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Overexpression of a soybean Globin (GmGlb1-1) gene reduces plant susceptibility to Meloidogyne incognita

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Abstract

Main conclusion

The overexpression of the GmGlb1-1 gene reduces plant susceptibility to Meloidogyne incognita.

Abstract

Non-symbiotic globin class #1 (Glb1) genes are expressed in different plant organs, have a high affinity for oxygen, and are related to nitric oxide (NO) turnover. Previous studies showed that soybean Glb1 genes are upregulated in soybean plants under flooding conditions. Herein, the GmGlb1-1 gene was identified in soybean as being upregulated in the nematode-resistant genotype PI595099 compared to the nematode-susceptible cultivar BRS133 during plant parasitism by Meloidogyne incognita. The Arabidopsis thaliana and Nicotiana tabacum transgenic lines overexpressing the GmGlb1-1 gene showed reduced susceptibility to M. incognita. Consistently, gall morphology data indicated that pJ2 nematodes that infected the transgenic lines showed developmental alterations and delayed parasitism progress. Although no significant changes in biomass and seed yield were detected, the transgenic lines showed an elongated, etiolation-like growth under well-irrigation, and also developed more axillary roots under flooding conditions. In addition, transgenic lines showed upregulation of some important genes involved in plant defense response to oxidative stress. In agreement, higher hydrogen peroxide accumulation and reduced activity of reactive oxygen species (ROS) detoxification enzymes were also observed in these transgenic lines. Thus, based on our data and previous studies, it was hypothesized that constitutive overexpression of the GmGlb1-1 gene can interfere in the dynamics of ROS production and NO scavenging, enhancing the acquired systemic acclimation to biotic and abiotic stresses, and improving the cellular homeostasis. Therefore, these collective data suggest that ectopic or nematode-induced overexpression, or enhanced expression of the GmGlb1-1 gene using CRISPR/dCas9 offers great potential for application in commercial soybean cultivars aiming to reduce plant susceptibility to M. incognita.

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Data availability statement

The partial genome sequences are provided in the NCBI database from GenBank accession number: GmGlb1.1_PI595099: ON228174 and GmGlb1-1_BRS133: ON228175. The nucleotide sequence can be accessed at https://www.ncbi.nlm.nih.gov/nuccore. The Sequence Read Archive (SRA) data from RNAseq are provided in the NCBI database from BioProject number: PRJNA75066. The BioProject can be accessed at https://www.ncbi.nlm.nih.gov/bioproject/. In addition, genome target sequence and transcriptome data, such as gene expression, are also provided by authors as supplementary data.

Abbreviations

DAI:

Days after inoculation

Glb:

Globin

J2:

Second-stage juveniles

NO:

Nitric oxide

pJ2:

Parasitic second-stage juveniles

ppJ2:

Pre-parasitic second-stage juveniles

Ev:

Transgenic event

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Acknowledgements

We are grateful to EMBRAPA, CAPES, CNPq, FAPESP, INCT PlantStress Biotech, INCT Bioethanol, and FAP-DF for the scientific research support. Marcela Araújo Santos, Eglee Silvia Gonçalves Igarashi, and Viviane Lopes da Costa for providing technical support in the lab.

Funding

MFB is grateful to CAPES for the postdoctoral research fellowship (process number: 88887.642997/2021-–00). AG is grateful to FAPESP 2019/13936-0. ITLT and CMP are grateful to CAPES/Cofecub project for financial support in the researcher and students exchange program between institutions. MFGS is grateful for grants from CNPq, FAP-DF, INCT Plant Stress Biotech, CAPES, and EMBRAPA. MSB is grateful for grants from INCT Bioethanol and FAPESP.

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Authors and Affiliations

  1. Embrapa Genetic Resources and Biotechnology, PqEB Final, W5 Norte, PO Box 02372, Brasília, DF, 70770-917, Brazil

    Marcos Fernando Basso, Isabela Tristan Lourenço-Tessutti, Clidia Eduarda Moreira-Pinto, Reneida Aparecida Godinho Mendes, Bruno Paes-de-Melo, Maysa Rosa das Neves, Leonardo Lima Pepino Macedo, Fabrício Barbosa Monteiro Arraes, Marcos Mota do Carmo Costa, Roberto Coiti Togawa, Ana Cristina Meneses Mendes Gomes, Maria Cristina Mattar Silva & Maria Fatima Grossi-de-Sa

  2. National Institute of Science and Technology, INCT Plant Stress Biotech, EMBRAPA, Brasília, DF, 70770-917, Brazil

    Marcos Fernando Basso, Isabela Tristan Lourenço-Tessutti, Clidia Eduarda Moreira-Pinto, Bruno Paes-de-Melo, Leonardo Lima Pepino Macedo, Fabrício Barbosa Monteiro Arraes, Roberto Coiti Togawa, Francismar Corrêa Marcelino-Guimaraes, Maria Cristina Mattar Silva, Janice de Almeida Engler & Maria Fatima Grossi-de-Sa

  3. Federal University of Brasília, Brasília, DF, 70910-900, Brazil

    Clidia Eduarda Moreira-Pinto & Reneida Aparecida Godinho Mendes

  4. Department of Botany, Biosciences Institute, University of São Paulo, São Paulo, SP, 05508-090, Brazil

    Amanda Ferreira Macedo, Adriana Grandis, Eny Iochevet Segal Floh & Marcos Silveira Buckeridge

  5. Multiuser Unit of Environmental Analysis and Institute of Biology, Federal University of Rio de Janeiro, Rio de Janeiro, RJ, 21941-971, Brazil

    Viviane Figueiredo & Alex Enrich-Prast

  6. Biogas Research Center and Department of Thematic Studies, Environmental Change, Linköping University, Linköping, Sweden

    Alex Enrich-Prast

  7. Embrapa Soybean, Londrina, PR, 86001-970, Brazil

    Francismar Corrêa Marcelino-Guimaraes

  8. INRAE, Université Côte d’Azur, CNRS, ISA, 06903, Sophia Antipolis, France

    Janice de Almeida Engler

  9. Catholic University of Brasília, Brasília, DF, 71966-700, Brazil

    Maria Fatima Grossi-de-Sa

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  1. Marcos Fernando Basso
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Correspondence to Maria Fatima Grossi-de-Sa.

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425_2022_3992_MOESM1_ESM.tif

Suppl. Fig. S1 Identification of orthologous genes of GmGlb1-1 (Glyma.11G121800) in genomes of nematode-resistant genotype PI595099 and nematode-susceptible cultivar BRS133. Pairwise sequence identity matrix from a transcript, b CDS, and c amino acid sequences of the GmGlb1-1 gene. d Alignment of amino acid sequences of the GmGlb1-1 gene, which were retrieved from genome sequencing datasets generated from genotype PI595099 and cultivar BRS133, and Glycine max Wm82.a2.v1 (BioProject: PRJNA19861). e and f In silico analysis of soybean GmGlb1-1 gene. The GmGlb1-1 (Glyma.11G121800) gene used in our study is highlighted in the red box. Positional conservation of globin-like superfamily domain (class1_nsHb_like cd:14784) generated from multiple sequence alignment by Color Align Conservation software while sequence alignment was performed using MEGA X 10 software. g Heatmap of expression profiles (Log2 of the recorded FPKM) of the soybean Globin genes in different plant tissues. The expression data were retrieved from the JGI Plant Gene Atlas Project available in Phytozome v.13 database, while data were then analyzed and viewed using Phytomine software (http://phytozome.jgi.doe.gov/phytomine/). Hierarchical clustering was performed for the transcript ratios from all conditions. The color scale shown below represents gene expression values, with blue indicating low levels while green indicating high levels of transcript abundance. FPKM values were calculated from a cufflink’s analysis of the aligned RNAseq data. h Correlation analysis from expression profiles (Log2 of the recorded FPKM) of soybean Globin genes was analyzed and viewed using Phytomine software. The globin sequences from soybean (Glycine max), bean (Phaseolus vulgaris), red clover (Trifolium pretense), barrel clover (Medicago truncatula), Arabidopsis (Arabidopsis thaliana), tomato (Solanum lycopersicum), cotton (Gossypium hirsutum), and cowpea (Vigna unguiculata) were retrieved of the Glycine max Wm82.a2.v1 (BioProject: PRJNA19861) dataset from Phytozome v.13 database (TIF 3232 KB)

425_2022_3992_MOESM2_ESM.tif

Suppl. Fig. S2 Sequence analysis of soybean GmGlb1-1 gene. The GmGlb1-1 (Glyma.11G121800) gene used in our study was highlighted with the red box. Pairwise sequence identity matrix from nucleotide a and amino acid b sequences generated using the Sequence Demarcation Tool Version 1.2 software. Evolutionary analysis from nucleotide c and e and amino acid d and f sequences generated from Phylogeny.fr web service. The globin sequences from Glycine max, Phaseolus vulgaris, Trifolium pretense, Medicago truncatula, Arabidopsis thaliana, Solanum lycopersicum, Gossypium hirsutum, and Vigna unguiculata were retrieved of the Glycine max Wm82.a2.v1 (BioProject: PRJNA19861) dataset from Phytozome v.13 database (TIF 2078 KB)

425_2022_3992_MOESM3_ESM.tif

Suppl. Fig. S3 GmGlb1-1 gene expression profile measured by real-time PCR from a 12 T1 A. thaliana and b 22 T0 N. tabacum transgenic lines compared with wild-type plants. The fold-change values were calculated with the 2^-∆∆CT formula and normalized with AtActin 2 and NtActin 4 as endogenous reference genes (Suppl. Table S3). Error bars represent confidence intervals corresponding to three technical replicates. Different letters indicate significant statistical differences between different transgenic lines based on Tukey’s test at 95% significance level. (TIF 453 KB)

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Basso, M.F., Lourenço-Tessutti, I.T., Moreira-Pinto, C.E. et al. Overexpression of a soybean Globin (GmGlb1-1) gene reduces plant susceptibility to Meloidogyne incognita. Planta 256, 83 (2022). https://doi.org/10.1007/s00425-022-03992-2

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