Legume–Rhizobial Symbiotic Interactions Beyond Nitrogen Fixation: History
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Contributor:
Ravinder K. Goyal
,
Ravinder Goyal
,
Jemaneh Z. Habtewold

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.
Symbiotic Rhizobia Co-Inoculant Legume Host Metal Beneficial Effects on the Plant Reference
Bradyrhizobium sp. RM8   Greengram Ni Reduced uptake of Ni and Zn [44]
Rhizobium sp. RP5   Pea Reduced uptake of Ni and Zn [45]
Rhizobium TAL–1148 Bacilus subtilis Faba bean Reduced uptake of Ni [31]
Rhizobium pisi Ochrobacterium pseudogrignonense Pongamia pinnata Ni accumulation in shoots and enhanced antioxidant activities [46]
Rhizobium pisi PZHK2 Ochrobacterium pseudo-grignonense PZHK4 Pongamia pinnata Enhanced activities of non-enzymatic antioxidants [47]
Bacilus japonicum CB1809   Soybean As Enhanced production of growth-promoting hormones [48]
Rizobium sp. VMA301   Black gram As accumulation in roots [24]
Rhizobium. meliloti Rm5038   Medicago truncatula Lowered accumulation of AS in shoots [33]
Bacilus japonicum E109 Azospirillum brasilense Az39 Soybean Reduced As translocation to shoots [49]
Recombinant R. leguminosarum bv. trifolii   Red clover Alleviated As stress [42]
Sinorhizobium medicae   Medicago truncatula Hg Alleviated Hg stress [35]
Bacilus canariense L-7AH   White lupin Limited mobility of Hg in roots [34]
Rhizobium leguminosarum RP 5   Pea Cd Accumulated Cd in roots [50]
Sinorhizobium meliloti   Medicago sativa Enhanced absorption in roots [51]
Sinorhizobium fredii HH103   Soybean Modulated methylation and expression of m6A RNA [36]
Rhizobium pusense KG2   Soybean Reduced Cd2+ absorption [41]
Mesorhizobium strain RC3   Chickpea Cr Reduced Cr uptake [52]
Rhizobium sp. AS05 Bacillus sp. AS03 Horse gram Reduced shoot translocation [53]
Rhizobium loti   Lotus purshianus Cu Accumulation of Cu [54]
Sinorhizobium meliloti   Medicago sativa Increased antioxidant activities [55]
Sinorhizobium meliloti   Medicago sativa Reduced Cu translocation [37]
Rhizobium spp.   Phaseolus vulgaris Al Production of exopolysaccharides [39]
Bacilus sp. 750 Pseudomonas sp., Ochrobactrum cytisi Lupinus luteus Pb Reduced metal accumulation in shoots and roots [56]

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]

This entry is adapted from the peer-reviewed paper 10.3390/microorganisms11061454

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