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AGRICULTURAL BIOLOGY, ISSN 2412-0324 (ВДЛ ed. Online)
2015, V. 50, № 3, pp. 267-277
(SEL’SKOKHOZYAISTVENNAYA BIOLOGIYA) ISSN 0131-6397 (Russian ed Print)
v_____________________________________' ISSN 2313-4836 (Russian ed. Online)
Molecular and cell symbiotic mechanisms
UDC 633.31/37:581.557.2:577.175.19 doi: 10.15389/agrobiology.2015.3.267rus
doi: 10.15389/agrobiology.2015.3.267eng
NEGATIVE HORMONAL REGULATION OF SYMBIOTIC NODULE DEVELOPMENT. I. ETHYLENE
(review)
A.V. TSYGANOVA, V.E. TSYGANOV
All-Russian Research Institute for Agricultural Microbiology, Federal Agency of Scientific Organizations, 3, sh.
Podbel’skogo, St. Petersburg, 196608 Russia, e-mail tsyganov@arriam.spb.ru
Acknowledgements:
Supported by Russian Science Foundation (project № 14-24-00135)
Received September 30, 2014
Abstract
The process of symbiotic nodule formation resulting from interaction between legume plants and rhizobia is controlled by both partners. From the plant side the important role belongs to a system of hormonal regulation, involving all classes of phytohormones identified in plants. Negative regulation of nodulation is very important for the plant since the symbiotic nodule formation is highly energy-consuming process. Moreover, nodules lacking nitrogen fixation might be formed during interaction with ineffective strain of rhizobia, and it is disadvantageous for the plant. Up to now, there are data about involving of four phytohormones into negative regulation of nodule formation: ethylene, abscisic, jasmonic and salicylic acids. In this review, the role of ethylene in negative regulation of nodulation is discussed. Ethylene negatively regulates the number of developing symbiotic nodules at different stages of their formation. The first negative effect of ethylene appears at the level of calcium spiking, triggered by Nod-factors produced by rhizobia. Further, ethylene negatively influences deformations of roots hairs, stimulated by Nod-factors, infection thread growth, as well as nodule primordium development. In tropical legume Sesbania rostrata Bremek. & Oberm. ethylene represses the activity of nodule meristem, leading to formation of determinate type of nodule (with temporal meristem activity), while at the absence of ethylene indeterminate nodules (with prolonged meristem activity) are formed. At the same time, it was found that in soybean Glycine max (L.) Merr., ethylene is not involved in regulation of nodulation. It seems that ethylene involvement into regulation of nodule formation is not strictly dependent on the type of nodules, since in the other legume plants, forming determinate nodules, number of nodules is negatively affected by ethylene. It is suggested that ethylene synthesis in inoculated roots is triggered by Nod-factors, which activate plant defense responses, leading to restriction of number of forming nodules. Hypernodulating mutant of Medicago truncatula Gaertn. sickle, carrying a mutation in the gene MtEIN2, which is the key component in ethylene signal transduction pathway, is characterized by decreased level of defense response activation, as it was shown by proteomic analysis. It is interesting that not only the plants, but rhizobia as well can control ethylene level in rhizosphere and therefore influence nodule number. One of such mechanisms is the synthesis of rhizobitoxin by some rhizobial strains, which has structural similarity with inhibitor of ethylene synthesis aminoethoxyvinilglycine (AVG). The other mechanism is more widespread among rhizobia and it deals with synthesis of ACC deaminase, an enzyme, which cleaves the precursor of ethylene synthesis 1-aminocyclopropane-1-carboxylic acid (ACC). Thus, regulation of ethylene level may be important for practical application, potentially allowing to increase plant’s ability to nodulation. However, it should be taken into account that nodule number is precisely regulated by the plant because nodule formation is very energy-consuming process. Even more, it is necessary to remember that ethylene stimulates development of root hairs and decrease of their level may influence an intake ability of root and lead to deficiency of nutrient elements.
Keywords: plant-microbe interactions, legume-rhizobial symbiosis, symbiotic nodule, phytohormones, ethylene, rhizobia, plant defense, ACC deaminase, rhizobitoxin.
Soil bacteria named rhizobia may be involved in symbiotic interaction with legumes and induce new root organs, nitrogen-fixing nodules [1, 2]. A signaling dialogue between rhizobia and legumes is the basis for the formation of nitrogen-fixing nodules [3].
Flavonoids excreted by legume roots induce the expression of nodule formation genes [4, 5]. As a result, rhizobia synthesize specific signaling molecules—lipochitooligosaccharides called Nod-factors [5]. In the last decade, genes of legumes involved in the initial stages of Nod-factor reception and signaling have been identified [3, 6, 7]. The signal triggers a variety of plant responses: membrane polarization, calcium oscillations in root hairs, and reorganization of their cytoskeleton elements [8]. As a result, root hair deformation and typical twisting occur. Simultaneously, cell division in the inner layers of root cortex and pericycle reactivates which results in nodule primordium formation [9]. Rhizobia infect symbiotic nodule tissue with tubular structures named infectious threads [9]. This leads to the output of bacteria into the cytoplasm of plant cells and to their differentiation induced by plant nodule-specific cysteine-rich peptides [10] into specialized forms, bacteroides [9, 11], able to fix atmospheric nitrogen to ammonium in plant host cells [12].
Phytohormones are important signaling molecules involved in the majority of physiological processes in plants. Obviously, they play an important role in the initiation, development and functioning of symbiotic nodules. To date, all phytohormone groups (auxin, cytokinin, ethylene, abscisic acid, jasmonic acid, salicylic acid, and gibberellin) have been shown to participate in the development of symbiotic nodules [13-19).
In this review, the role of ethylene in negative regulation of the development and functioning of symbiotic nodules is discussed.
Effect of ethylene on nodule formation. The negative effect of ethylene on the number and activity of developing nitrogen-fixing symbiotic nodules was identified over 40 years ago while studying various plants: pea (Pisum sativum L.) [20, 21], bean (Phaseolus vulgaris L.) [22)], and clover (Trifolium repens L.) [21]. At the same time, treatment of alfalfa (Medicago sativa L.) roots with the ethylene inhibitor aminoethoxyvinylglycine (AVG) has been shown to result in a 2-fold increase in the number of nodules developed, indicating ethylene involvement in regulation of nodule development in legumes [23]. Subsequently, it was confirmed that the inhibitors of ethylene synthesis and effect stimulate nodule development [24].
Ethylene was also suggested to mediate the negative effect of nitrates on nodule development, since treatment of alfalfa (M sativa) with AVG increased the number of nodules in plants exposed to nitrates [25]. At the same time, the studies of nitrate and light effect on nodule formation in Sparkle pea (P sativum) have demonstrated that nitrates block nodulation at early stages (before infectious thread development) compared with treatment with ethylene or light (the majority of infections were blocked in root hairs or cells of the outer cortex layers) [26]. Moreover, in plants grown under the exposure of nitrate (in contrast to exogenous ethylene), treatment with the inhibitors of ethylene effect (Ag+) restored the number of nodules on the main root only, not on lateral roots [26].
The effect of ethylene on nodule formation has been described in peas P sativum, white clover Melilotus alba annua Desr., and soybean Glycine max (L.) Merr. [27]. When treated with ethylene (0.07 |al/l), the number of nodules formed reduced two-fold in Sparkle and Rondo pea varieties. Increasing the amount of ethylene (0.45 ^l/l) resulted in complete inhibition of nodulation. Melilot showed similar sensitivity, while the number of nodules in soybean has not changed. Treatment with exogenous ethylene did not result in the decrease in the number of infections in pea plants and clover, but stopped their development in root hair cells or outer cortex layers. Thus, it was shown that ethylene may affect more than one stage of nodulation blocking both the growth of infectious
threads from epidermal cells to the outer cortex layers, and nodule primordium initiation [27].
Experiments with peas (P sativum) have demonstrated nodulation opposite to xylem poles [28]. Later, localization of ACC oxidase, an enzyme that controls the final stage of ethylene biosynthesis from 1-aminocyclopropane-1-carbo-xylic acid (ACC), has been shown. Treatment of roots with AVG or Ag+ resulted in formation of a part of nodules opposite to phloem poles. Thus, it was concluded that ethylene provides the location of symbiotic nodule initiation [29].
Inhibiting of nodulation at different stages of development by ethylene has been demonstrated using a model Medicago truncatula Gaertn. legume [30]. Moreover, the negative effect of ethylene was manifested since the earliest stages of symbiosis (before or during calcium oscillation caused by Nod-factors secreted by rhizobia). Also, ethylene inhibited root hair deformation and initiation of infection thread growth. Earlier, ethylene has been demonstrated to inhibit infection thread growth after its growth initiation in M. truncatula [31]. It has been suggested that multiple ethylene effects may be either due to the existence of inhibition of nodule formation at one early stage of development, or due to independent inhibiting of several stages of nodule development [30]. Activation of ethylene synthesis induced by inoculation of Sinorhizobum meliloti plants may regulate the number of successful infections terminated by formation of nodules by inhibiting further initiation of infections or by blockage of the emerging infectious threads [30].
A tropical legume Sesbania rostrata Bremek. & Oberm. is known to develop various types of nodules, i.e. determinate nodules (with limited meristem activity), or indeterminate nodules (with prolonged meristem activity) depending on depending on the growing conditions. Moreover, ethylene plays the leading role in the determining of nodule type: adding of its inhibitor (Ag+) to the substrate resulted in formation of indeterminate nodules, adding of ethephon (2-chloroethylphosphonic acid which decomposes with the evolution of ethylene) resulted in formation of determinate ones [32]. Thus, the negative effect of ethylene on the nodule meristem functioning has been shown.
The plants of Vicia sativa ssp. nigra (L.) Ehrh. inoculated with a strain of Rhizobium leguminosarum bv. viciae appeared to be an interesting model to study the role of ethylene in the regulation of nodulation. When growing in the light, they formed aberrant thick short roots («thick short root», a Tsr-phe-notype) with abnormal arrangement of nodules [33]. In the roots growing in light, rhizobia Nod-factors have been shown to induce an increased response expressed in overproduction of ethylene, with which the described phenotype is associated [34]. The Tsr-phenotype was accompanied by the changes in the transverse (relative to the longitudinal axis of the cell) microtubule organization resulting in the increase in cell diameter and thickened roots. Also, the Tsr-phenotype could be obtained by treating the roots with ethephon, and its expression was inhibited by treatment of plants with AVG, wherein nodulation of the main root was restored [34].
Genetic analysis of the role of ethylene in nodule formation. Further, the studies of the role of ethylene in nodule formation developed with adequate genetic models—symbiotic gene mutants exhibiting increased sensitivity or insensitivity to ethylene, transgenic plants with increased or decreased production of ethylene.
Ethylene sensitive Pssym5 и Pssyml6 mutants have been described in pea (P sativum) [35, 36]. A Pssym5 mutant forms just few root nodules, but their number is significantly increased after treatment with synthetic inhibitors of ethylene effect or synthesis, as well as at culturing of mutant plant root systems
at low temperatures. At this, ethylene production of mutant plants did not differ from wild type plants which indicates the Pssym5 mutants increased sensitivity to ethylene [35]. The Pssym5 E2 mutant demonstrated abortion of infectious threads and premature stopping of cell division in root cortex resulting in a greatly reduced number of nodule primordia and of the very nodules compared with the wild type (37).
In R50 (pea Pssyml6 mutant), the number of nodules is lower than that of wild type, and infectious threads grow not towards the center of the root, but aborize greatly in enlarged cortical cells. However, only a small proportion of these threads are related to cell division and formation of nodule primordia. Moreover, in case of its appearance primordia has abnormal structure, having been formed by the cells that had undergone essentially only anticlinal division, and a flattened shape. Inhibitors of ethylene synthesis and effect restored the R50 mutant ability to nodulation (36). In pea mutant E132 (Pssym21) with a strongly reduced ability to nodulation, treatment with cobalt or silver ions increases the number of root nodules formed, but it was considerably inferior to that in wild type roots (Sparkle variety) [38].
Pea R82 Pssym17 mutant was characterized by reduced and thickened roots as well as with shortened stems and reduced number of nodules (as compared with wild type). In addition, it produced an increased amount of ethylene, however, the inhibitors of ethylene synthesis and effect did not cause the the normal phenotype restoration [39].
A M. truncatula insensitive to ethylene sickle mutant was obtained developing a 10-fold number of nodules than the baseline [31]. This phenotype was the result of the successful completion of numerous infections (nodule formation), while the majority of the wild type infections have been aborted. At the same time, in contrast to the wild-type, the sickle mutant was insensitive to treatment with ethylene and ACC, which suggested that it had a broken ethylene signal transmission. Later, sickle was shown to have a mutation in the Arabidop-sis thaliana ETHYLENE-INSENSITIVE (EIN2) ortholog, the key component in the signal transduction pathway activated by ethylene [40]. The studies of the wild type root proteomes and the sickle mutant subjected to treatment with ACC and rhizobia inoculation revealed the proteins differentially synthesized during nodulation [41]. Thus, ACC treatment induced the synthesis of stress pprg-2 proteins (protein family PR10), ACC oxidase, Kunitz-type proteinase inhibitor, ascorbate, and heat shock proteins in wild type roots. In inoculated mutant roots, the synthesis of pprg-2, Kunitz-type proteinase, and ACC oxidase was reduced which indicates that the stress-activating proteins are regulated by ethylene in the process of nodulation. Probably, the reduced synthesis in mutants as compared to wild type allows the development of a significantly greater number of infections and nodules. Thus, the negative effect of ethylene on nodule formation may be mediated by stress-activated protein synthesis [41].
Transgenic Lotus japonicus (Regel) K. Larsen plants with Cm-ERS1/H70A mutated gene encoding the ethylene receptor of muskmelon (Cucumis melo L.) that demonstrated insensitivity to ethylene were used to study its role in nodule development in Japanese lotus. There was a significant increase in the number of infection threads and nodule primordia, and the number of mature nodules in wild type plants and in the three transgenic lines analyzed did not differ [42]. In transgenic line plant roots, the increased expression of the NIN gene necessary for the formation of infection threads and nodule primordia, has been shown [43]. Obviously, the early stages of symbiotic nodule development in L. japoni-cus including formation of infection threads and nodule primordia induction are negatively regulated by ethylene (probably indirectly through the NIN gene)
[42]. Transgenic plants of L. japonicus with the Arabidopsis thaliana (L.) Heynh. gene with a dominant AtETRl mutation insensitive to ethylene, showed an increase in the number of nodules (at decreasing the number of opposite formed xylem poles) and an increase in the number of bacteroides bounded with a conjoint symbiosome membrane [44].
A recent screening of Japanese lotus (L. japonicus) mutants revealed three allelic enigma mutants insensitive to ethylene, and its increased production (compared to wild-type) [45]. In LjEIN2a mutants, the number of nodules is reduced (unlike M. truncatula sickle with a mutation in the orthologous MtEIN2 gene and with a hyper-nodulation phenotype) [31]. At the same time, the majority of nodules in enigma mutants were formed opposite to protophloem poles thus proving the effect of the modified ethylene status on nodule initiation. This unexpected contradiction can probably be explained by the presence of the second gene copy in the L. japonicus genome, LjEIN2b [45]. In an independent study, two copies of the EIN2—EIN2-1 and EIN2-2 genes have been identified in L. japonicus, and disabling of both genes by RNAi resulted in an increase in the number of nodules formed [46].
Analysis of legume mutants revealed close relationship between signal pathways of ethylene and auxin transduction. Thus, a pea (P sativum) SGEcrt mutant (curly roots) forming a compact root system with crimped roots in high density substrates was characterized by increased auxin synthesis [47] and reduced nodulation [48]. Treatment of plants with AGV restored the nodule number up to the wild type value [49].
In a L. japonicus rel3 mutant with defective ta-siRNAs synthesis (transacting small interfering RNA) regulating ARF3a, ARF3b and ARF4 (Auxin Response Factors) activity, the number of nodules was reduced compared to that of wild type, and adding of AVG restored this value to the level characteristic of the wild type. Probably, changes in the mutant auxin signal transduction pathway results in the increase in ethylene production or in a higher sensitivity to it which, ultimately, results in the reduction of the nodule number [50].
Role of ethylene in nodule formation in soybean and other legumes with determinate type of symbiotic nodules. In soya (G. max), rhizobia inoculation in 4 weeks resulted in the activation of ethylene synthesis and accumulation of ACC ethylene synthesis precursor in plants. The main increase was associated with nodule functioning, and the quantity of excreted ethylene was not dependent on the efficacy of the strain used. Unlike legumes developing indeterminate nodules, physiologically active concentrations of ethephon had no inhibitory effect on nodule formation in soybean [51]. In later studies, induction of ethylene synthesis by soybean roots was observed in 3 days after inoculation with effective Bradyrhizobium japonicum strain, but there was no induction in case of a heterologous R. leguminosarum bv. viciae strain or in case of a mutants with blocked root hair curling (as a result, nodules were not formed) [52]. The AVG ethylene synthesis inhibitor caused a decrease in the amount of ethylene, but had no effect on the number of nodules, which raised a question about the role of ethylene in nodule formation in soybean [52]. In this connection, mutant soybean lines insensitive to ethylene were used, including T119N54 with a mutation in the etr-1 gene which encodes one of ethylene receptors [53]. It has been shown that in the Hobbit 87 wild type and the etrl-1 ethylene insensitive mutant, the number of nodules in plants, both treated and untreated with ethylene action inhibitor (silverthiosulfate), did not differ. Furthermore, ethylene is also not involved in the negative regulation of nodule formation by nitrates. After treatment with ACC, a decrease in the number of nodules was observed in Hobbit 87 wild type plants (unlike the
etr-1 mutant). The authors attribute this to the influence of ethylene on root development in Hobbit 87 wild type plants, resulting in a decrease in the root length. It was concluded that, unlike pea (P sativum) and alfalfa (M trunca-tula), ethylene does not play an important role in nodulation regulation in soybean which is associated with different types of nodules formed—indeterminate in the first case and detrminate in the second case [53]. In other experiments using inhibitors of ethylene biosynthesis (cobalt chloride and AVG), no ethylene effect on the inhibition of nodulation and nitrogen fixation has been shown in soybean as well [54].
At the same time, the above-described studies of transgenic L. japonicus plants that revealed nodulation sensitivity to ethylene in this type of legume with determinate nodules, refuted the hypothesis of the association of soybean insensitivity to ethylene and the nodule type. Also, nodulation sensitivity to ethylene has been shown for another legume with determinate nodules, the beans (P. vulgaris) in which treatment with AVG and cobalt ions increased the number of nodules, and treatment with ethephon decreased it [55].
Effect of rhizobia on the ethylene content in the roots of legumes. Considering the negative role of ethylene in nodulation, it is not surprising that rhizobia use various strategies to reduce the ethylene content [56]. Thus, the Bradyrhizobium elkanii strains produce rhizobitoxin, an ACC synthase inhibitor (one of the key enzymes in ethylene biosynthesis). It is noteworthy that rhizobitoxin has structural similarities to AVG. Rhizobitoxin synthesis by the USDA94 strain reduced the amount of ethylene excreted by inoculated roots and increased the number of root nodules in Macroptilium atropurpureum (DC.) Urb. host plants. At the same time, the mutant with defective rhizobitoxin synthesis formed a reduced (versus the original strain) number of nodules [57]. When inoculated with the rhizobitoxin synthesis mutant B. elkanii strain of elkanii Vigna radiata (L.) R. Wilczek, the number of mature root nodules decreased as well relative to the version with the original USDA61 strain. At the same time, the mutant formed a significant number of immature nodules, indicating the negative impact of ethylene at the later stages nodulation [58].
Another mechanism for reducing the amount of ethylene is the presence of ACC deaminase enzyme decomposing ACC in rhizobia [59]. The presence of ACC deaminase activity may contribute to the development of symbiosis in stressful conditions (for example, soil pollution with heavy metals) [60]. Meanwhile, disabling of ACC deaminase in different rhizobia species leads to different results, and the decrease of nodulation is observed not in all species [61].
So, the active synthesis of ethylene in legume roots is considered to be initiated as a result of the activity of Nod-factors produced by rhizobia. Ethylene negatively regulates nodulation both at the earliest (in calcium oscillations caused by the action of Nod-factor) and at later (growth infectious thread, formation of nodule primordium and maintenance of nodule meristem) stages of nodulation. Soybean plants are an exception, and it should be noted that soybean nodulation insensitivity is probably not related to the type of nodule formed, since nodulation in other legumes is a sensitive to ethylene process. Activation of defense reactions by ethylene in plant roots has been shown, which is probably the mechanism of realization of the negative effect of ethylene on nodulation. Synthesis of ethylene opposite to phloem poles determines the place nodule initiation opposite to xylem poles. Various mechanisms aimed at reducing the ethylene content in the rhizosphere (synthesis of certain rhizobotoxin strains and widespread of ACC deaminase activity among strains of rhizobia) can be regarded as an interesting example of adaptive evolution of rhizobia.
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