A legume genetic framework controls infection of nodules by symbiotic and endophytic bacteria.

Rafal Zgadzaj,Nadieh De Jonge,Dorthe B Jensen,Simona Radutoiu,Lene H Madsen,Simon Kelly,Euan K James,Yasuyuki Kawaharada,John M Mcdowell

doi:10.1371/journal.pgen.1005280

Rafal Zgadzaj, Nadieh De Jonge + Show 7 more

Open Access

https://doi.org/10.1371/journal.pgen.1005280

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Journal: PLoS genetics	Publication Date: Jun 4, 2015
Citations: 94	License type: CC BY 4.0

Affiliation: Aarhus University, James Hutton Institute

Abstract

Legumes have an intrinsic capacity to accommodate both symbiotic and endophytic bacteria within root nodules. For the symbionts, a complex genetic mechanism that allows mutual recognition and plant infection has emerged from genetic studies under axenic conditions. In contrast, little is known about the mechanisms controlling the endophytic infection. Here we investigate the contribution of both the host and the symbiotic microbe to endophyte infection and development of mixed colonised nodules in Lotus japonicus. We found that infection threads initiated by Mesorhizobium loti, the natural symbiont of Lotus, can selectively guide endophytic bacteria towards nodule primordia, where competent strains multiply and colonise the nodule together with the nitrogen-fixing symbiotic partner. Further co-inoculation studies with the competent coloniser, Rhizobium mesosinicum strain KAW12, show that endophytic nodule infection depends on functional and efficient M. loti-driven Nod factor signalling. KAW12 exopolysaccharide (EPS) enabled endophyte nodule infection whilst compatible M. loti EPS restricted it. Analysis of plant mutants that control different stages of the symbiotic infection showed that both symbiont and endophyte accommodation within nodules is under host genetic control. This demonstrates that when legume plants are exposed to complex communities they selectively regulate access and accommodation of bacteria occupying this specialized environmental niche, the root nodule.

Highlights

Plants are the major manufacturers of carbohydrates in ecosystems, and their roots develop in soil environments rich in heterotrophic microorganisms that require carbon for their growth
In order to test the ability of endophytic bacteria to colonise and multiply inside Lotus nodules we chose to: i) investigate endophytic bacteria that were previously found inside plant roots, as endophytes or presumptive endophytes, and ii) monitor their ability to colonise nodules by visualising their presence inside primordia induced by the M. loti symbiont
With the exception of H. frisingense, the other four strains were present inside the nodules or the cortical infection threads (ITs) induced by M. loti (Figs 1A and S1), but endophyte amplification and effective colonisation of the nodule interior was observed only for Burkholderia KAW25 and Rhizobium KAW12 (Figs 1B and S1C)

Summary

Introduction

Plants are the major manufacturers of carbohydrates in ecosystems, and their roots develop in soil environments rich in heterotrophic microorganisms that require carbon for their growth. In most legumes the infection starts at the stage of bacterial entrapment within curled root hairs This is followed by initiation and elongation of infection threads (ITs), which are plant-derived tubular structures that guide the microbe through the plant’s epidermal and cortical cell layers towards the nodule primordia, in which the bacteria are endocytosed in organelle-like symbiosomes where they develop into bacteroids and fix nitrogen. Later in the developmental process several genes, for example Sst, encoding a sulphate transporter, are required for bacterial persistence inside the plant cell [28], and Medicago truncatula, which develops indeterminate nodules with a persistent meristem, produces nodule-specific cysteine-rich (NCR) peptides to control the irreversible terminal differentiation of bacteria [29]

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Conclusion