizobium medicae or S. meliloti   Medicago truncatula Enhanced allocation of reserves to osmolytes [66]
Sinorhizobium meliloti   Kidney bean, black bean, mung bean, and chickpea Improved nodule number and photosynthesis [67]
Rhizobium meliloti   Medicago sativa Enhanced antioxidants [69]
Sinorhizobium fredii strain SMH12   Soybean Improved nodule number and water potentials [68]
Rhizobium leguminosarum   Faba bean Enhanced production of osmoprotectants [70]
Rhizobium tropici CIAT 899 Paenibacillus polymyxa spp. Phaselus vulgaris Increased leaf abscisic acid content [115]
IAA-overproducing Ensifer meliloti 1021 (Ms-RD64)   Medicago sativa Enhanced production of low-molecular-weight osmolytes [109]
Bradyrhizobium sp. SUTN9-2   Mung bean Enhanced ACC deaminase activity [110]
Rhizobium etli   Phaseolus vulgaris Overexpressed Trehalose-6-Phosphate Synthase [111]
Rhizobium etli   Phaseolus vulgaris Enhanced expression of Cytochrome cbb(3) oxidases [112]
Sinorhizobium meliloti   Alfalfa Overexpressed cytokinin and antioxidant enzymes [113]
Bradyrhizobium RJS9-2   Stylosanthes guianensis Salinity Induced IAA production, enhanced osmoprotectant accumulation [84]
Rhizobium leguminosarum   Phaseolus vulgaris Contributed to enhanced root osmotic water flow [85]
Rhizobium phaseoli M1, M6, and M9 Pseudomonas spp. Mung bean Expressed ACC deaminase [116]
Mesorhizobium ciceri IC53 Bacilus subtilis NUU4 Cicer arietinum. Increased proline contents [117]
Rhizobium meliloti   Medicago sativa Modulated key plant processes (efficient use of resources, oxidative stress, ion homeostasis) [87]
Sinorhizobium meliloti     Overexpressed flavodoxin (Cyanobacterial origin) [114]
Rhizobium tropici CIAT899   Phaseolus vulgaris pH Modulated rhizobial nod factors production [98]
Rhizobium tropici CIAT899   Phaseolus vulgaris Induced production of glutathione in beans [118]
Sinorhizobium meliloti   Medicago sativa   Adaptive acid-tolerance response [105]
Rhizobium spp.   Medicago sativa Longmu 806 Antioxidants and organic acids production [108]

References

  1. Niklas, K.J.; Tiffney, B.H.; Knoll, A.H. Patterns in vascular land plant diversification. Nature 1983, 303, 614–616.
  2. Friis, E.M.; Crane, P.R.; Pedersen, K.R. Early Flowers and Angiosperm Evolution; Cambridge University Press: Cambridge, UK, 2011; Available online: https://www.cambridge.org/9780521592833 (accessed on 27 March 2023).
  3. Crepet, W.L.; Niklas, K.J. Darwin’s second ‘abominable mystery’: Why are there so many angiosperm species? Am. J. Bot. 2009, 96, 366–381.
  4. Joppa, L.N.; Roberts, D.L.; Pimm, S.L. How many species of flowering plants are there? Proc. R. Soc. B Biol. Sci. 2011, 278, 554–559.
  5. Claramunt, S.; Derryberry, E.P.; Brumfield, R.T.; Remsen, J.V., Jr. Ecological opportunity and diversification in a continental radiation of birds: Climbing adaptations and cladogenesis in the Furnariidae. Am. Nat. 2012, 179, 649–666.
  6. le Roux, M.M.; Miller, J.T.; Waller, J.; Döring, M.; Bruneau, A. An expert curated global legume checklist improves the accuracy of occurrence, biodiversity and taxonomic data. Sci. Data 2022, 9, 708.
  7. Linder, H.P. Plant species radiations: Where, when, why? Philos. Trans. R. Soc. B Biol. Sci. 2008, 363, 3097–3105.
  8. Li, H.; Wang, W.; Lin, L.; Zhu, X.; Zhu, X.; Li, J.; Chen, Z. Diversification of the phaseoloid legumes: Effects of climate change, range expansion and habit shift. Front. Plant Sci. 2013, 4, 386.
  9. Roy, S.; Liu, W.; Nandety, R.S.; Crook, A.; Mysore, K.S.; Pislariu, C.I.; Frugoli, J.; Dickstein, R.; Udvardi, M.K. Celebrating 20 years of genetic discoveries in legume nodulation and symbiotic nitrogen fixation. Plant Cell 2020, 32, 15–41.
  10. Rahimlou, S.; Bahram, M.; Tedersoo, L. Phylogenomics reveals the evolution of root nodulating alpha- and beta-Proteobacteria (rhizobia). Microbiol. Res. 2021, 250, 126788.
  11. Liu, S.; Jiao, J.; Tian, C.-F. Adaptive Evolution of Rhizobial Symbiosis beyond Horizontal Gene Transfer: From Genome Innovation to Regulation Reconstruction. Genes 2023, 14, 274.
  12. Quides, K.W.; Weisberg, A.J.; Trinh, J.; Salaheldine, F.; Cardenas, P.; Lee, H.H.; Jariwala, R.; Chang, J.H.; Sachs, J.L. Experimental evolution can enhance benefits of rhizobia to novel legume hosts. Proc. Biol. Sci. 2021, 288, 20210812.
  13. Zhong, Y.; Yang, Y.; Liu, P.; Xu, R.; Rensing, C.; Fu, X.; Liao, H. Genotype and rhizobium inoculation modulate the assembly of soybean rhizobacterial communities. Plant Cell Environ. 2019, 42, 2028–2044.
  14. Skorupska, A.; Janczarek, M.; Marczak, M.; Mazur, A.; Król, J. Rhizobial exopolysaccharides: Genetic control and symbiotic functions. Microb. Cell Factories 2006, 5, 7.
  15. Kubier, A.; Wilkin, R.T.; Pichler, T. Cadmium in soils and groundwater: A review. Appl. Geochem. 2019, 108, 104388.
  16. Mir, A.R.; Pichtel, J.; Hayat, S. Copper: Uptake, toxicity and tolerance in plants and management of Cu-contaminated soil. Biometals 2021, 34, 737–759.
  17. Oliveira, H. Chromium as an Environmental Pollutant: Insights on Induced Plant Toxicity. J. Bot. 2012, 2012, 375843.
  18. Sharma, P.; Dubey, R. Lead Toxicity in Plants. Braz. J. Plant Physiol. 2005, 17, 35–52.
  19. Farooq, M.A.; Islam, F.; Ali, B.; Najeeb, U.; Mao, B.; Gill, R.A.; Yan, G.; Siddique, K.H.M.; Zhou, W. Arsenic toxicity in plants: Cellular and molecular mechanisms of its transport and metabolism. Environ. Exp. Bot. 2016, 132, 42–52.
  20. Chaudri, A.M.; McGrath, S.P.; Giller, K.E. Survival of the indigenous population of Rhizobium leguminosarum biovar trifolii in soil spiked with Cd, Zn, Cu and Ni salts. Soil Biol. Biochem. 1992, 24, 625–632.
  21. Chen, Y.X.; He, Y.F.; Yang, Y.; Yu, Y.L.; Zheng, S.J.; Tian, G.M.; Luo, Y.M.; Wong, M.H. Effect of cadmium on nodulation and N2-fixation of soybean in contaminated soils. Chemosphere 2003, 50, 781–787.
  22. Chubukova, O.V.; Postrigan’, B.N.; Baimiev, A.K.; Chemeris, A.V. The effect of cadmium on the efficiency of development of legume-rhizobium symbiosis. Biol. Bull. 2015, 42, 458–462.
  23. Laguerre, G.; Courde, L.; Nouaïm, R.; Lamy, I.; Revellin, C.; Breuil, M.C.; Chaussod, R. Response of rhizobial populations to moderate copper stress applied to an agricultural soil. Microb. Ecol. 2006, 52, 426–435.
  24. Mandal, S.M.; Gouri, S.S.; De, D.; Das, B.K.; Mondal, K.C.; Pati, B.R. Effect of Arsenic on Nodulation and Nitrogen Fixation of Blackgram (Vigna mungo). Indian J. Microbiol. 2011, 51, 44–47.
  25. Mondal, N.K.; Das, C.; Datta, J.K. Effect of mercury on seedling growth, nodulation and ultrastructural deformation of Vigna radiata (L) Wilczek. Environ. Monit Assess. 2015, 187, 241.
  26. Neumann, H.; Bode-Kirchhoff, A.; Madeheim, A.; Wetzel, A. Toxicity testing of heavy metals with the Rhizobium-legume symbiosis: High sensitivity to cadmium and arsenic compounds. Environ. Sci. Pollut. Res. Int. 1998, 5, 28–36.
  27. Sheirdil, R.A.; Bashir, K.; Hayat, R.; Akhtar, M.S. Effect of cadmium on soybean (Glycine max L.) growth and nitrogen fixation. Afr. J. Biotechnol. 2012, 11, 1886–1891.
  28. Talano, M.A.; Cejas, R.B.; González, P.S.; Agostini, E. Arsenic effect on the model crop symbiosis Bradyrhizobium-soybean. Plant Physiol. Biochem. 2013, 63, 8–14.
  29. Mengoni, A.; Schat, H.; Vangronsveld, J. Plants as extreme environments? Ni-resistant bacteria and Ni-hyperaccumulators of serpentine flora. Plant Soil 2010, 331, 5–16.
  30. Fagorzi, C.; Checcucci, A.; diCenzo, G.C.; Debiec-Andrzejewska, K.; Dziewit, L.; Pini, F.; Mengoni, A. Harnessing Rhizobia to Improve Heavy-Metal Phytoremediation by Legumes. Genes 2018, 9, 542.
  31. Elbagory, M.; El-Nahrawy, S.; Omara, A.E. Synergistic Interaction between Symbiotic N(2) Fixing Bacteria and Bacillus strains to Improve Growth, Physiological Parameters, Antioxidant Enzymes and Ni Accumulation in Faba Bean Plants (Vicia faba) under Nickel Stress. Plants 2022, 11, 1812.
  32. Wani, P.A.; Khan, M.S. Nickel detoxification and plant growth promotion by multi metal resistant plant growth promoting Rhizobium species RL9. Bull. Environ. Contam. Toxicol. 2013, 91, 117–124.
  33. Ye, L.; Yang, P.; Zeng, Y.; Li, C.; Jian, N.; Wang, R.; Huang, S.; Yang, R.; Wei, L.; Zhao, H.; et al. Rhizobium symbiosis modulates the accumulation of arsenic in Medicago truncatula via nitrogen and NRT3.1-like genes regulated by ABA and linalool. J. Hazard. Mater. 2021, 415, 125611.
  34. Quiñones, M.A.; Ruiz-Díez, B.; Fajardo, S.; López-Berdonces, M.A.; Higueras, P.L.; Fernández-Pascual, M. Lupinus albus plants acquire mercury tolerance when inoculated with an Hg-resistant Bradyrhizobium strain. Plant Physiol. Biochem. 2013, 73, 168–175.
  35. Arregui, G.; Hipólito, P.; Pallol, B.; Lara-Dampier, V.; García-Rodríguez, D.; Varela, H.P.; Tavakoli Zaniani, P.; Balomenos, D.; Paape, T.; Coba de la Peña, T.; et al. Mercury-Tolerant Ensifer medicae Strains Display High Mercuric Reductase Activity and a Protective Effect on Nitrogen Fixation in Medicago truncatula Nodules Under Mercury Stress. Front. Plant Sci. 2020, 11, 560768.
  36. Han, X.; Wang, J.; Zhang, Y.; Kong, Y.; Dong, H.; Feng, X.; Li, T.; Zhou, C.; Yu, J.; Xin, D.; et al. Changes in the m6A RNA methylome accompany the promotion of soybean root growth by rhizobia under cadmium stress. J. Hazard. Mater. 2022, 441, 129843.
  37. Chen, J.; Liu, Y.Q.; Yan, X.W.; Wei, G.H.; Zhang, J.H.; Fang, L.C. Rhizobium inoculation enhances copper tolerance by affecting copper uptake and regulating the ascorbate-glutathione cycle and phytochelatin biosynthesis-related gene expression in Medicago sativa seedlings. Ecotoxicol. Env. Saf. 2018, 162, 312–323.
  38. Lu, M.; Jiao, S.; Gao, E.; Song, X.; Li, Z.; Hao, X.; Rensing, C.; Wei, G. Transcriptome Response to Heavy Metals in Sinorhizobium meliloti CCNWSX0020 Reveals New Metal Resistance Determinants That Also Promote Bioremediation by Medicago lupulina in Metal-Contaminated Soil. Appl. Environ. Microbiol. 2017, 83, e01244-17.
  39. Avelar Ferreira, P.A.; Bomfeti, C.A.; Lima Soares, B.; de Souza Moreira, F.M. Efficient nitrogen-fixing Rhizobium strains isolated from amazonian soils are highly tolerant to acidity and aluminium. World J. Microbiol. Biotechnol. 2012, 28, 1947–1959.
  40. Wekesa, C.; Muoma, J.O.; Reichelt, M.; Asudi, G.O.; Furch, A.C.U.; Oelmüller, R. The Cell Membrane of a Novel Rhizobium phaseoli Strain Is the Crucial Target for Aluminium Toxicity and Tolerance. Cells 2022, 11, 873.
  41. Li, Y.; Yu, X.; Cui, Y.; Tu, W.; Shen, T.; Yan, M.; Wei, Y.; Chen, X.; Wang, Q.; Chen, Q.; et al. The potential of cadmium ion-immobilized Rhizobium pusense KG2 to prevent soybean root from absorbing cadmium in cadmium-contaminated soil. J. Appl. Microbiol. 2019, 126, 919–930.
  42. Zhang, J.; Xu, Y.; Cao, T.; Chen, J.; Rosen, B.P.; Zhao, F.J. Arsenic methylation by a genetically engineered Rhizobium-legume symbiont. Plant Soil 2017, 416, 259–269.
  43. Nies, A.; Nies, D.H.; Silver, S. Nucleotide sequence and expression of a plasmid-encoded chromate resistance determinant from Alcaligenes eutrophus. J. Biol. Chem. 1990, 265, 5648–5653.
  44. Wani, P.A.; Khan, M.S.; Zaidi, A. Effect of metal tolerant plant growth promoting Bradyrhizobium sp. (vigna) on growth, symbiosis, seed yield and metal uptake by greengram plants. Chemosphere 2007, 70, 36–45.
  45. Wani, P.A.; Khan, M.S.; Zaidi, A. Effect of metal-tolerant plant growth-promoting Rhizobium on the performance of pea grown in metal-amended soil. Arch. Environ. Contam. Toxicol. 2008, 55, 33–42.
  46. Shoaib, M.; Hussain, S.; Cheng, X.; Cui, Y.; Liu, H.; Chen, Q.; Ma, M.; Gu, Y.; Zhao, K.; Xiang, Q.; et al. Synergistic anti-oxidative effects of Pongamia pinnata against nickel mediated by Rhizobium pisi and Ochrobacterium pseudogrignonense. Ecotoxicol. Environ. Saf. 2021, 217, 112244.
  47. Yu, X.; Shoaib, M.; Cheng, X.; Cui, Y.; Hussain, S.; Yan, J.; Zhou, J.; Chen, Q.; Gu, Y.; Zou, L.; et al. Role of rhizobia in promoting non-enzymatic antioxidants to mitigate nitrogen-deficiency and nickel stresses in Pongamia pinnata. Ecotoxicol. Environ. Saf. 2022, 241, 113789.
  48. Reichman, S.M. The potential use of the legume–rhizobium symbiosis for the remediation of arsenic contaminated sites. Soil Biol. Biochem. 2007, 39, 2587–2593.
  49. Armendariz, A.L.; Talano, M.A.; Olmos Nicotra, M.F.; Escudero, L.; Breser, M.L.; Porporatto, C.; Agostini, E. Impact of double inoculation with Bradyrhizobium japonicum E109 and Azospirillum brasilense Az39 on soybean plants grown under arsenic stress. Plant Physiol. Biochem. 2019, 138, 26–35.
  50. Wani, P.A.; Khan, M.S.; Zaidi, A. Effects of heavy metal toxicity on growth, symbiosis, seed yield and metal uptake in pea grown in metal amended soil. Bull Environ. Contam. Toxicol. 2008, 81, 152–158.
  51. Ghnaya, T.; Mnassri, M.; Ghabriche, R.; Wali, M.; Poschenrieder, C.; Lutts, S.; Abdelly, C. Nodulation by Sinorhizobium meliloti originated from a mining soil alleviates Cd toxicity and increases Cd-phytoextraction in Medicago sativa L. Front. Plant Sci. 2015, 6, 863.
  52. Wani, P.A.; Khan, M.S.; Zaidi, A. Chromium-reducing and plant growth-promoting Mesorhizobium improves chickpea growth in chromium-amended soil. Biotechnol. Lett. 2008, 30, 159–163.
  53. Dhali, S.; Pradhan, M.; Sahoo, R.K.; Mohanty, S.; Pradhan, C. Alleviating Cr(VI) stress in horse gram (Macrotyloma uniflorum Var. Madhu) by native Cr-tolerant nodule endophytes isolated from contaminated site of Sukinda. Environ. Sci. Pollut. Res. Int. 2021, 28, 31717–31730.
  54. Wu, L.; Lin, S.L. Copper tolerance and copper uptake of Lotus purshianus (Benth.) Clem. & Clem. and its symbiotic Rhizobium loti derived from a copper mine waste population. New Phytol. 1990, 116, 531–539.
  55. Duan, C.; Mei, Y.; Wang, Q.; Wang, Y.; Li, Q.; Hong, M.; Hu, S.; Li, S.; Fang, L. Rhizobium Inoculation Enhances the Resistance of Alfalfa and Microbial Characteristics in Copper-Contaminated Soil. Front. Microbiol. 2021, 12, 781831.
  56. Dary, M.; Chamber-Perez, M.A.; Palomares, A.J.; Pajuelo, E. In situ phytostabilisation of heavy metal polluted soils using Lupinus luteus inoculated with metal resistant plant-growth promoting rhizobacteria. J. Hazard. Mater. 2010, 177, 323–330.
  57. Marino, D.; Frendo, P.; Ladrera, R.; Zabalza, A.; Puppo, A.; Arrese-Igor, C.; Gonzalez, E.M. Nitrogen fixation control under drought stress. Localized or systemic? Plant Physiol. 2007, 143, 1968–1974.
  58. McCulloch, L.A.; Piotto, D.; Porder, S. Drought and soil nutrients effects on symbiotic nitrogen fixation in seedlings from eight Neotropical legume species. Biotropica 2021, 53, 703–713.
  59. Serraj, R.; Sinclair, T.R.; Purcell, L.C. Symbiotic N2 fixation response to drought. J. Exp. Bot. 1999, 50, 143–155.
  60. Streeter, J.G. Effects of drought on nitrogen fixation in soybean root nodules. Plant Cell Environ. 2003, 26, 1199–1204.
  61. Cruz de Carvalho, M.H. Drought stress and reactive oxygen species: Production, scavenging and signaling. Plant Signal. Behav. 2008, 3, 156–165.
  62. Sarker, U.; Oba, S. Drought Stress Effects on Growth, ROS Markers, Compatible Solutes, Phenolics, Flavonoids, and Antioxidant Activity in Amaranthus tricolor. Appl. Biochem. Biotechnol. 2018, 186, 999–1016.
  63. You, J.; Chan, Z. ROS Regulation During Abiotic Stress Responses in Crop Plants. Front. Plant Sci. 2015, 6, 1092.
  64. Cerezini, P.; Kuwano, B.H.; Grunvald, A.K.; Hungria, M.; Nogueira, M.A. Soybean tolerance to drought depends on the associated Bradyrhizobium strain. Braz. J. Microbiol. 2020, 51, 1977–1986.
  65. Liu, Y.; Guo, Z.; Shi, H. Rhizobium Symbiosis Leads to Increased Drought Tolerance in Chinese Milk Vetch (Astragalus sinicus L.). Agronomy 2022, 12, 725.
  66. Staudinger, C.; Mehmeti-Tershani, V.; Gil-Quintana, E.; Gonzalez, E.M.; Hofhansl, F.; Bachmann, G.; Wienkoop, S. Evidence for a rhizobia-induced drought stress response strategy in Medicago truncatula. J. Proteom. 2016, 136, 202–213.
  67. Siddiqui, Z.S.; Ali, F.; Uddin, Z. Sustainable effect of a symbiotic nitrogen-fixing bacterium Sinorhizobium meliloti on nodulation and photosynthetic traits of four leguminous plants under low moisture stress environment. Lett. Appl. Microbiol. 2021, 72, 714–724.
  68. Kibido, T.; Kunert, K.; Makgopa, M.; Greve, M.; Vorster, J. Improvement of rhizobium-soybean symbiosis and nitrogen fixation under drought. Food Energy Secur. 2020, 9, e177.
  69. Yang, P.; Zhang, P.; Li, B.; Hu, T. Effect of nodules on dehydration response in alfalfa (Medicago sativa L.). Environ. Exp. Bot. 2013, 86, 29–34.
  70. Amine-Khodja, I.R.; Boscari, A.; Riah, N.; Kechid, M.; Maougal, R.T.; Belbekri, N.; Djekoun, A. Impact of Two Strains of Rhizobium leguminosarum on the Adaptation to Terminal Water Deficit of Two Cultivars Vicia faba. Plants 2022, 11, 515.
  71. Yadav, A.; Singh, R.P.; Singh, A.L.; Singh, M. Identification of genes involved in phosphate solubilization and drought stress tolerance in chickpea symbiont Mesorhizobium ciceri Ca181. Arch. Microbiol. 2021, 203, 1167–1174.
  72. Corwin, D.L. Climate change impacts on soil salinity in agricultural areas. Eur. J. Soil Sci. 2020, 72, 842–862.
  73. Tedeschi, A.; Dell’Aquila, R. Effects of irrigation with saline waters, at different concentrations, on soil physical and chemical characteristics. Agric. Water Manag. 2005, 77, 308–322.
  74. Wang, Q.; Huo, Z.; Zhang, L.; Wang, J.; Zhao, Y. Impact of saline water irrigation on water use efficiency and soil salt accumulation for spring maize in arid regions of China. Agric. Water Manag. 2016, 163, 125–138.
  75. Gul, Z.; Tang, Z.-H.; Arif, M.; Ye, Z. An Insight into Abiotic Stress and Influx Tolerance Mechanisms in Plants to Cope in Saline Environments. Biology 2022, 11, 597.
  76. Chakraborty, S.; Harris, J.M. At the Crossroads of Salinity and Rhizobium-Legume Symbiosis. Mol. Plant Microbe Interact. 2022, 35, 540–553.
  77. Yadav, N.K.; Vyas, S.R. Salt and pH tolerance of Rhizobia. Folia Microbiol. 1973, 18, 242–247.
  78. Dardanelli, M.S.; Manyani, H.; González-Barroso, S.; Rodríguez-Carvajal, M.A.; Gil-Serrano, A.M.; Espuny, M.R.; López-Baena, F.J.; Bellogín, R.A.; Megías, M.; Ollero, F.J. Effect of the presence of the plant growth promoting rhizobacterium (PGPR) Chryseobacterium balustinum Aur9 and salt stress in the pattern of flavonoids exuded by soybean roots. Plant Soil 2009, 328, 483–493.
  79. Zahran, H.H.; Sprent, J.I. Effects of sodium chloride and polyethylene glycol on root-hair infection and nodulation of Vicia faba L. plants by Rhizobium leguminosarum. Planta 1986, 167, 303–309.
  80. Tu, J.C. Effect of salinity on rhizobium-root-hair interaction, nodulation and growth of soybean. Can. J. Plant Sci. 1981, 61, 231–239.
  81. Borucki, W.; Sujkowska, M. The effects of sodium chloride-salinity upon growth, nodulation, and root nodule structure of pea (Pisum sativum L.) plants. Acta Physiol. Plant. 2007, 30, 293–301.
  82. L’Taief, B.; Sifi, B.; Zaman-Allah, M.; Drevon, J.J.; Lachaâl, M. Effect of salinity on root-nodule conductance to the oxygen diffusion in the Cicer arietinum-Mesorhizobium ciceri symbiosis. J. Plant Physiol. 2007, 164, 1028–1036.
  83. Aridhi, F.; Sghaier, H.; Gaitanaros, A.; Khadri, A.; Aschi-Smiti, S.; Brouquisse, R. Nitric oxide production is involved in maintaining energy state in Alfalfa (Medicago sativa L.) nodulated roots under both salinity and flooding. Planta 2020, 252, 22.
  84. Dong, R.; Zhang, J.; Huan, H.; Bai, C.; Chen, Z.; Liu, G. High Salt Tolerance of a Bradyrhizobium Strain and Its Promotion of the Growth of Stylosanthes guianensis. Int. J. Mol. Sci. 2017, 18, 1625.
  85. Franzini, V.I.; Azcón, R.; Ruiz-Lozano, J.M.; Aroca, R. Rhizobial symbiosis modifies root hydraulic properties in bean plants under non-stressed and salinity-stressed conditions. Planta 2019, 249, 1207–1215.
  86. Wang, Y.; Yang, P.; Zhou, Y.; Hu, T.; Zhang, P.; Wu, Y. A proteomic approach to understand the impact of nodulation on salinity stress response in alfalfa (Medicago sativa L.). Plant Biol. 2022, 24, 323–332.
  87. Pérez-Montaño, F.; del Cerro, P.; Jiménez-Guerrero, I.; López-Baena, F.J.; Cubo, M.T.; Hungria, M.; Megías, M.; Ollero, F.J. RNA-seq analysis of the Rhizobium tropici CIAT 899 transcriptome shows similarities in the activation patterns of symbiotic genes in the presence of apigenin and salt. BMC Genom. 2016, 17, 198.
  88. López-Bucio, J.; Guevara-Garcia, A.; Ramírez-Rodríguez, V.; Nieto Jacobo, M.; de la Fuente Martínez, J.; Herrera-Estrella, L. Agriculture for Marginal Lands: Transgenic Plants Towards the Third Millennium. Dev. Plant Genet. Breed. 2000, 5, 159–165.
  89. Ferguson, B.J.; Lin, M.H.; Gresshoff, P.M. Regulation of legume nodulation by acidic growth conditions. Plant Signal. Behav. 2013, 8, e23426.
  90. Cooper, J.E. Nodulation of Legumes by Rhizobia in Acid Soils. In Developments in Soil Science; Vančura, V., Kunc, F., Eds.; Elsevier: Amsterdam, The Netherlands, 1989; Volume 18, pp. 57–61.
  91. Hungria, M.; Stacey, G. Molecular signals exchanged between host plants and rhizobia: Basic aspects and potential application in agriculture. Soil Biol. Biochem. 1997, 29, 819–830.
  92. Miransari, M.; Balakrishnan, P.; Smith, D.; Mackenzie, A.F.; Bahrami, H.A.; Malakouti, M.J.; Rejali, F. Overcoming the Stressful Effect of Low pH on Soybean Root Hair Curling using Lipochitooligosacharides. Commun. Soil Sci. Plant Anal. 2006, 37, 1103–1110.
  93. Richardson, A.E.; Simpson, R.J.; Djordjevic, M.A.; Rolfe, B.G. Expression of Nodulation Genes in Rhizobium leguminosarum biovar trifolii is Affected by Low pH and by Ca and Al Ions. Appl Environ. Microbiol 1988, 54, 2541–2548.
  94. Ferreira, T.C.; Aguilar, J.V.; Souza, L.A.; Justino, G.C.; Aguiar, L.F.; Camargos, L.S. pH effects on nodulation and biological nitrogen fixation in Calopogonium mucunoides. Braz. J. Bot. 2016, 39, 1015–1020.
  95. Han, Q.; Ma, Q.; Chen, Y.; Tian, B.; Xu, L.; Bai, Y.; Chen, W.; Li, X. Variation in rhizosphere microbial communities and its association with the symbiotic efficiency of rhizobia in soybean. ISME J. 2020, 14, 1915–1928.
  96. Checcucci, A.; Marchetti, M. The Rhizosphere Talk Show: The Rhizobia on Stage. Front. Agron. 2020, 2, 591494.
  97. Mehboob, I.; Naveed, M.; Zahir, Z.A.; Sessitsch, A. Potential of Rhizosphere Bacteria for Improving Rhizobium-Legume Symbiosis. In Plant Microbe Symbiosis: Fundamentals and Advances; Arora, N., Ed.; Springer: New Delhi, India, 2013.
  98. Moron, B.; Soria-Diaz, M.E.; Ault, J.; Verroios, G.; Noreen, S.; Rodriguez-Navarro, D.N.; Gil-Serrano, A.; Thomas-Oates, J.; Megias, M.; Sousa, C. Low pH changes the profile of nodulation factors produced by Rhizobium tropici CIAT899. Chem. Biol. 2005, 12, 1029–1040.
  99. Kiss, E.; Huguet, T.; Poinsot, V.; Batut, J. The typA gene is required for stress adaptation as well as for symbiosis of Sinorhizobium meliloti 1021 with certain Medicago truncatula lines. Mol. Plant Microbe. Interact. 2004, 17, 235–244.
  100. Martini, M.C.; Vacca, C.; Torres Tejerizo, G.A.; Draghi, W.O.; Pistorio, M.; Lozano, M.J.; Lagares, A.; del Papa, M.F. ubiF is involved in acid stress tolerance and symbiotic competitiveness in Rhizobium favelukesii LPU83. Braz. J. Microbiol. 2022, 53, 1633–1643.
  101. Reeve, W.G.; Bräu, L.; Castelli, J.; Garau, G.; Sohlenkamp, C.; Geiger, O.; Dilworth, M.J.; Glenn, A.R.; Howieson, J.G.; Tiwari, R.P. The Sinorhizobium medicae WSM419 lpiA gene is transcriptionally activated by FsrR and required to enhance survival in lethal acid conditions. Microbiology 2006, 152, 3049–3059.
  102. Tiwari, S.; Sarangi, B.K.; Thul, S.T. Identification of arsenic resistant endophytic bacteria from Pteris vittata roots and characterization for arsenic remediation application. J. Environ. Manag. 2016, 180, 359–365.
  103. Martinez, E.; Pardo, M.A.; Palacios, R.; Miguel, A.C. Reiteration of Nitrogen Fixation Gene Sequences and Specificity of Rhizobium in Nodulation and Nitrogen Fixation in Phaseolus vulgaris. Microbiology 1985, 131, 1779–1786.
  104. Riccillo, P.M.; Muglia, C.I.; de Bruijn, F.J.; Roe, A.J.; Booth, I.R.; Aguilar, O.M. Glutathione is involved in environmental stress responses in Rhizobium tropici, including acid tolerance. J. Bacteriol. 2000, 182, 1748–1753.
  105. Draghi, W.O.; del Papa, M.F.; Pistorio, M.; Lozano, M.; de Los Angeles Giusti, M.; Torres Tejerizo, G.A.; Jofré, E.; Boiardi, J.L.; Lagares, A. Cultural conditions required for the induction of an adaptive acid-tolerance response (ATR) in Sinorhizobium meliloti and the question as to whether or not the ATR helps rhizobia improve their symbiosis with alfalfa at low pH. FEMS Microbiol. Lett. 2010, 302, 123–130.
  106. Soto, M.J.; Dillewijn, P.; Martínez-Abarca, F.; Jiménez-Zurdo, J.I.; Toro, N. Attachment to plant roots and nod gene expression are not affected by pH or calcium in the acid-tolerant alfalfa-nodulating bacteria Rhizobium sp. LPU83. FEMS Microbiol. Ecol. 2004, 48, 71–77.
  107. Kulkarni, S.; Nautiyal, C.S. Effects of salt and pH stress on temperature-tolerant Rhizobium sp. NBRI330 nodulating Prosopis juliflora. Curr. Microbiol. 2000, 40, 221–226.
  108. Song, T.; Sun, N.; Dong, L.; Cai, H. Enhanced alkali tolerance of rhizobia-inoculated alfalfa correlates with altered proteins and metabolic processes as well as decreased oxidative damage. Plant Physiol. Biochem. 2021, 159, 301–311.
  109. Defez, R.; Andreozzi, A.; Dickinson, M.; Charlton, A.; Tadini, L.; Pesaresi, P.; Bianco, C. Improved Drought Stress Response in Alfalfa Plants Nodulated by an IAA Over-producing Rhizobium Strain. Front. Microbiol. 2017, 8, 2466.
  110. Sarapat, S.; Songwattana, P.; Longtonglang, A.; Umnajkitikorn, K.; Girdthai, T.; Tittabutr, P.; Boonkerd, N.; Teaumroong, N. Effects of Increased 1-Aminocyclopropane-1-Carboxylate (ACC) Deaminase Activity in Bradyrhizobium sp. SUTN9-2 on Mung Bean Symbiosis under Water Deficit Conditions. Microbes Environ. 2020, 35, ME20024.
  111. Suárez, R.; Wong, A.; Ramírez, M.; Barraza, A.; Orozco Mdel, C.; Cevallos, M.A.; Lara, M.; Hernández, G.; Iturriaga, G. Improvement of drought tolerance and grain yield in common bean by overexpressing trehalose-6-phosphate synthase in rhizobia. Mol. Plant Microbe Interact. 2008, 21, 958–966.
  112. Talbi, C.; Sanchez, C.; Hidalgo-Garcia, A.; Gonzalez, E.M.; Arrese-Igor, C.; Girard, L.; Bedmar, E.J.; Delgado, M.J. Enhanced expression of Rhizobium etli cbb(3) oxidase improves drought tolerance of common bean symbiotic nitrogen fixation. J. Exp. Bot. 2012, 63, 5035–5043.
  113. Xu, J.; Li, X.L.; Luo, L. Effects of engineered Sinorhizobium meliloti on cytokinin synthesis and tolerance of alfalfa to extreme drought stress. Appl. Environ. Microbiol. 2012, 78, 8056–8061.
  114. Redondo, F.J.; Coba de la Peña, T.; Lucas, M.M.; Pueyo, J.J. Alfalfa nodules elicited by a flavodoxin-overexpressing Ensifer meliloti strain display nitrogen-fixing activity with enhanced tolerance to salinity stress. Planta 2012, 236, 1687–1700.
  115. Figueiredo, M.V.B.; Burity, H.A.; Martínez, C.R.; Chanway, C.P. Alleviation of drought stress in the common bean (Phaseolus vulgaris L.) by co-inoculation with Paenibacillus polymyxa and Rhizobium tropici. Appl. Soil Ecol. 2008, 40, 182–188.
  116. Ahmad, M.; Zahir, Z.A.; Asghar, H.N.; Asghar, M. Inducing salt tolerance in mung bean through coinoculation with rhizobia and plant-growth-promoting rhizobacteria containing 1-aminocyclopropane-1-carboxylate deaminase. Can. J. Microbiol. 2011, 57, 578–589.
  117. Egamberdieva, D.; Wirth, S.J.; Shurigin, V.V.; Hashem, A.; Abd Allah, E.F. Endophytic Bacteria Improve Plant Growth, Symbiotic Performance of Chickpea (Cicer arietinum L.) and Induce Suppression of Root Rot Caused by Fusarium solani under Salt Stress. Front. Microbiol. 2017, 8, 1887.
  118. Vinuesa, P.; Neumann-Silkow, F.; Pacios-Bras, C.; Spaink, H.P.; Martínez-Romero, E.; Werner, D. Genetic analysis of a pH-regulated operon from Rhizobium tropici CIAT899 involved in acid tolerance and nodulation competitiveness. Mol. Plant Microbe Interact. 2003, 16, 159–168.
More
Information
Subjects: Microbiology
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register : , ,
View Times: 120
Revisions: 2 times (View History)
Update Date: 16 Jun 2023
1000/1000