Endophytic Colonization of Rice (Oryza sativa L.) by the Symbiotic Strain Nostoc punctiforme PCC 73102

Abstract

Cyanobacteria are phototrophic microorganisms able to establish nitrogen-fixing symbiotic associations with representatives of all four of the major phylogenetic divisions of terrestrial plants. Despite increasing knowledge on the beneficial effects of cyanobacteria in rice fields, the information about the interaction between these microorganisms and rice at the molecular and structural levels is still limited. We have used the model nitrogen-fixing cyanobacterium Nostoc punctiforme to promote a long-term stable endophytic association with rice. Inoculation with this strain of hydroponic cultures of rice produces a fast adherence of the cyanobacterium to rice roots. At longer times, cyanobacterial growth in the proximity of the roots increased until reaching a plateau. This latter phase coincides with the intracellular colonization of the root epidermis and exodermis. Structural analysis of the roots revealed that the cyanobacterium use an apoplastic route to colonize the plant cells. Moreover, plant roots inoculated with N. punctiforme show both the presence of heterocysts and nitrogenase activity, resulting in the promotion of plant growth under nitrogen deficiency, thus providing benefits for the plant.

Early events of the endophytic symbiotic between Oryza sativa and Nostoc punctiforme involve the SYM pathway

“…Previous studies of colonization of Oryza with Nostoc strains showed an early phase of contact that started a few hours of co-culture followed by a second phase of colonization that lasted 20 days (Nilsson et al, 2002; Álvarez et al 2020). This first phase of contact at early stages is critical for the success of the symbiotic process, since is the period when both organisms exchange signals and react to the presence of the partner.…”

“…However, this might not be the mode of entry of Nostoc into the plant roots. We have observed that the infection started in the plant body and then extended through the root hairs, being root tips unaffected (Álvarez et al, 2020). In legume-rhizobia symbiosis NFs induce at the cellular level depolarization of the cytoplasmic membrane and calcium spiking response, activating genes of the SYM pathway (Kosuta et al, 2008).…”

“…It grows epiphytically in specialized compartments of liverworts, hornworts and Azolla , meanwhile colonizes endophytically stem glands of Gunnera sp. Oryza sativa (hereafter Oryza ) and Triticum vulgare , providing fixed nitrogen to the plant (Gantar et al, 1991; Santi et al 2013; Álvarez et al, 2020). Symbiotic nitrogen fixation with cereals is central for exploring new sustainable agricultural practices that may reduce the usage of synthetic fertilizers, whose application results in adverse environmental consequences (diCenzo et al, 2020).…”

Sustaining Rice Production through Biofertilization with N2-Fixing Cyanobacteria

“…Nostoc punctiforme is a terrestrial cyanobacterium with a broad symbiotic competence with fungi and terrestrial plants, including bryophytes, gymnosperms, and angiosperms, providing fixed nitrogen to the plant partner [27]. It has been shown that Nostoc punctiforme PCC 73102 enhances rice growth [12]. Strain G10 formed brown colonies on a solid medium and growth forming rough mats in liquid BG11 0 .…”

“…The paddy field ecosystem represents a unique aquatic-terrestrial habitat, which provides a favorable environment for the growth of cyanobacteria. From the different groups of cyanobacteria, the N 2 -fixing Nostoc genera are naturally found in floating assemblages, attached to the root surface, and can colonize the roots of rice [11,12]. These cyanobacteria, which are of great relevance in the global carbon and nitrogen cycles, are the main contributors to the natural deposition of nitrogen in paddy fields [13,14].…”