1. Introduction
Leguminous plants form root nodules, in which symbiotic rhizobia fix atmospheric nitrogen. The nodulation process in the legume-rhizobium symbiosis consists of a series of events initiated by an exchange of specific signaling compounds between the two partners. The roots of leguminous plants secrete flavonoids, which trigger the synthesis of lipochitin-oligosaccharide signaling molecules, Nod factors (NFs), by rhizobia. NFs activate nodule organogenesis in the roots by stimulating the division of cortical cells. Many nodule development stages resemble other plant organ development such as cell divisions and differentiations. Because phytohormones are signal molecules involved in most plant physiological activities, they are likely to positively or negatively regulate nodulation and nitrogen fixation in the legume-rhizobium symbiosis.
In this chapter, we review the roles of several key phytohormones, namely auxins, cytokinins, gibberellins, ethylene, brassinosteroids, abscisic acid, salicylic acid, jasmonic acid and strigolactones in nodulation and nitrogen fixation in leguminous plants.
2. Auxins
Auxins were the first class of plant hormones discovered, and play a central role on the regulation of germination, plant growth, flower bud formation and flowering, and other developmental processes. In addition, auxins are involved in responses to environmental stimuli such as temperature, light and gravity. The most important member of the auxin family is indole-3-acetic acid (IAA), a native auxin in plants. The highest auxin levels are found in the cells undergoing cell division, elongation, differentiation and vascular bundle formation. Therefore, auxin may play a significant role in nodulation. The possible involvement of auxins in nodule formation was first reported by Thimann in 1936. Thimann reported that the nodules of
These reports also suggest that the auxin transport system is an important control on the number of indeterminate-type nodules. The effects of treatment with auxin transport inhibitors (NPA and TIBA) and with an auxin antagonist, α-(phenylethyl-2-one)-indole-3-acetic acid (PEO-IAA), on determinate-type nodulation were investigated by using
The role of auxins in nodulation is linked to the development of other root structures, such as lateral roots. Both lateral roots and root nodules development are known to be regulated by the auxin-to-cytokinin ratio. An increase in the auxin concentration stimulated lateral root formation, whereas an increase of in the cytokinin concentration or an inhibition of auxin transport induced the development of pseudo-nodules. Previously, it has been assumed that nodule initiation in plants that form indeterminate-type nodules is stimulated by a low auxin-to-cytokinin ratio [2]. Recently, Suzaki et al. (2012) investigated auxin distribution during root nodule development by using a DR5::GFP transformant of
3. Cytokinins
Cytokinins have been found in all living cells of intact higher plants. Cytokinins play roles ranging from minor to major throughout development, from germination to leaf and plant senescence and modulate physiological processes important throughout the life of the plant, including photosynthesis and respiration [14, 15]. Cytokinins are also involved in as the control of root architecture development, including root nodulation.
In
Recent research has confirmed that cytokinin receptors also play a significant role in nodule organogenesis [22-24]. The gain-of-function
Exogenous application of cytokinins enhanced nitrogenase activity in nodules at all stages [25]. Rao et al. (1984) reported that the stimulatory effect of cytokinins increased the efficiency of nitrogen fixation. The application of cytokinins stimulated nitrate-induced nitrate reductase activity in the dark. Stimulation of nitrate reductase by cytokinins was inhibited significantly 6-methylpurine and cycloheximide, suggesting a requirement of RNA and protein synthesis [26].
4. Gibberellins
Gibberellins (GAs) are another important family of growth regulators in higher plants. GAs are also involved in root nodule symbiosis. Mutants deficient in GA biosynthesis or signaling develop dwarf phenotypes [27]. The GA-deficient mutants
The F-box containing protein, SLEEPY 1 (SLY1), functions as a positive regulator in GA signaling. In the presence of GAs, SLY1 interacts with negative regulators of GA signaling, leading to the degradation of these negative regulators [32, 33]. The over-expression of
The application of a GA decreased nodulation and nitrogen fixation under optimal growth conditions [35]. However, in
5. Ethylene
Ethylene is a gaseous phytohormone involved in fruit ripening, leaf and fruit abscission, germination, seedling morphogenesis, root emergence, root hair elongation, promotion of flowering, senescence and stress response. Several studies have shown that ethylene production can have a negative effect on nodule formation. For example, ethylene production significantly increased in roots infected by rhizobia, and added exogenous ethylene can decrease the number of nodules [37, 38]. In
ACC deaminase catalyzes the degradation of ACC into ammonium and α-ketobutyrate. The ACC deaminase gene (
6. Brassinosteroids
Brassinosteroids (BRs) are a group of plant steroid hormones that regulate a wide range of physiological responses, including cell elongation, photomorphogenesis, xylem differentiation, and seed germination. BRs are present in the plants in extremely low concentrations, but they are highly mobile within the plant. BRs supplied via the root system remarkably promoted the elongation of cotyledon petioles and the hypocotyls of young radish and tomato plants [56]. This study clearly demonstrated the mobility of BRs in the plant system.
In addition, application of BRs affected nodulation and nitrogen fixation in groundnut (
7. Abcisic acid
Abcisic acid (ABA) plays crucial roles in plant growth, development and responses to environment stresses such as cold, drought and high salinity. ABA has been reported to play negative roles at different stages of nodule development. The application of ABA inhibited nodulation in
The nitrogenase activity of nodules treated with ABA was lower than in untreated wild-type in
The role of ABA in autoregulation of nodulation was investigated in the
8. Salicylic acid
Salicylic acid (SA) is involved in plant responses to pathogen, and its mode of action has been well characterized. SA is an inducer of systemic acquired resistance in the defense responses to pathogen attacks. In terms of the interaction between plants and rhizobia, several reports have shown that SA strongly inhibits nodulation and nodule development, leading to decreased nitrogen fixation activity. When
9. Jasmonic acid
Jasmonic acid (JA) is also involved in plant defenses against pathogens and in wound responses. JA has been reported to be a negative regulator of nodulation. In
10. Strigolactones
Strigolactones (SLs) have been identified as phytohormones that are involved in the regulation of shoot branching in plants and thus have been suggested to be ubiquitous in the plant kingdom [88]. SLs are released by roots into the rhizosphere, and appear to stimulate germination of the seeds of parasitic plants such as
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