Legume crops such as soybean obtain a large portion of their nitrogen nutrition through symbiotic nitrogen fixation by diazotrophic rhizobia bacteria in root nodules. However, nodule occupancy by low‐capacity nitrogen‐fixing rhizobia can lead to lower‐than‐optimal levels of nitrogen fixation. Seed/root coating with engineered materials such as graphene‐carrying biomolecules that may promote specific attraction/attachment of desirable bacterial strains is a potential strategy that can help overcome this rhizobia competition problem. As a first step towards this goal, we assessed the impact of graphene on soybean and
Glycerol-3-phosphate (G3P) is a well-known mobile regulator of systemic acquired resistance (SAR), which provides broad spectrum systemic immunity in response to localized foliar pathogenic infections. We show that G3P-derived foliar immunity is also activated in response to genetically-regulated incompatible interactions with nitrogen-fixing bacteria. Using gene knock-down we show that G3P is essential for strain-specific exclusion of non-desirable root-nodulating bacteria and the associated foliar pathogen immunity in soybean. Grafting studies show that while recognition of rhizobium incompatibility is root driven, bacterial exclusion requires G3P biosynthesis in the shoot. Biochemical analyses support shoot-to-root transport of G3P during incompatible rhizobia interaction. We describe a root-shoot-root signaling mechanism which simultaneously enables the plant to exclude non-desirable nitrogen-fixing rhizobia in the root and pathogenic microbes in the shoot.
more » « less- NSF-PAR ID:
- 10153784
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 10
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract Bradyrhizobium using a set of growth, biochemical, and physiological assays. Three different concentrations of graphene were tested for toxicity in soybean (50, 250, and 1,000 mg/l) andBradyrhizobia (25, 50, and 100 mg/l). Higher graphene concentrations (250 mg/l and 1,000 mg/l) promoted seed germination but slightly delayed plant development. Spectrometric and microscopy assays for hydrogen peroxide and superoxide anion suggested that specific concentrations of graphene led to higher levels of reactive oxygen species in the roots. In agreement, these roots also showed higher activities of antioxidant enzymes, catalase, and ascorbate peroxidase. Conversely, no toxic effects were detected onBradyrhizobia treated with graphene, and neither did they have higher levels of reactive oxygen species. Graphene treatments at 250 mg/l and 1,000 mg/l significantly reduced the number of nodules, but rhizobia infection and the overall nitrogenase activity were not affected. Our results show that graphene can be used as a potential vehicle for seed/root treatment. -
Cooper, Vaughn S. (Ed.)ABSTRACT Root nodulating rhizobia are nearly ubiquitous in soils and provide the critical service of nitrogen fixation to thousands of legume species, including staple crops. However, the magnitude of fixed nitrogen provided to hosts varies markedly among rhizobia strains, despite host legumes having mechanisms to selectively reward beneficial strains and to punish ones that do not fix sufficient nitrogen. Variation in the services of microbial mutualists is considered paradoxical given host mechanisms to select beneficial genotypes. Moreover, the recurrent evolution of non-fixing symbiont genotypes is predicted to destabilize symbiosis, but breakdown has rarely been observed. Here, we deconstructed hundreds of genome sequences from genotypically and phenotypically diverse Bradyrhizobium strains and revealed mechanisms that generate variation in symbiotic nitrogen fixation. We show that this trait is conferred by a modular system consisting of many extremely large integrative conjugative elements and few conjugative plasmids. Their transmissibility and propensity to reshuffle genes generate new combinations that lead to uncooperative genotypes and make individual partnerships unstable. We also demonstrate that these same properties extend beneficial associations to diverse host species and transfer symbiotic capacity among diverse strains. Hence, symbiotic nitrogen fixation is underpinned by modularity, which engenders flexibility, a feature that reconciles evolutionary robustness and instability. These results provide new insights into mechanisms driving the evolution of mobile genetic elements. Moreover, they yield a new predictive model on the evolution of rhizobial symbioses, one that informs on the health of organisms and ecosystems that are hosts to symbionts and that helps resolve the long-standing paradox. IMPORTANCE Genetic variation is fundamental to evolution yet is paradoxical in symbiosis. Symbionts exhibit extensive variation in the magnitude of services they provide despite hosts having mechanisms to select and increase the abundance of beneficial genotypes. Additionally, evolution of uncooperative symbiont genotypes is predicted to destabilize symbiosis, but breakdown has rarely been observed. We analyzed genome sequences of Bradyrhizobium, bacteria that in symbioses with legume hosts, fix nitrogen, a nutrient essential for ecosystems. We show that genes for symbiotic nitrogen fixation are within elements that can move between bacteria and reshuffle gene combinations that change host range and quality of symbiosis services. Consequently, nitrogen fixation is evolutionarily unstable for individual partnerships, but is evolutionarily stable for legume- Bradyrhizobium symbioses in general. We developed a holistic model of symbiosis evolution that reconciles robustness and instability of symbiosis and informs on applications of rhizobia in agricultural settings.more » « less
-
more » « less
Abstract Medicago (Medicago truncatula) establishes a symbiosis with the rhizobia Sinorhizobium sp, resulting in the formation of nodules where the bacteria fix atmospheric nitrogen. The loss of immunity repression or early senescence activation compromises symbiont survival and leads to the formation of nonfunctional nodules (fix−). Despite many studies exploring an overlap between immunity and senescence responses outside the nodule context, the relationship between these processes in the nodule remains poorly understood. To investigate this phenomenon, we selected and characterized three Medicago mutants developing fix− nodules and showing senescence responses. Analysis of specific defense (PATHOGENESIS-RELATED PROTEIN) or senescence (CYSTEINE PROTEASE) marker expression demonstrated that senescence and immunity seem to be antagonistic in fix− nodules. The growth of senescence mutants on non-sterile (sand/perlite) substrate instead of sterile in vitro conditions decreased nodule senescence and enhanced defense, indicating that environment can affect the immunity/senescence balance. The application of wounding stress on wild-type (WT) fix+ nodules led to the death of intracellular rhizobia and associated with co-stimulation of defense and senescence markers, indicating that in fix+ nodules the relationship between the two processes switches from opposite to synergistic to control symbiont survival during response to the stress. Our data show that the immune response in stressed WT nodules is linked to the repression of DEFECTIVE IN NITROGEN FIXATION 2 (DNF2), Symbiotic CYSTEINE-RICH RECEPTOR-LIKE KINASE (SymCRK), and REGULATOR OF SYMBIOSOME DIFFERENTIATION (RSD), key genes involved in symbiotic immunity suppression. This study provides insight to understand the links between senescence and immunity in Medicago nodules.
-
more » « less
Summary Bacteria are a globally sustainable source of fixed nitrogen, which is essential for life and crucial for modern agriculture. Many nitrogen‐fixing bacteria are agriculturally important, including bacteria known as rhizobia that participate in growth‐promoting symbioses with legume plants throughout the world. To be effective symbionts, rhizobia must overcome multiple environmental challenges: from surviving in the soil, to transitioning to the plant environment, to maintaining high metabolic activity within root nodules. Climate change threatens to exacerbate these challenges, especially through fluctuations in soil water potential. Understanding how rhizobia cope with environmental stress is crucial for maintaining agricultural yields in the coming century. The bacterial outer membrane is the first line of defence against physical and chemical environmental stresses, and lipids play a crucial role in determining the robustness of the outer membrane. In particular, structural remodelling of lipid A and sterol‐analogues known as hopanoids are instrumental in stress acclimation. Here, we discuss how the unique outer membrane lipid composition of rhizobia may underpin their resilience in the face of increasing osmotic stress expected due to climate change, illustrating the importance of studying microbial membranes and highlighting potential avenues towards more sustainable soil additives.
-
more » « less
Abstract Immune perception in flowering plants is mediated by a repertoire of cytoplasmic and cell‐surface receptors that detect invading microbes and their effects on cells. Here, we show that several large families of immune receptors exhibit size variations related to a plant's competence to host symbiotic root fungi (mycorrhiza). Plants that do not participate in mycorrhizal associations have significantly smaller immune repertoires, while the most promiscuous symbiotic hosts (ectomycorrhizal plant species) have significantly larger immune repertoires. By contrast, we find no significant increase in immune repertoire size among legumes competent to form a symbiosis with nitrogen‐fixing bacteria (rhizobia). To explain these observations, we hypothesize that plant immune repertoire size expands with symbiote species diversity.
