Nonlegume Parasponia andersonii Deploys a Broad Rhizobium Host Range Strategy Resulting in Largely Variable Symbiotic Effectiveness

Abstract

The non-legume genus Parasponia has evolved the rhizobium symbiosis independent from legumes and has done so only recently. We aim to study the promiscuity of such newly evolved symbiotic engagement and determine the symbiotic effectiveness of infecting rhizobium species. It was found that Parasponia andersonii can be nodulated by a broad range of rhizobia belonging to four different genera, and therefore, we conclude that this non-legume is highly promiscuous for rhizobial engagement. A possible drawback of this high promiscuity is that low-efficient strains can infect nodules as well. The strains identified displayed a range in nitrogen-fixation effectiveness, including a very inefficient rhizobium species, Rhizobium tropici WUR1. Because this species is able to make effective nodules on two different legume species, it suggests that the ineffectiveness of P. andersonii nodules is the result of the incompatibility between both partners. In P. andersonii nodules, rhizobia of this strain become embedded in a dense matrix but remain vital. This suggests that sanctions or genetic control against underperforming microsymbionts may not be effective in Parasponia spp. Therefore, we argue that the Parasponia-rhizobium symbiosis is a delicate balance between mutual benefits and parasitic colonization.

Parasponia: a novel system for studying mutualism stability

“…Tests where legumes and Parasponia were grown using native Parasponia strains suggest that legumes have around three times higher nitrogenase activity than Parasponia (Table 2), but more work is needed to explore the extent of this pattern. Finally, Parasponia exhibit high levels of partner promiscuity and are nodulated by many rhizobial species [42]. In legumes, various degrees of promiscuity are found, ranging from very strict (e.g., the tribes Cicereae, Trifolieae, and Viceae) to highly promiscuous (comparable with Parasponia) as in many tropical legumes [13].…”

“…However, experimental work later demonstrated that, in the laboratory, Parasponia andersonii was successfully nodulated by rhizobia from European soil containing three additional genera (Rhizobium, Mesorhizobium, and Sinorhizobium [42]), indicating high promiscuity. How to reconcile these seemingly divergent patterns?…”

“…A second possibility is that Parasponia cannot discriminate against European strains due to a lack of evolutionary history and/or shows abnormal symbiotic association patterns under laboratory conditions. Regardless, the experiments discussed in [42] demonstrate the potential for extraordinary breadth in symbiotic partnerships in Parasponia compared with most legumes and lay the foundation for more ecologically relevant host-microbe research focused on strains collected from Parasponia's native habitat.…”

“…Although such post-infection mechanisms can theoretically keep exploitation levels low, physiological evidence suggests that Parasponia is unable to terminate symbiotic engagement via 'premature' nodule senescence [39,42]. For example, when P. andersonii was nodulated by European strains varying in effectiveness, one rhizobial species -Rhizobium tropici WUR1 -was so exploitative that it induced localized host cell death in young nodules [42].…”

RAPD-inferred genetic variability of some indigenousRhizobium leguminosarumisolates from red clover (Trifolium pratenseL.) nodules

“…Some free-living proteobacteria can form symbioses with legumes and the non-legume Parasponia [13]. In this symbiotic relationship they are able of fixing atmospheric nitrogen and are collectively known as rhizobia.…”