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Suppression of tomato bacterial wilt by anaerobic soil disinfestation and associations with production of antagonistic compounds

Plant and Soil (2022)Cite this article

Abstract

Background

Anaerobic soil disinfestation (ASD) has been proven to be an effective and environmentally friendly method for controlling soil-borne plant diseases. Mechanisms of ASD-mediated pathogen suppression are not fully elucidated but appear to depend on the carbon (C) sources used and involve a combination of abiotic and biotic factors. This study sought to assess the impacts of ASD with different C sources on soil chemical properties, microbial activity, and antagonistic compounds, and identify the major factor(s) driving suppression of tomato bacterial wilt caused by Ralstonia solanacearum.

Methods

A pot experiment was conducted containing five treatments, i.e., untreated control (CK), anaerobic treatment without C source (ASD-CK), anaerobic treatment with rice bran (ASD-R), wheat bran (ASD-W) and peanut bran (ASD-P).

Results

All the ASD treatments significantly reduced disease incidence by 83–100% and simultaneously promoted tomato growth, while anaerobic treatments with C sources achieved a better effect than anaerobic treatment alone. This could be associated with the improved soil chemical (lowered Eh, NO3−, SO42− and elevated pH) and biological (elevated dehydrogenase and urease activities) properties and elevated production of antagonistic compounds (Fe2+, Mn2+, citric acid, succinic acid, and ammonia) by anaerobic treatments with C sources. Redundancy analysis further indicated that the elevated ammonia (11.1%, P = 0.002), Mn2+ (5.3%, P = 0.002), citric acid (1.8%, P = 0.046) and urease activity (1.0%, P = 0.036) were the major factors driving disease suppression, which all achieved the highest value in ASD-P.

Conclusions

In summary, the incorporation of organic materials that improve antagonistic compounds (especially ammonia) production could induce higher inhibition effect against tomato bacterial wilt during the ASD process.

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References

  • Blok WJ, Lamers JG, Termorshuizen AJ, Bollen GJ (2000) Control of soilborne plant pathogens by incorporating fresh organic amendments followed by tarping. Phytopathology 90:253–259

    CAS  Article  Google Scholar 

  • Butler DM, Kokalis-Burelle N, Albano JP, McCollum TG, Muramoto J, Shennan C, Rosskopf EN (2014) Anaerobic soil disinfestation (ASD) combined with soil solarization as a methyl bromide alternative: vegetable crop performance and aoil nutrient dynamics. Plant Soil 378:365–381

    CAS  Article  Google Scholar 

  • Butler DM, Ownley BH, Dee ME, Eichler Inwood SE, McCarty DG, Shrestha U, Kokalis-Burelle N, Rosskopf EN (2014) Low carbon amendment rates during anaerobic soil disinfestation (ASD) at moderate soil temperatures do not decrease viability of Sclerotinia sclerotiorum sclerotia or fusarium root rot of common bean. Acta Horticult 1044:203–208

    Article  Google Scholar 

  • Butler DM, Rosskopf EN, Kokalis-Burelle N, Albano JP, Muramoto J, Shennan C (2012) Exploring warm-season cover crops as carbon sources for anaerobic soil disinfestation (ASD). Plant Soil 355:149–165

    CAS  Article  Google Scholar 

  • Cameron KC, Di HJ, Moir JL (2013) Nitrogen losses from the soil/plant system: a review. Ann Appl Biol 162:145–173

    CAS  Article  Google Scholar 

  • Di Gioia F, Ozores-Hampton M, Zhao X, Thomas J, Wilson P, Li Z, Hong J, Albano J, Swisher M, Rosskopf E (2017) Anaerobic soil disinfestation impact on soil nutrients dynamics and nitrous oxide emissions in fresh-market tomato. Agr Ecosyst Environ 240:194–205

    Article  Google Scholar 

  • Diogo RVC, Wydra K (2007) Silicon-induced basal resistance in tomato against Ralstonia solanacearum is related to modification of pectic cell wall polysaccharide structure. Physiol Mol Plant P 70:120–129

    CAS  Article  Google Scholar 

  • Gambrell RP (1996) Manganese. In: Sparks DL, Page AL, Helmke PA, Loeppert RH, Soltanpour PN, Tabatabai MA, Johnston CT, Sumner ME (eds) Methods of Soil Analysis Part 3-Chemical Methods. Soil Science Society of America, American Society of Agronomy, Madison, WI, pp 665–682

    Google Scholar 

  • Goud J-KC, Termorshuizen AJ, Blok WJ, van Bruggen AHC (2004) Long-term effect of biological soil disinfestation on Verticillium wilt. Plant Dis 88:688–694

    Article  Google Scholar 

  • Hewavitharana SS, Ruddell D, Mazzola M (2014) Carbon source-dependent antifungal and nematicidal volatiles derived during anaerobic soil disinfestation. Eur J Plant Pathol 140:39–52

    CAS  Article  Google Scholar 

  • Huang XQ, Liu LL, Wen T, Zhang JB, Wang FH, Cai ZC (2016) Changes in the soil microbial community after reductive soil disinfestation and cucumber seedling cultivation. Appl Microbiol Biot 100:5581–5593

    CAS  Article  Google Scholar 

  • Huang XQ, Wen T, Zhang JB, Meng L, Zhu TB, Liu LL, Cai ZC (2015) Control of soil-borne pathogen Fusarium oxysporum by biological soil disinfestation with incorporation of various organic matters. Eur J Plant Pathol 143:223–235

    CAS  Article  Google Scholar 

  • Husson O (2013) Redox potential (Eh) and pH as drivers of soil/plant/microorganism systems: a transdisciplinary overview pointing to integrative opportunities for agronomy. Plant Soil 362:389–417

    CAS  Article  Google Scholar 

  • Jin C, Zhu J, Li M, Zhao B (2013) A greenhouse study on the dynamics of organic acids in the rhizosphere of wheat and maize. J Arid Land Resour Environ 27:86–91

    Google Scholar 

  • Ju X-T, Xing G-X, Chen X-P, Zhang S-L, Zhang L-J, Liu X-J, Cui Z-L, Yin B, Christie P, Zhu Z-L, Zhang F-S (2009) Reducing environmental risk by improving N management in intensive Chinese agricultural systems. Proc Natl Acad Sci U S A 106:3041–3046

    CAS  Article  Google Scholar 

  • Kandeler E, Poll C, Frankenberger WT, Tabatabai MA (2011) Nitrogen Cycle Enzymes. In: Dick RP (ed) Methods of Soil Enzymology. Soil Science Society of America, Madison, WI, pp 211–245

    Google Scholar 

  • Khan SA, Mulvaney RL, Hoeft RG (2001) A simple soil test for detecting sites that are nonresponsive to nitrogen fertilization. Soil Sci Soc Am J 65:1751–1760

    CAS  Article  Google Scholar 

  • Li S, Liu Y, Wang J, Yang L, Zhang S, Xu C, Ding W (2017) Soil acidification aggravates bacterial wilt in South China. Front Microbiol 8:703

    Article  Google Scholar 

  • Liu L, Kong J, Cui H, Zhang J, Wang F, Cai Z, Huang X (2016) Relationships of decomposability and C/N ratio in different types of organic matter with suppression of Fusarium oxysporum and microbial communities during reductive soil disinfestation. Biol Control 101:103–113

    CAS  Article  Google Scholar 

  • Loeppert RH, Inskeep WP (1996) Iron. In: DL Sparks, AL Page, PA Helmke, RH Loeppert, PN Soltanpour, MA Tabatabai, CT Johnston, ME Sumner (eds) Methods of Soil Analysis Part 3-Chemical Methods. Soil Science Society of America, American Society of Agronomy, Madison, 639–664

  • Meng T, Yang Y, Cai Z, Ma Y (2018) The control of Fusarium oxysporum in soil treated with organic material under anaerobic condition is affected by liming and sulfate content. Biol Fert Soils 54:295–307

    Article  Google Scholar 

  • Momma N (2008) Biological soil disinfestation (BSD) of soilborne pathogens and its possible mechanisms. Jarq-Jpn Agric Res 42:7–12

    CAS  Article  Google Scholar 

  • Momma N, Kobara Y, Momma M (2011) Fe2+ and Mn2+, potential agents to induce suppression of Fusarium oxysporum for biological soil disinfestation. J Gen Plant Pathol 77:331–335

    CAS  Article  Google Scholar 

  • Momma N, Kobara Y, Uematsu S, Kita N, Shinmura A (2013) Development of biological soil disinfestations in Japan. Appl Microbiol Biotechnol 97:3801–3809

    CAS  Article  Google Scholar 

  • Morgunov IG, Kamzolova SV, Dedyukhina EG, Chistyakova TI, Lunina JN, Mironov AA, Stepanova NN, Shemshura ON, Vainshtein MB (2017) Application of organic acids for plant protection against phytopathogens. Appl Microbiol Biotechnol 101:921–932

    CAS  Article  Google Scholar 

  • Nannipieri P, Ascher-Jenull J, Ceccherini MT, Pietramellara G, Renella G, Schloter M (2020) Beyond microbial diversity for predicting soil functions: A mini review. Pedosphere 30:5–17

    Article  Google Scholar 

  • Poret-Peterson AT, Albu S, McClean AE, Kluepfel DA (2019) Shifts in soil bacterial communities as a function of carbon source used during anaerobic soil disinfestation. Front Environ Sci 6:160

    Article  Google Scholar 

  • Poret-Peterson AT, Sayed N, Glyzewski N, Forbes H, Gonzalez-Orta ET, Kluepfel DA (2020) Temporal responses of microbial communities to anaerobic soil disinfestation. Microb Ecol 80:191–201

    CAS  Article  Google Scholar 

  • Posas MB, Toyota K, Islam TMD (2007) Inhibition of bacterial wilt of tomato caused by Ralstonia solanacearum by sugars and amino acids. Microbes Environ 22:290–296

    Article  Google Scholar 

  • Rousk J, Baath E (2007) Fungal and bacterial growth in soil with plant materials of different C/N ratios. FEMS Microbiol Ecol 62:258–267

    CAS  Article  Google Scholar 

  • Shrestha U, Auge RM, Butler DM (2016) A meta-analysis of the impact of anaerobic soil disinfestation on pest suppression and yield of horticultural crops. Front Plant Sci 7:1254

    PubMed  PubMed Central  Google Scholar 

  • Šmilauer P, Lepš J (2014) Multivariate analysis of ecological data using Canoco 5. 2nd edn. Cambridge University Press, Cambridge

  • Strauss SL, Kluepfel DA (2015) Anaerobic soil disinfestation: A chemical-independent approach to pre-plant control of plant pathogens. J Integr Agr 14:2309–2318

    CAS  Article  Google Scholar 

  • Tabatabai MA (1994) Soil Enzymes. In: PS Bottomley, JS Angle, RW Weaver (eds) Methods of Soil Analysis: Part 2-Microbiological and Biochemical Properties. Soil Science Society of America. Madison, 775–833

  • Tenuta M, Lazarovits G (2002) Ammonia and nitrous acid from nitrogenous amendments kill the microsclerotia of Verticillium dahliae Phytopathology 92:255–264

    CAS  Article  Google Scholar 

  • Tian J, Rao S, Gao Y, Lu Y, Cai K (2021) Wheat straw biochar amendment suppresses tomato bacterial wilt caused by Ralstonia solanacearum: potential effects of rhizosphere organic acids and amino acids. J Integr Agric 20:2450–2462

    CAS  Article  Google Scholar 

  • Wang L, Cai K, Chen Y, Wang G (2013) Silicon-mediated tomato resistance against Ralstonia solanacearum is associated with modification of soil microbial community structure and activity. Biol Trace Elem Res 152:275–283

    CAS  Article  Google Scholar 

  • Wang X, Zou C, Gao X, Guan X, Zhang W, Zhang Y, Shi X, Chen X (2018) Nitrous oxide emissions in Chinese vegetable systems: A meta-analysis. Environ Pollut 239:375–383

    CAS  Article  Google Scholar 

  • Weller DM, Raaijmakers JM, Gardener BBM, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40:309–348

    CAS  Article  Google Scholar 

  • Yang J, Jiao Y, Yang WZ, Gu P, Bai SG, Liu LJ (2018) Review of methods for determination of ammonia volatilization in farmland. IOP Conf Ser: Earth Environ Sci 113:012022

  • Yao J, Allen C (2006) Chemotaxis is required for virulence and competitive fitness of the bacterial wilt pathogen Ralstonia solanacearum J Bacteriol 188:3697–3708

    CAS  Article  Google Scholar 

  • Yuliar, Nion YA, Toyota K (2015) Recent trends in control methods for bacterial wilt diseases caused by Ralstonia solanacearum Microbes Environ 30:1–11

    Article  Google Scholar 

  • Zhao J, Mei Z, Zhang X, Xue C, Zhang C, Ma T, Zhang S (2017) Suppression of Fusarium wilt of cucumber by ammonia gas fumigation via reduction of Fusarium population in the field. Sci Rep 7:43103

    CAS  Article  Google Scholar 

Download references

Acknowledgements

The present study was financially supported by grants from the National Natural Science Foundation of China (31870420, 41807084), the Natural Science Foundation of Guangdong Province, China (2017A030313177, 2018A030310214, 2022A1515011034), the Science and Technology Program of Guangdong Province (2015A050502043, 2121A0505030057) and the Basic Research Program of Guangzhou City, China (202102020390).

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Author notes

  1. Yihang Mao and Abdul Hafeez contributed equally.

Authors and Affiliations

  1. Guangdong Provincial Key Laboratory of Eco-Circular Agriculture, South China Agricultural University, Guangzhou, 510642, China

    Yihang Mao, Abdul Hafeez, Taowen Pan, Chaorong Wu, Lei Wang, Kunzheng Cai & Jihui Tian

  2. Key Laboratory of Tropical Agricultural Environment in South China, Ministry of Agriculture, 510642, Guangzhou, China

    Yihang Mao, Abdul Hafeez, Taowen Pan, Chaorong Wu, Lei Wang, Kunzheng Cai & Jihui Tian

  3. College of Natural Resources and Environment, South China Agricultural University, 510642, Guangzhou, China

    Yihang Mao, Abdul Hafeez, Taowen Pan, Chaorong Wu, Lei Wang, Kunzheng Cai & Jihui Tian

  4. Environmental Studies, University of California Santa Cruz, 1156 High Street, Santa Cruz, CA, 95064, USA

    Joji Muramoto & Carol Shennan

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  1. Yihang Mao
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Contributions

Formal analysis and investigation: Yihang Mao, Taowen Pan, Chaorong Wu and Lei Wang; Writing - original draft preparation: Yihang Mao, Abdul Hafeez and Jihui Tian; Writing - review and editing: Taowen Pan, Joji Muramoto, Carol Shennand, Kunzheng Cai, Jihui Tian; Funding acquisition and supervision: Kunzheng Cai and Jihui Tian.

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Correspondence to Kunzheng Cai or Jihui Tian.

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Mao, Y., Hafeez, A., Pan, T. et al. Suppression of tomato bacterial wilt by anaerobic soil disinfestation and associations with production of antagonistic compounds. Plant Soil (2022). https://doi.org/10.1007/s11104-022-05452-y

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Keywords

  • Reductive soil disinfestation
  • Bacterial wilt
  • Organic acid
  • ammonia volatilization