Skip to main content
SpringerLink
Log in

On the genetic architecture in a public tropical maize panel of the symbiosis between corn and plant growth-promoting bacteria aiming to improve plant resilience

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Exploring the symbiosis between plants and plant growth-promoting bacteria (PGPB) is a new challenge for sustainable agriculture. Even though many works have reported the beneficial effects of PGPB in increasing plant resilience for several stresses, its potential is not yet widely explored. One of the many reasons is the differential symbiosis performance depending on the host genotype. This opens doors to plant breeding programs to explore the genetic variability and develop new cultivars with higher responses to PGPB interaction and, therefore, have higher resilience to stress. Hence, we aimed to study the genetic architecture of the symbiosis between PGPB and tropical maize germplasm, using a public association panel and its impact on plant resilience. Our findings reveal that the synthetic PGPB population can modulate and impact root architecture traits and improve resilience to nitrogen stress, and 37 regions were significant for controlling the symbiosis between PGPB and tropical maize. In addition, we found two overlapping SNPs in the GWAS analysis indicating strong candidates for further investigations. Furthermore, genomic prediction analysis with genomic relationship matrix computed using only significant SNPs obtained from GWAS analysis substantially increased the predictive ability for several traits endorsing the importance of these genomic regions for the response of PGPB. Finally, the public tropical panel reveals a significant genetic variability to the symbiosis with the PGPB and can be a source of alleles to improve plant resilience.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data Availability

Genomic data: https://data.mendeley.com/datasets/5gvznd2b3n

Code availability

Code for image processing: https://github.com/RafaelYassue/Root-phenotyping

References

  • Adebayo AR, Kutu FR, Sebetha ET (2020) Data on root system architecture of water efficient maize as affected by different nitrogen fertilizer rates and plant density. Data in Brief 30:105561

    Article  PubMed  PubMed Central  Google Scholar 

  • Alexander DH, Lange K (2011) Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinformatics 12:246

    Article  PubMed  PubMed Central  Google Scholar 

  • Allen M, Poggiali D, Whitaker K et al (2021) Raincloud plots: a multi-platform tool for robust data visualization. Wellcome Open Res 4:63

    Article  Google Scholar 

  • Araus JL, Cairns JE (2014) Field high-throughput phenotyping: the new crop breeding frontier. Trends Plant Sci 19:52–61

    Article  CAS  PubMed  Google Scholar 

  • Barnawal D, Bharti N, Maji D et al (2012) 1-Aminocyclopropane-1-carboxylic acid (ACC) deaminase-containing rhizobacteria protect Ocimum sanctum plants during waterlogging stress via reduced ethylene generation. Plant Physiol Biochem 58:227–235

    Article  CAS  PubMed  Google Scholar 

  • Bashan Y, de-Bashan LE, Prabhu SR, Hernandez JP (2014) Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013). Plant Soil 378:1–33

    Article  CAS  Google Scholar 

  • Bashan Y, Levanony H (1990) Current status of Azospirillum inoculation technology: Azospirillum as a challenge for agriculture. Can J Microbiol 36:591–608

    Article  CAS  Google Scholar 

  • Batista BD, Lacava PT, Ferrari A et al (2018) Screening of tropically derived, multi-trait plant growth-promoting rhizobacteria and evaluation of corn and soybean colonization ability. Microbiol Res 206:33–42

    Article  PubMed  Google Scholar 

  • Batista BD, Dourado MN, Figueredo EF et al (2021) The auxin-producing Bacillus thuringiensis RZ2MS9 promotes the growth and modifies the root architecture of tomato (Solanum lycopersicum cv. Micro-Tom). Arch Microbiol in press.

  • Belimov AA, Dodd IC, Safronova VI et al (2014) Abscisic acid metabolizing rhizobacteria decrease ABA concentrations in planta and alter plant growth. Plant Physiol Biochem 74:84–91

    Article  CAS  PubMed  Google Scholar 

  • Bian Y, Yang Q, Balint-Kurti PJ, Wisser RJ, Holland JB (2014) Limits on the reproducibility of marker associations with southern leaf blight resistance in the maize nested association mapping population. BMC Genomics 15:1–5

    Article  CAS  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE et al (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

    Article  CAS  PubMed  Google Scholar 

  • Browning BL, Zhou Y, Browning SR (2018) A one-penny imputed genome from next-generation reference panels. Am J Hum Genet 103:338–348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Butler DG, Cullis BR, Gilmour AR, et al (2017) ASReml-R reference manual version 4. VSN International Ltd

  • Chi F, Shen S-H, Cheng H-P et al (2005) Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Appl Environ Microbiol 71:7271–7278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678

    Article  CAS  Google Scholar 

  • Cotta MS, do Amaral FP, Cruz LM, et al (2020) Genome-wide association studies reveal important candidate genes for the Bacillus pumilus TUAT-1-Arabidopsis thaliana interaction. bioRxiv

  • Creus CM, Graziano M, Casanovas EM et al (2005) Nitric oxide is involved in the Azospirillum brasilense-induced lateral root formation in tomato. Planta 221:297–303

    Article  CAS  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue

  • Egamberdiyeva D (2007) The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Appl Soil Ecol 36:184–189

    Article  Google Scholar 

  • Esteras C, Formisano G, Roig C, Díaz A, Blanca J, Garcia-Mas J, Gómez-Guillamón ML, López-Sesé AI, Lázaro A, Monforte AJ, Picó B (2013) SNP genotyping in melons: genetic variation, population structure, and linkage disequilibrium. Theor Appl Genet 126(5):1285–1303

    Article  CAS  PubMed  Google Scholar 

  • Gaffney J, Bing J, Byrne PF et al (2019) Science-based intensive agriculture: sustainability, food security, and the role of technology. Glob Food Sec 23:236–244

    Article  Google Scholar 

  • Gaiero JR, McCall CA, Thompson KA et al (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100:1738–1750

    Article  PubMed  Google Scholar 

  • Galli G, Alves FC, Morosini JS, Fritsche-Neto R (2020) On the usefulness of parental lines GWAS for predicting low heritability traits in tropical maize hybrids. PLoS One 15:e0228724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gamalero E, Lingua G, Berta G, Glick BR (2009) Beneficial role of plant growth promoting bacteria and arbuscular mycorrhizal fungi on plant responses to heavy metal stress. Can J Microbiol 55:501–514

    Article  CAS  PubMed  Google Scholar 

  • Grieder C, Trachsel S, Hund A (2014) Early vertical distribution of roots and its association with drought tolerance in tropical maize. Plant Soil 377:295–308

    Article  CAS  Google Scholar 

  • Gutiérrez-Luna FM, López-Bucio J, Altamirano-Hernández J et al (2010) Plant growth-promoting rhizobacteria modulate root-system architecture in Arabidopsis thaliana through volatile organic compound emission. Symbiosis 51:75–83

    Article  CAS  Google Scholar 

  • Hoagland DR, Snyder WC (1933) Nutrition of strawberry plant under controlled conditions : (a) effects of deficiencies of boron and certain other elements : (b) susceptibility to injury from sodium salts. Proceed Am Soc Horticult Sci 30:288

    Google Scholar 

  • Hungria M, Campo RJ, Souza EM, Pedrosa FO (2010) Inoculation with selected strains of Azospirillum brasilense and A. lipoferum improves yields of maize and wheat in Brazil. Plant Soil 331:413–425

    Article  CAS  Google Scholar 

  • Jeong S, Kim J-Y, Kim N (2020) GMStool: GWAS-based marker selection tool for genomic prediction from genomic data. Sci Rep 10:19653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ji X, Lu G, Gai Y et al (2010) Colonization of Morus alba L. by the plant-growth-promoting and antagonistic bacterium Burkholderia cepacia strain Lu10-1. BMC Microbiol 10:243

    Article  PubMed  PubMed Central  Google Scholar 

  • Kant S, Bi Y-M, Rothstein SJ (2011) Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. J Exp Bot 62:1499–1509

    Article  CAS  PubMed  Google Scholar 

  • Khan AL, Waqas M, Kang S-M et al (2014) Bacterial endophyte Sphingomonas sp. LK11 produces gibberellins and IAA and promotes tomato plant growth. J Microbiol 52:689–695

    Article  CAS  PubMed  Google Scholar 

  • Khan MIR, Trivellini A, Fatma M et al (2015) Role of ethylene in responses of plants to nitrogen availability. Front Plant Sci 6:927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kroll S, Agler MT, Kemen E (2017) Genomic dissection of host–microbe and microbe–microbe interactions for advanced plant breeding. Curr Opin Plant Biol 36:71–78

    Article  CAS  PubMed  Google Scholar 

  • Laurance WF, Sayer J, Cassman KG (2014) Agricultural expansion and its impacts on tropical nature. Trends Ecol Evol 29:107–116

    Article  PubMed  Google Scholar 

  • Lemanceau P, Blouin M, Muller D, Moënne-Loccoz Y (2017) Let the core microbiota be functional. Trends Plant Sci 22:583–595

    Article  CAS  PubMed  Google Scholar 

  • Liu F, Xing S, Ma H et al (2013) Cytokinin-producing, plant growth-promoting rhizobacteria that confer resistance to drought stress in Platycladus orientalis container seedlings. Appl Microbiol Biotechnol 97:9155–9164

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Huang M, Fan B et al (2016) Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PLoS Genet 12:e1005767

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lombardi M, De Gara L, Loreto F (2021) Determinants of root system architecture for future-ready, stress-resilient crops. Physiol Plant. https://doi.org/10.1111/ppl.13439

    Article  PubMed  PubMed Central  Google Scholar 

  • Lynch JP (2013) Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Ann Bot 112:347–357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martins MR, Jantalia CP, Reis VM et al (2018) Impact of plant growth-promoting bacteria on grain yield, protein content, and urea-15 N recovery by maize in a Cerrado Oxisol. Plant Soil 422:239–250

    Article  CAS  Google Scholar 

  • Matias FI, Sabadin JFG, Moreira LA, et al (2021) Soil-app: a tool for soil analysis interpretation. Sci Agric 78.: https://doi.org/10.1590/1678-992x-2019-0113

  • Ma W, Li J, Qu B et al (2014) Auxin biosynthetic gene TAR2 is involved in low nitrogen-mediated reprogramming of root architecture in Arabidopsis. Plant J 78:70–79

    Article  CAS  PubMed  Google Scholar 

  • Mi G, Chen F, Wu Q et al (2010) Ideotype root architecture for efficient nitrogen acquisition by maize in intensive cropping systems. Sci China Life Sci 53:1369–1373

    Article  PubMed  Google Scholar 

  • Molina‐Favero C, Creus CM, Lanteri ML, et al (2007) Nitric oxide and plant growth promoting rhizobacteria: common features influencing root growth and development. Advances in Botanical Research 1–33

  • Obeidat W, Avila L, Earl H, Lukens L (2018) Leaf spectral reflectance of maize seedlings and its relationship to cold tolerance. Crop Sci 58:2569–2580

    Article  CAS  Google Scholar 

  • Olivoto T, Lúcio AD (2020) metan: an R package for multi-environment trial analysis. Methods Ecol Evol 11:783–789

    Article  Google Scholar 

  • Poland JA, Brown PJ, Sorrells ME, Jannink J-L (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS One 7:e32253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pradhan P, Fischer G, van Velthuizen H et al (2015) Closing yield gaps: how sustainable can we be? PLoS One 10:e0129487

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Proietti S, Caarls L, Coolen S et al (2018) Genome-wide association study reveals novel players in defense hormone crosstalk in Arabidopsis. Plant Cell Environ 41:2342–2356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiao S, Fang Y, Wu A et al (2019) Dissecting root trait variability in maize genotypes using the semi-hydroponic phenotyping platform. Plant Soil 439:75–90

    Article  CAS  Google Scholar 

  • Qi X, Fu Y, Wang RY et al (2018) Improving the sustainability of agricultural land use: an integrated framework for the conflict between food security and environmental deterioration. Appl Geogr 90:214–223

    Article  Google Scholar 

  • Quecine MC, Araujo WL, Rossetto PB et al (2012) Sugarcane growth promotion by the endophytic bacterium Pantoea agglomerans 33.1. Appl Environ Microb 78:7511–7518

    Article  CAS  Google Scholar 

  • Ray DK, Mueller ND, West PC, Foley JA (2013) Yield trends are insufficient to double global crop production by 2050. PLoS One 8:e66428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Remans R, Beebe S, Blair M et al (2008) Physiological and genetic analysis of root responsiveness to auxin-producing plant growth-promoting bacteria in common bean (Phaseolus vulgaris L.). Plant Soil 302:149–161

    Article  CAS  Google Scholar 

  • Rodríguez-Blanco A, Sicardi M, Frioni L (2015) Plant genotype and nitrogen fertilization effects on abundance and diversity of diazotrophic bacteria associated with maize (Zea mays L.). Biol Fertil Soils 51:391–402

    Article  CAS  Google Scholar 

  • Rojas-Tapias D, Moreno-Galván A, Pardo-Díaz S et al (2012) Effect of inoculation with plant growth-promoting bacteria (PGPB) on amelioration of saline stress in maize (Zea mays). Appl Soil Ecol 61:264–272

    Article  Google Scholar 

  • Rosier A, Medeiros FHV, Bais HP (2018) Defining plant growth promoting rhizobacteria molecular and biochemical networks in beneficial plant-microbe interactions. Plant Soil 428:35–55

    Article  CAS  Google Scholar 

  • Rouphael Y, Spíchal L, Panzarová K, et al (2018) High-throughput plant phenotyping for developing novel biostimulants: from lab to field or from field to lab? Front Plant Sci 9.: https://doi.org/10.3389/fpls.2018.01197

  • Sandhya V, Ali SZ, Grover M et al (2010) Effect of plant growth promoting Pseudomonas spp. on compatible solutes, antioxidant status and plant growth of maize under drought stress. Plant Growth Regul 62:21–30

    Article  CAS  Google Scholar 

  • Santoyo G, Moreno-Hagelsieb G, del Carmen O-M, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99

    Article  CAS  PubMed  Google Scholar 

  • Seethepalli A, Dhakal K, Griffiths M, (2021) et al RhizoVision Explorer: open-source software for root image analysis and measurement standardization

  • Shamimuzzaman M, Gardiner JM, Walsh AT et al (2020) MaizeMine: a data mining warehouse for the maize genetics and genomics database. Front Plant Sci 11:592730

    Article  PubMed  PubMed Central  Google Scholar 

  • Sim S-C, Durstewitz G, Plieske J et al (2012) Development of a large SNP genotyping array and generation of high-density genetic maps in tomato. PLoS ONE 7:e40563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strigens A, Grieder C, Haussmann BIG, Melchinger AE (2012) Genetic variation among inbred lines and testcrosses of maize for early growth parameters and their relationship to final dry matter yield. Crop Sci 52:1084–1092

    Article  Google Scholar 

  • Trachsel S, Kaeppler SM, Brown KM, Lynch JP (2011) Shovelomics: high throughput phenotyping of maize (Zea mays L.) root architecture in the field. Plant Soil 341:75–87

    Article  CAS  Google Scholar 

  • Valente J, Gerin F, Le Gouis J et al (2020) Ancient wheat varieties have a higher ability to interact with plant growth-promoting rhizobacteria. Plant, Cell Environ 43:246–260

    Article  CAS  Google Scholar 

  • Van Deynze A, Zamora P, Delaux P-M et al (2018) Nitrogen fixation in a landrace of maize is supported by a mucilage-associated diazotrophic microbiota. PLOS Biology 16:e2006352

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • VanRaden PM (2008) Efficient methods to compute genomic predictions. J Dairy Sci 91:4414–4423

    Article  CAS  PubMed  Google Scholar 

  • Vejan P, Abdullah R, Khadiran T et al (2016) Role of plant growth promoting rhizobacteria in agricultural sustainability—a review. Molecules 21:573

    Article  PubMed Central  CAS  Google Scholar 

  • Vidotti MS, Lyra DH, Morosini JS et al (2019) Additive and heterozygous (dis)advantage GWAS models reveal candidate genes involved in the genotypic variation of maize hybrids to Azospirillum brasilense. PLoS One 14:e0222788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vidotti MS, Matias FI, Alves FC et al (2019) Maize responsiveness to Azospirillum brasilense: insights into genetic control, heterosis and genomic prediction. PLoS One 14:e0217571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner MR, Roberts JH, Balint-Kurti P, Holland JB (2020) Heterosis of leaf and rhizosphere microbiomes in field-grown maize. New Phytol 228:1055–1069

    Article  CAS  PubMed  Google Scholar 

  • Wallace JG, Zhang X, Beyene Y et al (2016) Genome-wide association for plant height and flowering time across 15 tropical maize populations under managed drought stress and well-watered conditions in sub-Saharan Africa. Crop Sci 56:2365–2378

    Article  CAS  Google Scholar 

  • Wang X, Wang H, Liu S et al (2016) Genetic variation in ZmVPP1 contributes to drought tolerance in maize seedlings. Nat Genet 48:1233–1241

    Article  CAS  PubMed  Google Scholar 

  • Wei Z, Jousset A (2017) Plant breeding goes microbial. Trends Plant Sci 22:555–558

    Article  CAS  PubMed  Google Scholar 

  • Wintermans PCA, Bakker PAHM, Pieterse CMJ (2016) Natural genetic variation in Arabidopsis for responsiveness to plant growth-promoting rhizobacteria. Plant Mol Biol 90:623–634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan W, Frégeau-Reid J (2018) Genotype by yield* trait (GYT) biplot: a novel approach for genotype selection based on multiple traits. Sci Rep 8:1–10

    Article  Google Scholar 

  • Yassue RM, Sabadin JFG, Galli G, Alves FC (2021) CV-α: designing validations sets to increase the precision and enable multiple comparison tests in genomic prediction. Euphytica 217:106

    Article  CAS  Google Scholar 

  • Yin L, Zhang H, Tang Z, et al (2020) rMVP: a memory-efficient, visualization-enhanced, and parallel-accelerated tool for genome-wide association study. 2020.08.20.258491

  • Yonis BO, Pino Del Carpio D, Wolfe M et al (2020) Improving root characterisation for genomic prediction in cassava. Sci Rep 10:8003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • York LM, Galindo-Castañeda T, Schussler JR, Lynch JP (2015) Evolution of US maize (Zea mays L.) root architectural and anatomical phenes over the past 100 years corresponds to increased tolerance of nitrogen stress. J Exp Bot 66:2347–2358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng X, Levine D, Shen J et al (2012) A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28:3326–3328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. The Plant Genome 1:1–16

    Article  CAS  Google Scholar 

Download references

Funding

This study was financed in part by São Paulo Research Foundation (FAPESP, Process: 19/04697–2; 17/24327–0), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001, and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

Author information

Authors and Affiliations

  1. Department of Genetics, Luiz de Queiroz College of Agriculture, University of São Paulo, Piracicaba, São Paulo, Brazil

    Rafael Massahiro Yassue, Humberto Fanelli Carvalho, Raysa Gevartosky, Felipe Sabadin, Pedro Henrique Souza, Maria Leticia Bonatelli, João Lúcio Azevedo, Maria Carolina Quecine & Roberto Fritsche-Neto

Authors
  1. Rafael Massahiro Yassue
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Humberto Fanelli Carvalho
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Raysa Gevartosky
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Felipe Sabadin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pedro Henrique Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maria Leticia Bonatelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. João Lúcio Azevedo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Maria Carolina Quecine
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Roberto Fritsche-Neto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rafael Massahiro Yassue.

Ethics declarations

Ethics approval

Not applicable because this article does not contain any studies with human or animal subjects.

Consent to participate

Not applicable because this article does not contain any studies with human or animal subjects.

Consent for publication

All authors have approved the manuscript and agreed with submission to the Molecular Breeding journal.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 79 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yassue, R.M., Carvalho, H.F., Gevartosky, R. et al. On the genetic architecture in a public tropical maize panel of the symbiosis between corn and plant growth-promoting bacteria aiming to improve plant resilience. Mol Breeding 41, 63 (2021). https://doi.org/10.1007/s11032-021-01257-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11032-021-01257-6

Keywords

Search

Navigation