Diversity and regulation of symbiotic nitrogen fixation in plants

Xu, Peng; Wang, Ertao

doi:10.1016/j.cub.2023.04.053

Cited by 25 publications

(4 citation statements)

References 203 publications

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“…While microbes fix large quantities of atmospheric dinitrogen to make biologically usable ammonia, it is only directly coupled to plant growth in a limited number of crops used for human consumption, such as soybean (Xu & Wang, 2023 ). The major crop staples of corn, wheat and potatoes require vast inputs of nitrogen derived from the industrial Haber‐Bosch process.…”

Section: Water Sanitationmentioning

confidence: 99%

A microbial evolutionary approach for a sustainable future

Wackett

2023

Microbial Biotechnology

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With the continued population increase, more sustainable use of water, land, air and chemicals is imperative. Microorganisms will need to be called upon to aid in many sustainability efforts. Prokaryotes are the fastest‐evolving cellular life, and most manipulatable via synthetic biology. Moreover, their natural diversity in processing organic and inorganic chemicals, and their survivability in extreme niches, make them prime agents to enlist for solving many of society's pressing problems.

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Section: Water Sanitationmentioning

confidence: 99%

A microbial evolutionary approach for a sustainable future

Wackett

2023

Microbial Biotechnology

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“…Plant-associated microbiota directly affect the fitness of their hosts through a variety of mechanisms. These mechanisms include interactions with plant immunity (Pieterse et al 2014; Durrant and Dong 2004; Schlatter et al 2017), secretion and metabolism of phytohormones and other signaling molecules (Orozco-Mosqueda, Santoyo, and Glick 2023; Spaepen 2015; Spaepen and Vanderleyden 2011; Glick 2005), mediating nutrient bioavailability (P. Xu and Wang 2023; Richardson and Simpson 2011; Kramer, Özkaya, and Kümmerli 2020), and otherwise altering the physico-chemical environment experienced by plants (Liu et al 2020; Kumar et al 2020). Intentional manipulation of plant microbiomes to enhance fitness—through growth promotion, disease suppression, and alleviation of abiotic stress—therefore represents an alternative or supplement to plant breeding to improve agricultural productivity (Friesen et al 2011; Finkel et al 2017; Shayanthan, Ordoñez, and Oresnik 2022; Vorholt et al 2017).…”

Section: Introductionmentioning

confidence: 99%

Improving rice drought tolerance through host-mediated microbiome selection

Styer,

Pettinga,

Caddell

et al. 2024

Preprint

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Plant microbiome engineering remains a significant challenge due to challenges associated with accurately predicting microbiome assembly and function in complex, heterogeneous soil environments. However, host-mediated selection can simplify the process by using plant host phenotype as a reporter of microbiome function; by iteratively selecting microbiomes from hosts with desired phenotypes and using them to inoculate subsequent cohorts of hosts, artificial selection can steer the microbiome towards a composition producing optimized plant phenotypes. In this study, we inoculated rice with wild microbial communities from fallow rice field, desert, and serpentine seep field soils. By challenging these plants with drought and iteratively selecting microbiomes from the least drought stressed plants across multiple generations, we derived simplified microbiomes that enhanced both the growth and drought tolerance of rice. Across selection cycles, microbiomes within and between soil treatments became increasingly similar, implicating both dispersal and selection as drivers of community composition. With amplicon sequencing data we identified specific bacterial taxa associated with improved rice drought phenotypes; while many of these taxa have been previously described as plant growth promoters, we also identified novel taxa exhibiting strong positive correlation with improved drought performance. Lastly, we resolved 272 metagenome-assembled genomes (MAGs) and used these MAGs to identify functions enriched in bacteria driving enhanced drought tolerance. The most significantly enriched functions--particularly glycerol-3-phosphate and iron transport--have been previously implicated as potential mediators of plant-microbe interactions during drought. Altogether, these data demonstrate that host-mediated selection provides an efficient framework for microbiome engineering through the identification of both individual taxa and simplified communities associated with enhanced plant phenotypes.

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“…While the molecular link between nutrient status of the host plant and establishment, as well as maintenance of the symbiotic interaction is well known in the plant-AMF and nodule forming bacteria symbioses, it is poorly understood in other plant-microbe symbiotic interactions. Some plants form endophytic, extracellular symbioses with cyanobacteria which are also under the control of the nutrient status of the host plant (Meeks, 1998; Xu and Wang, 2023; Álvarez et al, 2023b). On one hand, endophytic plant-cyanobacteria symbioses are similar to the plant-AMF and nodule forming bacteria symbioses because nitrogen starvation is necessary for the reconstitution of the symbiotic interaction in vitro as well as to maintain cyanobacteria nitrogen fixation (Enderlin and Meeks, 1983; Kimura and Nakano, 1990; CAMPBELL and MEEKS, 1992).…”

Section: Introductionmentioning

confidence: 99%

“…On the other hand, plant-endophytic cyanobacteria and the well-investigated plant-microbe symbioses (plant AMF/ nodule forming bacteria) differ in two important aspects. While most plant-endophytic cyanobacteria symbioses are extracellular and the cavities of the host plant containing the cyanobiont are present even in the absence of the cyanobiont (Meeks, 2003; Gorelova and Baulina, 2009; Xu and Wang, 2023), the well-investigated plant-microbe symbioses (plant AMF/ nodule forming bacteria) are all intracellular and cellular structures of the host plant essential for the colonization of the microbial partner must be induced by nutrient starvation and by contact with the microbial partner (Oldroyd, 2013; Ma and Chen, 2021). Therefore, nutrient starvation may induce a less complex genetic network in plant-cyanobacteria systems mainly related to the production of the HIF and immune system adjustment in contrast to intracellular symbioses (plant-AMF/nodule-forming bacteria).…”

Section: Introductionmentioning

confidence: 99%

Nitrogen starvation response in hornworts and liverworts provides little evidence for complex priming to the cyanobiont

Yue,

Sablok,

Neubauer

et al. 2024

Preprint

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Mutualistic plant-microbe symbiotic interactions are thought to have evolved from a loose association often observed between host plants and microbes when nutrients are limited and caused by chemical attractants released by the host plant. Therefore, the molecular network enabling intimate mutualistic plant-microbe symbioses may have evolved from a general nutrient starvation response shared by all land plants (embryophytes). Nevertheless, this hypothesis remains to be tested because information on the consequences of nutrient starvation is mainly available for vascular plants but missing for most non-vascular plant lineages. While well-studied in vascular plants, particularly in arbuscular mycorrhizal fungi- and nodule-forming bacteria-plant symbioses, the molecular link between nutrient status and symbiotic interaction remains poorly understood in other systems. This is especially true to the symbiotic associations between plants and cyanobacteria, in which host plants release so-called hormogonia inducing factors (HIF) only under nutrient limited conditions to mobilize the cyanobiont and initiate the interaction. Nevertheless, in contrast to the well-investigated mycorrhiza- and nodule-forming bacteria-plant associations, plant-cyanobacteria interactions are extracellular and morphological structures hosting the cyanobionts are formed even in the absence of the microbial partner. Therefore, nutrient starvation may induce a less complex genetic network in plant-cyanobacteria systems in contrast to intracellular symbioses (plant-AMF/nodule-forming bacteria). To test the hypothesis of a conserved starvation network across land plants and to investigate the link between nutrient starvation and symbiosis initiation in the plant-cyanobacteria symbiosis, we explore the transcriptional responses to nutrient starvation in two non-vascular plant species, a hornwort Anthoceros agrestis and a liverwort Blasia pusilla, serving as ideal model systems for plant-cyanobacteria endophytic symbioses. By analyzing time-series RNA-seq data, we investigate gene expression changes associated with nutrient starvation in these bryophyte species and compare them with data available for vascular plants. Our study aims to identify convergent and divergent transcriptomic responses and to uncover transcriptomic signatures specific to cyanobacteria symbiosis-capable organisms. Our results reveal that A. agrestis and B. pusilla exhibit similar transcriptional responses to the nitrogen starvation, characterized by the upregulation of genes involved in nitrogen uptake and assimilation, hormonal regulation, stress response, and signal transduction pathways. Moreover, our findings suggest that bioactive molecules, particularly flavonoids produced under nutrient starvation, may play a role in initiating the plant-mycorrhiza and nodule-forming bacteria symbioses, particularly serving as HIF in plant-cyanobacteria symbioses.

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Diversity and regulation of symbiotic nitrogen fixation in plants

Cited by 25 publications

References 203 publications

A microbial evolutionary approach for a sustainable future

A microbial evolutionary approach for a sustainable future

Improving rice drought tolerance through host-mediated microbiome selection

Nitrogen starvation response in hornworts and liverworts provides little evidence for complex priming to the cyanobiont

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