Source: UNIVERSITY OF CALIFORNIA, DAVIS submitted to NRP
BENEFICIAL PLANT MICROBE INTERACTIONS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1013601
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Oct 1, 2017
Project End Date
Sep 30, 2022
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
UNIVERSITY OF CALIFORNIA, DAVIS
410 MRAK HALL
DAVIS,CA 95616-8671
Performing Department
Plant Sciences
Non Technical Summary
This project supports the mission of the Agricultural Experiment Station by addressing the Hatch Act area(s) of: plant and animal production, protection, and health; sustainable agriculture; biotechnology Plants require a source of reduced nitrogen for growth and development. This can be provided in the form of organic or inorganic fertilizer or, for some plants, from plant-associated microbes capable of carrying out biological nitrogen fixation. Corn is a major user of inorganic nitrogen fertilizer and does not typically associate with nitrogen fixing microbes. This project will examine indigenous landraces of corn that appear to associate nitrogen fixing microbes in order to understand the mechanisms of this association and whether an association with nitorgen fixing microbes can be transferred to modern corn varieties.
Animal Health Component
(N/A)
Research Effort Categories
Basic
100%
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2011510106025%
2021510106025%
2031510110050%
Goals / Objectives
Plants grow in close association with microbial communities that influence plant traits related to nutrient acquisition, plant development, plant defenses, and abiotic stress responses. The root-associated microbiota of Arabidopsis thaliana has been characterized and shown to be much less complex than the microbiota of the surrounding soil, being enriched in Proteobacteria, Bacteroidetes, and Actinobacteria. These microbes are selected in part by plant cell wall features and metabolic cues from host cells. Characterization of the rhizosphere microbiome associated with 27 modern maize inbred lines also indicated substantial differences in relative abundance of microbial taxa between bulk soil and the rhizosphere with the maize genotype contributing a small but significant influence on the rhizosphere selectivity. Similarly, the maize seed-associated microbiota in wild maize ancestors (teosinte) and geographically diverse modern maize was shown to have a phylogenetic-dependent community composition overlaid upon a core microbiota conserved across evolutionary and geographical boundaries. Collectively, these studies suggest that the plant microbiome is determined, at least in part, by the genetics of the host plant. Nitrogen-fixing microbial associations with non-legumes, especially cereals, have been a topic of intense interest for several decades. Nitrogen-fixing endophytes contribute to the nitrogen nutrition of sugarcane in some environments, but there is little evidence for the occurrence of efficient associations in other cereals. Triplett (1996) suggested that to identify maize diazotrophic endophytes, it may be interesting to survey primitive maize landraces from many locations including the areas of maize origin. Estrada et al. (2002) followed this suggestion and examined a landrace of maize in the Sierra Juarez region of Oaxaca, Mexico. This group successfully isolated a nitrogen-fixing endophyte from the resident maize landrace and tentatively identified the isolate as a new species of Burkholderia but did not demonstrate that atmospheric dinitrogen (N2) contributed to the nitrogen economy of the plant. Interestingly this group also reported the isolation of a similar endophyte from field grown teosinte plants and speculated that the Burkholderia strain might have formed a primitive symbiosis with teosinte that persisted during domestication of maize. We also learned of isolated indigenous landraces of maize in the Sierra Juarez region of Oaxaca that were reportedly grown using traditional practices with little or no fertilizer and speculated that these might have evolved unique microbial community associations not found in maize that had been cultivated and selected under high nutrient conditions. This indigenous maize landrace is characterized by an extensive development of aerial roots that produce large amounts of mucilage. The mucilage associated with maize underground roots has been previously described and it has been suggested that root exudates play a significant role in structuring rhizosphere microbial communities. Indeed, it has been shown that pea root mucilage can serve as a sole carbon source for some rhizosphere bacteria, including Rhizobium sp., Burkholderia sp. and Pseudomonas sp. In this project we will 1) examine the microbiota associated with Sierra Juarez indigenous maize and determine whether the mucilage supports a diazotrophic microbial community, 2) assess the contribution of diazotrophic activity to maize N nutrition and 3) characterize resident microbes and their ability to promote growth of other crops.
Project Methods
Plant Material Sierra Juarez maize seeds will be obtained in Sierra Juarez region of Oaxaca, Mexico (N 17° 15.772′; W 096° 01.758′), from an open pollinated population. Zea mays subsp. mexicana (Teosinte), LH123HT, Mo17, PHG39, LH82, PH207, and B73 seeds were obtained from USDA National Plant Germplasm System (NPGS) (accessions Ames 8083, PI601079, PI558532, PI600981, PI601170, PI601005, and PI550473, respectively). Maize line Hickory King was obtained from Victory Seeds (accession 3140041). Sample CollectionRhizosphere and plant tissues that include stem, leaf, aerial roots, underground roots and mucilage of Sierra Juarez maize will be sampled in Sierra Juarez. For plant endophyte analysis, tissues will be surface sterilized by rinsing with mqH2O, shaken gently in 70% ethanol for 5 minutes, placed into 1% hypochlorite bleach gently stirred for 10 minutes, rinsed three times in mqH20 and dried in a laminar flow cabinet. Roots and stems will also dissected to remove epidermal tissues before extraction. For seed endophyte analysis, embryo and endosperm of Sierra Juarez, Hickory King, and B73 will be withdrawn from the seeds by hand using a razor blade in a laminar flow cabinet and collected. Rhizosphere will be defined as a layer of soil covering the outer surface of the root system that could be washed from roots in a buffer/detergent solution. Plant GrowthFor experiments in the greenhouse, seeds of Sierra Juarez maize and conventional varieties will be surface sterilized and germinated. After one week, seedlings will be transplanted in 40-liter pots filled with a mix of sand and perlite (v:v) and grown in a high ceiling greenhouse. Plants were watered twice a day for two minutes with half-strength of Hoagland solution3. For experiments in the field, three independent plots of 20 plants per genotype will be planted with three border rows (B73) between each genotype. Measurements of the Sierra Juarez maize will be taken for 135 days post-planting. Mucilage Glycosyl CompositionGlycosyl composition analysis of the mucilage will be performed by combined gas chromatography/mass spectrometry (GC/MS) of the per-O-trimethylsilyl (TMS) derivatives of the monosaccharide methyl glycosides produced from the sample by acidic methanolysis. Methyl glycosides will first be prepared from dry mucilage samples by methanolysis in 1 M HCl in methanol at 80°C (18-22 hours), followed by re-N-acetylation with pyridine and acetic anhydride in methanol (for detection of amino sugars). The samples will then be per-O-trimethylsilylated by treatment with Tri-Sil (Pierce) at 80°C (0.5 hours) and GC/MS analysis of the TMS methyl glycosides performed on an HP 6890 GC interfaced to a 5975b MSD, using an All Tech EC-1 fused silica capillary column (30m 0.25 mm ID). Metagenome AnalysisDNA (80-150ngμl?1) will be extracted from 100 mg of the rhizosphere, plant tissues using a DNA isolation kit (Mo Bio Laboratories, Inc, USA). The PCR control for microbial DNA isolation will be performed on 16S rDNA genes. PCR will be performed using eubacterial primers 27F (5′-AGAGTTTGATCCTGGCTCAG-3′), and 1492R (5′-GGTTACCTTGTTACGACTT-3′). Amplification will be carried out with 1 ?M of each primer in 3 mM MgCl2, 20 μM of each dNTP, 1.25 units of Taq polymerase (Promega) in a total volume of 20 μl of 1× reaction buffer (Promega). The products obtained will be purified with a NucleoSpin Gel extraction kit (Clontech, Palo Alto, USA).Illumina-based 16S rRNA Gene Sequencing16S rDNA PCR and sequencing of rhizosphere and plant tissues will be carried out using the Caporaso protocol4, extended to include a dual barcode scheme for each sample and replacing the Golay barcodes with a different set of Illumina-compatible barcodes designed to balance base composition and tolerate up to four sequencing errors in barcode sequences. The barcodes will be designed to allow pooling of multiple samples within a single MiSeq run. Ten cycles of PCR with barcoded primers will be performed at low annealing temperature (55°C); samples were then pooled and cleaned using a Qiagen column to remove the unincorporated primers. At this stage, an additional 10 or 20 cycles of PCR will be performed on the pool using the Illumina paired-end flowcell primers with a higher annealing temperature (65°C). The resulting PCR product will be subjected to QC with an Agilent Bioanalyzer and estimated concentration using KAPA Biosystems qPCR kit. The samples will be diluted to the appropriate loading concentration for a MiSeq run, spiked with 25% phiX control library, and sequenced using an Illumina MiSeq instrument with the manufacturer's standard 150 nucleotides paired-end dual-index sequencing protocol and the custom sequencing primers. Alpha and Beta diversity metrics will be generated using the Phyloseq R package.Illumina sequencing libraries from the same DNA extractions as above will be made using an adaptation of the Nextera transposase-based library construction method with multiplex barcoding. Samples will then be submitted to sequencing using the MiSeq and HiSeq instruments. Illumina sequences will then be demultiplexed and trimmed using Trimmomatic (ver 0.33) with the following parameter: Illuminaclip 2:30:10, Headcrop:15, Leading:20, Trailing:20, Sliding window:4:20, and Minlen:100. Nitrogenase SearchPeptide sequences of the six core nif genes (nifH, nifD, nifE, nifK, nifN, nifB) and alternate nitrogenase (anfG, vnfG) from known diazotrophs as previously published will be retrieved from GenPept as a reference. A blast search (E-value < 0.001) of six frame-translated metagenomic reads will be conducted against these reference sequences and the hits aligned against the multiple sequences alignment of reference using clustal-Omga followed by generation of phylogenetic trees for every individual nif gene using Fasttree2.1 with WAG model of amino acid evolution and gamma20 likelihood. The counts of nif genes can be normalized by recA counts ( determined using RecA TIGRFAM HMM with HMMER3 and an e-value cutoff of e-10).Acetylene Reduction Assay (ARA)For ARA with the mucilage, 2 ml of freshly collected mucilage from one or two aerial roots (Sierra Juarez) or several plants (teosinte) grown in the field will be introduced into sealed 14.5 ml vials (Wheaton). Then, 850 μl of acetylene (Airgas) will be injected into each vial and ethylene quantified by injecting 1 ml of the air phase, sampled after 72 hours, on a Gas Chromatography (GC-2010 Shimadzu) equipped with a Rt-Alumina BOND/KCL column (Restek).Mucilage 15N2 Assimilation The enrichment of mucilage in 15N atom will be achieved by removing 4 ml of headspace gas and replacing it with 4 ml of either 15N2 or 14N2 nitrogen gas directly into a vial containing 1.0 mL of mucilage. Mucilage samples will be incubated at 37°C for 0 and 70 hours in the presence of 15N2. 15N2 assimilation will be stopped by freezing the mucilage samples at -20°C, the samples freeze-dried and weighed and 15N analysis in the mucilage samples performed at the UC Davis Stable Isotope Facility (Davis, CA).15N Stable Isotope Analysis The proportion (%) of nitrogen derived from biological nitrogen fixation (%Ndfa) will be estimated from the 15N natural abundance (expressed in delta units, ‰) of the Sierra Juarez maize (δ15Nfixing plant) and that of the reference plant species (δ15Nref). Individual maize samples and reference plant samples, representing 8-10 species of non-nitrogen-fixing plants will be analyzed.

Progress 10/01/19 to 09/30/20

Outputs
Target Audience:The target audiences of this project include the scientific community, agricultural technology companies and the public. These audiences were directly addressed through scientific journal publications, industry seminars and two podcasts. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?The project provided a highly interdiscipinary training environment spanning plant biology, microbiology and metagenomics for one graduate student. How have the results been disseminated to communities of interest?The genomic characterization was published in open source journals and so this information is widely available to the scientific community. What do you plan to do during the next reporting period to accomplish the goals?During the next reporting period, we will focus on two major goals: 1) determining the alternative mechanisms on N2 fixation and 2) determine the maize genetic determinants for diazotrophic microbial association.

Impacts
What was accomplished under these goals? A collection of diazotrophic microbial isolates from maize were characterized with regard to their N2 fixing capability and their potential to stimulate plant growth. We sequenced over 600 microbial genomes and determined that there exist novel pathways for microbial N2 fixation.

Publications

  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Higdon SM, PozzoT, Kong N, Huang BC, Yang ML, Jeannotte R, Brown CT, Bennett AB, Weimer BC. 2020. Genomic characterization of a diazotrophic microbiota associated with maize aerial root mucilage. PLoS ONE 15(9): e0239677. https://doi.org/10.1371/journal.pone.0239677
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Higdon SM, PozzoT, Tibbett EJ, Chiu C, Jeannotte R, Weimer BC, Bennett AB, 2020. Diazotrophic bacteria from maize exhibit multifaceted plant growth promotion traits in multiple hosts. PLoS ONE 15(9): e0239081. https://doi.org/10.1371/journal.pone.0239081
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Higdon SM, Huang BC, Bennett AB, Weimer BC. 2020. Identification of Nitrogen Fixation Genes in Lactococcus Isolated from Maize Using Population Genomics and Machine Learning. Microorganisms. 8(12):2043. https://doi.org/10.3390/microorganisms8122043


Progress 10/01/18 to 09/30/19

Outputs
Target Audience:The target audiences of this project include the scientific community, agricultural technology companies and the public. These audiences were directly addressed through scientific journal publications, industry seminars and a podcast (http://www.talkingbiotechpodcast.com/154-nitrogen-fixing-and-corn/). Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?The project provided a highly interdisciplinary training environment spanning plant biology, microbiology and metagenomics for one graduate student. How have the results been disseminated to communities of interest?The results have been disseminated in seminars to two agricultural technology companies (KWS Seeds and Pivot Biotechnology) and one major agricultural university (University of Missouri), through scientific publications and through a podcast targeted to the public (http://www.talkingbiotechpodcast.com/154-nitrogen-fixing-and-corn/. ? What do you plan to do during the next reporting period to accomplish the goals?During the next reporting period, we will focus on two major goals: 1) determining the microbial determinants of cereal crop diazotrophic association and 2) assess the potential of using cereal crop associated microbes to promote growth in other crops.

Impacts
What was accomplished under these goals? We previously reported that an indigenous landrace of maize found in Totontepec Villa de Morelos in the Sierra Mixe region of Mexico acquires 28-82% of its nitrogen from the air. This conclusion was supported by multiple techniques to evaluate nitrogen fixation: acetylene reduction assays (ARA), 15N natural abundance, 15N dilution, 15N gas enrichment, and nitrogen balance experiments. Interestingly, unlike most modern maize varieties, this Sierra Mixe maize develops extensive aerial roots which secrete large amounts of mucilage after rain. This mucilage is rich in arabinose, fucose, and galactose and harbors a diazotrophic microbial community which was concluded to be, at least partially, responsible for the fixation and delivery of atmospheric nitrogen to the maize plant. In this reporting period, we determined the structure of the complex polysaccharide that comprises the mucilage which led to the identification of specific catabolic activities required of the diazotrophic community to utilize this presumptive source of carbohydrate. The role of mucilage in providing an environment for nitrogen fixation has also been proposed in different biological systems, including the Gunnera-Nostoc and the Azolla-Anabaena symbioses. During this reporting period, we developed a general model for a functional diazotrophic plant-microbe association proposedthat this may be a general feature supporting nitrogen fixation in cereal crops. This model is intended to provide a framework to evaluate diazotrophic activity in cereal crops and, potentially, to increase nitrogen fixation in cereals by optimizing these mucilage functionalities through genetic selection and/or the structure of mucilage-associated microbial communities.

Publications

  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Amicucci MJ, Galermo AG, Guerrero A, Treves G, Nandita E, Kailema MJ, Higdon S, Pozzo T, Labavitch J, Bennett AB, Lebrilla CB. 2019. Strategy for Structural Elucidation of Polysaccharides: Elucidation of a maize mucilage that harbors diazotrophic bacteria. Anal Chem: DOI: 10.1021/acs.analchem.9b00789
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Bennett AB, Pankievicz VCS, Ane J-M. 2020. A model for nitrogen fixation in cereal crops. Trends in Pl Sci., 25:226-235. https://doi.org/10.1016/j.tplants.2019.12.004


Progress 10/01/17 to 09/30/18

Outputs
Target Audience:Microbiologists and plant breeders in public and private institutions. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?The project provided a highly interdisciplinary training environment spanning plant biology, microbiology and metagenomics for students and postdoctoral associates. How have the results been disseminated to communities of interest?Results were disseminated through scientific publications as well as numerous press reports such as this example from The Atlantic. https://www.theatlantic.com/science/archive/2018/08/amaizeballs/567140/ What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? We completed studies of an indigenous landrace of maize grown in nitrogen depleted soils in the Sierra Mixe region of Oaxaca, Mexico. This landrace is characterized by extensive development of aerial roots that secrete a carbohydrate-rich mucilage. Analysis of the mucilage microbiota indicated that it was enriched in taxa for which many known species are diazotrophic; was enriched for homologs of genes encoding nitrogenase subunits; and harbored active nitrogenase activity as assessed by acetylene reduction and 15N2 incorporation assays. Field experiments in Sierra Juarez using I SN natural abundance or I SN-enrichment assessments over five years indicated that atmospheric nitrogen fixation contributed 30-82% of the nitrogen nutrition of Sierra Mixe maize.

Publications

  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Van Deynze A, Zamora P, Delaux P-M, Heitmann C, Jayaraman D, Rajasekar S, Maeda J, Bhatnagar S, Jospin G, Graham D, Jeannotte R, Gibson D, Darling A, Schwartz KD, Berry AM, Lopez landrace J, of Weimer maize is BC, Eisen supported JA, by a Shapiro H-Y, mucilage-associated Ane J-M. Bennett diazotrophic AB. (2018) microbiota. Nitrogen PLoS fixation Biol in 16(8):e2006352
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Pozo T, Higdon SM, Pattathil S, Hahn MG, Bennett AB. 2018. Characterization of novel glycosyl hydrolases discovered by cell wall glycan directed monodonal antibody screening and metagenome analysis of maize aerial root mucilage. PLoS ONE 13(9): e0204525. https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0204525