systems (type I, type III, type IV, and type VI) which can transport specific proteins
affecting formation of symbiosis [91]. Rhizobia can produce different proteins that
influence host range or suppress plant defense reactions. The first secreted rhizobial
protein for which a role in symbiosis was shown was R. leguminosarum bv. viciae
NodO. NodO is a calcium-binding protein that is released by a type I secretion
system [107]. This protein is encoded by nodO, a flavonoid- and NodD-inducible
gene, and promotes development of infection thread in root hairs [19]. Among other
proteins that are secreted via the type I secretion system, there are several adhesins.
Adhesins seem to play rather a role in attachment and biofilm formation than in
infection process [108]. Rhizobial type III secretion system plays the most important
role in transport of secreted proteins involved in legume-rhizobium symbiosis.
In particular, type III secretion system is responsible for transport of nodulation
outer proteins or Nops. The Nop may be delivered into host-plant cells via pili on the
bacterial surface [19, 109]. Expression of rhizobial genes of type III secretion system
is induced by flavonoids and depends on NodD [109]. Some of secreted proteins
promote symbiosis on certain legumes, whereas other proteins either have no effect
or can significantly reduce symbiotic proficiency in legumes [110]. The role of
secreted proteins is rhizobia symbiosis and nodule formation is not fully clear and
needs to be studied in details.
2.5
Role of Phytohormones in Legume-Rhizobium Symbiosis
The development and functioning of nitrogen-fixing nodules require a complex
regulation of rhizobial infection and root nodule organogenesis. In recent years,
the role of phytohormone signaling pathways has been evidenced in the establishment of legume-rhizobium symbiosis. Plant hormones (phytohormones) are known
to be major regulators of cell proliferation, differentiation, and senescence; thus,
they control plant growth and organogenesis, ripening of fruits and seeds, and plant
death [24, 26, 111]. During legume-rhizobium symbiosis, levels of phytohormones
are significantly changed. Modulation in phytohormone levels may be achieved
in two ways: through direct synthesis of phytohormones by rhizobia and through
indirect effect of bacterial Nod factors on the phytohormone balance in the
plant [24]. The majority of soil microorganisms, including rhizobia, can produce
a number of phytohormones (auxins, gibberellins, cytokinins, ethylene, and abscisic
acid) [24, 112, 113]. Phytohormones synthesized by rhizobia enhance symbiotic
efficacy but do not appear to be necessary for nodule formation [24]. In addition,
many studies suggest that Nod factor-induced changes in the host phytohormone
balance have a crucial role for successful nodule formation [24, 25, 27, 111]. Cytokinin, strigolactones, and local accumulation of auxin can promote nodule
development. However, ethylene, jasmonic acid, abscisic acid, and gibberellic acid
negatively regulate infection thread formation and nodule development [111]. Effects
of some hormones can depend on their concentration, as it was found for indole-3acetic acid (IAA). At low levels, IAA is required for root hair infection in rhizobialegume symbiosis, but IAA at high concentrations inhibits nodule formation, in
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affecting formation of symbiosis [91]. Rhizobia can produce different proteins that
influence host range or suppress plant defense reactions. The first secreted rhizobial
protein for which a role in symbiosis was shown was R. leguminosarum bv. viciae
NodO. NodO is a calcium-binding protein that is released by a type I secretion
system [107]. This protein is encoded by nodO, a flavonoid- and NodD-inducible
gene, and promotes development of infection thread in root hairs [19]. Among other
proteins that are secreted via the type I secretion system, there are several adhesins.
Adhesins seem to play rather a role in attachment and biofilm formation than in
infection process [108]. Rhizobial type III secretion system plays the most important
role in transport of secreted proteins involved in legume-rhizobium symbiosis.
In particular, type III secretion system is responsible for transport of nodulation
outer proteins or Nops. The Nop may be delivered into host-plant cells via pili on the
bacterial surface [19, 109]. Expression of rhizobial genes of type III secretion system
is induced by flavonoids and depends on NodD [109]. Some of secreted proteins
promote symbiosis on certain legumes, whereas other proteins either have no effect
or can significantly reduce symbiotic proficiency in legumes [110]. The role of
secreted proteins is rhizobia symbiosis and nodule formation is not fully clear and
needs to be studied in details.
2.5
Role of Phytohormones in Legume-Rhizobium Symbiosis
The development and functioning of nitrogen-fixing nodules require a complex
regulation of rhizobial infection and root nodule organogenesis. In recent years,
the role of phytohormone signaling pathways has been evidenced in the establishment of legume-rhizobium symbiosis. Plant hormones (phytohormones) are known
to be major regulators of cell proliferation, differentiation, and senescence; thus,
they control plant growth and organogenesis, ripening of fruits and seeds, and plant
death [24, 26, 111]. During legume-rhizobium symbiosis, levels of phytohormones
are significantly changed. Modulation in phytohormone levels may be achieved
in two ways: through direct synthesis of phytohormones by rhizobia and through
indirect effect of bacterial Nod factors on the phytohormone balance in the
plant [24]. The majority of soil microorganisms, including rhizobia, can produce
a number of phytohormones (auxins, gibberellins, cytokinins, ethylene, and abscisic
acid) [24, 112, 113]. Phytohormones synthesized by rhizobia enhance symbiotic
efficacy but do not appear to be necessary for nodule formation [24]. In addition,
many studies suggest that Nod factor-induced changes in the host phytohormone
balance have a crucial role for successful nodule formation [24, 25, 27, 111]. Cytokinin, strigolactones, and local accumulation of auxin can promote nodule
development. However, ethylene, jasmonic acid, abscisic acid, and gibberellic acid
negatively regulate infection thread formation and nodule development [111]. Effects
of some hormones can depend on their concentration, as it was found for indole-3acetic acid (IAA). At low levels, IAA is required for root hair infection in rhizobialegume symbiosis, but IAA at high concentrations inhibits nodule formation, in
302
U. Y. Stambulska and M. M. Bayliak