Symbiosis between cyanobacteria and plants: from molecular studies to agronomic applications

Abstract

Nitrogen-fixing cyanobacteria from the order Nostocales are able to establish symbiotic relationships with diverse plant species. They are promiscuous symbionts, as the same strain of cyanobacterium is able to form symbiotic biological nitrogen-fixing relationships with different plants species. This review will focus on the different types of cyanobacterial-plant associations, both endophytic and epiphytic, and provide insights from a structural viewpoint, as well as our current understanding of the mechanisms involved in the symbiotic crosstalk. In all these symbioses, the benefit for the plant is clear; it obtains from the cyanobacterium fixed nitrogen and other bioactive compounds, such as phytohormones, polysaccharides, siderophores, or vitamins, leading to enhanced plant growth and productivity. Additionally, there is increasing use of different cyanobacterial species as bio-inoculants for biological nitrogen fixation to improve soil fertility and crop production, thus providing an eco-friendly, alternative, and sustainable approach to reduce the over-reliance on synthetic chemical fertilizers.

Keywords: Nostoc; Biofertilizer; PGPR; cyanobacteria; heterocyst; symbiosis.

Fig. 1.

Schematic illustration of the Nostocales life cycle. The vegetative trichome is composed of vegetative cells performing oxygenic photosynthesis. Heterocysts develop from vegetative cells in response to nitrogen deprivation, and they are arranged in the trichome in a semi-regular pattern. The vegetative cells develop into motile hormogonia (plant infection units) in response to changes in external conditions or in response to plant factors; their ability to move facilitates colonization of new habitats. Akinetes are produced to endure harsh conditions for long periods of time.

Fig. 2.

Symbiotic interactions between Nostocales cyanobacteria and plants. Simplified green plant phylogeny inferred by Davis et al. (2014). The most representative genera in each plant division with which the symbiosis is established is indicated in parentheses. The line in orange denotes epiphytic associations, which is established with mosses. The green line denotes endophytic, extracellular associations, which is extended into non-vascular plants (hornworts and liverworts) and vascular plants (pteridophytes and gymnosperms). The blue lines denote endophytic, intracellular associations, restricted to angiosperms. Created with Biorender.com.

Fig. 3.

Multihost symbiotic competence of Nostoc punctiforme with plants. (A, D) Epiphytic association of N. punctiforme (red/yellow) with Sphagnum palustre. Hy, hyalocysts; Chl, chlorocysts. The cyanobacterium is allocated within hyalocysts, which are empty structures connected with the environment. (B, E) Endophytic, extracellular association of N. punctiforme with Anthoceros agrestis. Cyanobacterial trichomes (in red) are found in the slime cavities (SC), which provide a protective environment for the cyanobacteria to reside. (C, F) Endophytic, intracellular symbiosis between N. punctiforme and O. sativa; cyanobacterial filaments (in red) are enclosed inside the root epidermal cells (in green).

Fig. 4.

Schematic illustration of the cyanobacterial symbiosis signalling pathway in the context of the common symbiosis signalling pathway (CSSP) in rhizobial, actinorhizal, and mycorrhizal symbiosis. Symbiosis is activated following the perception of secreted lipochitooligosaccharide (LCO) Nod factors (Nod Fs) from legumes and LCOs from Alnus spp., and LCOs and chitin oligomers (COs; Myc Fs) from plants by plasma membrane-localized heterodimeric LysM-RLKs. These LysM-RLKs interact with the leucine-rich repeat-type SYMBIOSIS RECEPTOR KINASE (SYMRK) to activate the CSSP core module. While the LysM-RLKs for rhizobial and mycorrhizal symbioses have been characterized, the identity of the LysM-RLK for actinorhizal symbiosis remains elusive. Calcium signalling is a hallmark of the CSSP, and nuclear Ca²⁺ oscillations (Ca²⁺ spiking) have been observed in rhizobial, actinorhizal, and mycorrhizal symbioses. SYMRK and CASTOR/POLLUX are responsible for encoding Ca²⁺ signals (Ca²⁺ spiking), while CCamK/DMI3 and CYCLOPS/IPD3 are responsible for decoding the calcium signals, followed by downstream transcriptional reprogramming, ultimately resulting in rhizobia and actinobacteria infection, colonization and nodulation in rhizobial and actinorhizal symbiosis, and arbuscular mycorrhizal fungal (AMF) infection and colonization in mycorrhizal symbiosis. In cyanobacterial symbiosis, only some components of the CSSP core module, POLLUX, CcaMK, and CYCLOPS, have been identified. Created with Biorender.com.